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d825b5b791b541b3a2fd9c796e0a8161_Characteristics and Diagnostic Yield of Pediatric Colonoscopy in Taiwan_10.1016_j.pedneo.2015.01.005.xml
|
Characteristics and Diagnostic Yield of Pediatric Colonoscopy in Taiwan
|
[
"Wu, Chien-Ting",
"Chen, Chih-An",
"Yang, Yao-Jong"
] |
Background
Colonoscopy of the lower gastrointestinal tract has diagnostic and therapeutic value. This retrospective study aimed to investigate the indications, complications, and diagnostic yield of diagnostic colonoscopy among Taiwanese children.
Methods
The application of colonoscopy performed on children aged < 18 years between 1998 and 2010 in a referral tertiary center in Southern Taiwan was reviewed. Data on age, gender, indications, complications, and colonoscopic and final diagnoses were collected and analyzed.
Results
One hundred and ninety-two children with 201 colonoscopies and 27 sigmoidoscopies were enrolled. The rate of successful ileocecal approach was 77.5%. The most common indication was lower gastrointestinal bleeding (LGIB; 53.5%), followed by chronic abdominal pain (20.6%), iron deficiency anemia (IDA; 11.8%), and chronic diarrhea (11.4%). There were 144 patients (75%) with a conclusive diagnosis in their first colonoscopy, including nonspecific colitis (23.4%), polyp (20.4%), and inflammatory bowel disease (8.3%). The diagnostic yields of colonoscopy according to the major indications were 77.3% in LGIB, 68.1% in chronic abdominal pain, 66.7% in IDA, and 79.2% in chronic diarrhea. Among the patients with LGIB, juvenile polyp (26.4%) was the most common etiology. There were no major procedure-related complications.
Conclusion
LGIB is the most common indication for pediatric colonoscopy. Pediatric colonoscopy is most effective in diagnosing pediatric LGIB and chronic diarrhea.
|
1 Introduction Pediatric fiber optic colonoscopy was introduced in the 1970s. Since then, improvements in fiber optic and video technology, conscious sedation, and physicians' experience have led to the establishment of colonoscopy as a procedure for the diagnosis, evaluation, and management of lower gastrointestinal tract disorders in children. Colonoscopy is technically more challenging than esophagogastroduodenoscopy, especially in pediatric patients, due to their poor compliance and cooperation. 1–4 The development of pediatric colonoscopy in Taiwan began in the late 1970s, and both diagnostic and therapeutic colonoscopies are now widely performed by most pediatric gastroenterologists. 5 Despite the generally increased use of colonoscopy in pediatric patients, careful selection of the indications for colonoscopy in these patients can still achieve higher diagnostic yields and prevent complications. The most common indications are unexplained iron deficiency anemia (IDA), lower gastrointestinal bleeding (LGIB), and diarrhea. However, the diagnostic yield varies depending on the indication, with unexplained diarrhea and blood in the stools having the highest diagnostic yield (91–97%). 6 Therapeutic colonoscopy is most frequently applied in children for polypectomy and for bleeding, 7,8 with successful resection rates exceeding 96% for polypectomy. 9,10 2,11,12 With the rapidly increasing number of colorectal polyps, polypectomy has also become the most common endoscopic procedure in adults. Although the potential for malignant change of colorectal polyps in children is rare, symptomatic colorectal polyps are not uncommon, especially in those with LGIB. However, available data regarding the prevalence, clinical features, and significance of colonoscopy in the evaluation of colorectal polyps in children remain limited. This retrospective study aimed to investigate the indications, complications, and diagnostic yield of pediatric colonoscopy, and the prevalence and clinical characteristics of colorectal polyps in children. 13–15 2 Methods 2.1 Participants enrolled, data collected, and definitions The application of diagnostic colonoscopy in consecutive children aged < 18 years between 1998 and 2010 at National Cheng Kung University Hospital, a tertiary referral center in Southern Taiwan, was reviewed. Data were collected from the hospital's electronic database system. Demographic data, indications for colonoscopy, final diagnosis, and complications were recorded and analyzed. A positive diagnostic yield was defined as colonoscopic and/or histologic findings leading to a conclusive diagnosis that corresponded with the symptoms. Nonspecific colitis was defined as colonoscopic features showing erosive or erythematous mucosal lesions combined with lymphocytic infiltration in histologic examinations. Major complications were defined as complications related to the procedure that led to prolonged admission, morbidity, or mortality. The hospital's Ethical Committee approved the study protocol. 2.2 Colonoscopy preparation and procedure Each patient had a bowel preparation of low residue diet for 2 days prior to examination, followed by either oral castor oil (dosage: > 2 years, 5–15 mL; < 2 years, 1–5 mL), and suppository bisacodyl (dosage: > 10 years, 10 mg; < 10 years, 5 mg) on the night before the examination, or oral sodium phosphate (dosage: > 12 years, 20–45 mL; 10–11 years, 10–20 mL; 5–9 years, 5–10 mL) with liquid in the night and on the day before the examination. Bowel-cleansing enemas were also performed on the day of the examination. Intravenous or intramuscular meperidine (dosage: 2 mg/kg, maximum 50 mg) and hyoscine butyl bromide (0.5 mg/kg, maximum 20 mg) were given 30 minutes prior to the examination. Patients who were not cooperative or tolerant during the examination received conscious sedation with intravenous midazolam (single dose 0.2 mg/kg) and propofol (single dose 2.5 mg/kg for induction of anesthesia, with a bolus dose of 5–10 mg if needed). 16 Under conscious sedation, the patients were given oxygen supplementation via nasal cannula and monitored by pulse oximetry. 17,18 All of the colonoscopy procedures were performed by a single pediatric gastrointestinal endoscopist using an Olympus PCF-240L colonoscope (Olympus Corporation, Tokyo, Japan). In neonates or young infants, the Olympus GIF-Q230 gastroscope (Olympus Corporation, Tokyo, Japan) was used instead of a colonoscope. The examinations were performed in the left lateral position. The position of the patient was changed and manual compression of the abdomen was performed when there was difficulty in advancing the colonoscope. If a colorectal polyp was found, it was removed using the forceps or by polypectomy, and the specimen was sent for histologic studies. 3 Results 3.1 Demographic data and indications for examination One hundred and ninety-two children with 201 colonoscopies and 27 rectosigmoidoscopies were enrolled. There were 81 girls and 111 boys, with a mean age of 7.7 ± 5.4 years (range, from 15 days to 18 years). Two or more sequential endoscopies were performed in 22 (11.5%) patients ( Table 1 ), and 65% of the procedures involved conscious sedation. There were no major procedure-related complications in any of the patients. In the first colonoscopies of 169 patients, the cecum was successfully reached in 131 (77.5%) cases, while the terminal ileum was reached in 92 (54.4%) ( Table 1 ). The most common indication for colonoscopy or sigmoidoscopy was LGIB (53.5%), followed by chronic abdominal pain (20.6%), IDA (11.8%), and chronic diarrhea (11.4%) ( Table 2 ). 3.2 Conclusive diagnosis and diagnostic yield Conclusive diagnosis relied on endoscopic imaging and/or histology and 144 patients (75%) had a conclusive diagnosis on their first examination, while 48 had negative findings. The most common conclusive diagnosis was nonspecific colitis (23.4%), followed by colorectal polyp (20.4%), lymphoid hyperplasia (6.3%), Crohn's disease (4.7%), ulcerative colitis (3.6%), and cow's milk protein allergy (3.6%). The diagnostic yield was 77.3% in 110 patients with LGIB and colorectal polyp (26.4%) was the most commonly encountered etiology, followed by nonspecific colitis (22.7%) and inflammatory bowel disease (IBD; 10.9%) ( Table 2 ). Of the 47 patients with chronic abdominal pain, the diagnostic yield was 68.1%, with nonspecific colitis (25.5%) as the most common etiology. In 24 IDA patients, the diagnostic yield was 66.7% and most cases were IBD (25%) or cow's milk allergy (25%). Among the 24 patients with chronic diarrhea, the diagnostic yield was 79.2%, with IBD (29.2%) as the most common etiology. 3.3 Characteristics of colorectal polyps The clinical and colonoscopic characteristics of 39 patients with colorectal polyps revealed a male predominance (2.2:1) and a mean age of 6.1 years ( Table 3 ). Thirty-six (92.3%) of the 39 polyps were solitary, 36 were juvenile polyps, and three were tubular adenoma. The most common location of the polyp was the colon (53.8%) above the rectosigmoid portion, and 74.3% of patients presented with LGIB. All polyps were removed by forceps or polypectomy without significant bleeding or perforation. 4 Discussion Except for data from the Pediatric Endoscopy Database System-Clinical Outcomes Research Initiative, the current report is the largest series of pediatric colonoscopy in the literature in English. Colonoscopy is performed less frequently in children than in adults because of difficulties in preparation and sedation, which are usually needed in children. 6 In the report by Hassall et al, 6 all 113 patients received colonoscopy under either general anesthesia or conscious sedation. By contrast, the present report shows only 65% of the procedures involving conscious sedation. This may be one of the reasons for the slightly lower success rate of reaching the cecum or terminal ileum (77.5%) in the present study compared to the series with full sedation (84–97.6%). 2 Another reason may be that while the pathologic lesions identified in other images were reached, the procedures were terminated in some patients before the endoscope reached the cecum. Although the terminal ileum approach is not necessary in each colonoscopy, previous study revealed that up to 85% of patients with Crohn's disease had a terminal ileum lesion, which was confirmed using colonoscopy and ileum biopsy. 2,3,19 Therefore, if IBD is suspected or there are no lesions in the colon, the ileum intubation is crucial in making a prompt diagnosis. As in other reports, there are no major procedure-related complications in the patients here. 20 Minor complications like cough with transient desaturation, intravenous fluid extravasation, and occasional slight oozing after polypectomy also occurred. 3,7 The most common indication for colonoscopy in this study is LGIB. Chronic abdominal pain, IDA, and chronic diarrhea are also common reasons for pediatric colonoscopy. Moreover, this study highlights a new indication for evaluating the lead points of recurrent intussusception suspected from imaging studies. All (2 lymphomas and 2 polyps) were managed nonsurgically, with good outcomes. 3–5,11 According to the endoscopic features and histology, a conclusive diagnosis has been made in 75% of the patients. As in other reports from Asia, the two most common etiologies are nonspecific colitis (23.4%) and colorectal polyp (20.4%). However, there is a lower rate (8.3%) of IBD in this study than that reported in The Netherlands. 3,7,21 Furthermore, 6.7% of 192 children with indications for colonoscopy have eosinophilic colitis (including cow's milk protein allergy). 14 The diagnostic yield of colonoscopy according to the major indications is 77.3% in LGIB, 68.1% in chronic abdominal pain, 66.7% in IDA, and 79.2% in chronic diarrhea. These results imply that LGIB (including colorectal polyps, nonspecific colitis, and IBD) and chronic diarrhea are alarming events for children who require further lower gastrointestinal investigations. The results also show more cases of colorectal polyps in children undergoing colonoscopy compared to those of a report from the United Kingdom (20.4% vs. 4.0%). Among patients with chronic diarrhea, IBD is the leading etiology. El Mouzan et al 12 reported that pediatric patients with bloody diarrhea had a high colonoscopic yield (91%) compared to those with only chronic diarrhea (43%). 7 In the present study, only two patients with visible blood in their stools were categorized into the chronic diarrhea group. One was diagnosed as pseudomembranous colitis and the other eosinophilic colitis pathologically. 7 In contrast to colonoscopy in adults with unexplained IDA, which is highly recommended, the role of diagnostic colonoscopy in children with IDA is uncertain. Esophagogastroduodenoscopy is generally applied in pediatric patients with unexplained IDA because it is associated with 22 Helicobacter pylori infection. However, in this study, 23 H. pylori infection has been excluded in all of the patients with IDA prior to colonoscopy. The diagnostic yield of colonoscopy among these patients is 66.7%. This indicates that colonoscopy is an appropriate examination for evaluating children with unexplained IDA but without H. pylori infection, especially IBD and cow's milk protein allergy. As in the current report, the reported prevalence of colon polyps in pediatric diagnostic colonoscopy in Asian populations (20.3–20.5%) is higher than that in Western populations (4.0–8.6%). Most reports showed that 80–90% of polyps were located at the rectosigmoid colon. 5,12,15,24 However, in this study, only 43.6% of the polyps are at the rectosigmoid colon, which is similar to the report by Gupta et al. 3,5 Although most pediatric colon polyps are juvenile polyps, some are potentially premalignant. 24 This highlights the importance of colonoscopy rather than sigmoidoscopy for the diagnosis and treatment of pediatric colon polyps. 25 A colonic pathology is not uncommon in pediatric patients. Children presenting with symptoms or signs of lower gastrointestinal disorders should undergo colonoscopy to obtain a definite diagnosis and prompt treatment. Pediatric colonoscopy is a safe and effective procedure to detect pathologic lesions of the lower gastrointestinal tract. Conflicts of interest The authors have no conflicts of interest relevant to this article.
|
[
"SQUIRES",
"HASSALL",
"TAM",
"KALAOUI",
"PARK",
"GILGER",
"ELMOUZAN",
"ELMOUZAN",
"BARNERT",
"NG",
"MUDAWI",
"LATT",
"HYER",
"DERIDDER",
"THAKKAR",
"HUNTER",
"KOH",
"ELITSUR",
"KAWAMITSU",
"BATRES",
"THAPA",
"PEYTREMANNBRIDEVAUX",
"HUANG",
"GUPTA",
"LEE"
] |
a06f37f7790f4ac9aabdb783a16ac922_Upregulation of liver VLDL receptor and FATCD36 expression in LDLR apoB100100 mice fed trans-10cis-1_10.1194_jlr.M600140-JLR200.xml
|
Upregulation of liver VLDL receptor and FAT/CD36 expression in LDLR−/− apoB100/100 mice fed trans-10,cis-12 conjugated linoleic acid
1
|
[
"Degrace, Pascal",
"Moindrot, Bastien",
"Mohamed, Ismaël",
"Gresti, Joseph",
"Du, Zhen-Yu",
"Chardigny, Jean-Michel",
"Sébédio, Jean-Louis",
"Clouet, Pierre"
] |
This study explores the mechanisms responsible for the fatty liver setup in mice fed trans-10,cis-12 conjugated linoleic acid (t10c12 CLA), hypothesizing that an induction of low density lipoprotein receptor (LDLR) expression is associated with lipid accumulation. To this end, the effects of t10c12 CLA treatment on lipid parameters, serum lipoproteins, and expression of liver lipid receptors were measured in LDLR−/− apoB100/100 mice as a model of human familial hypercholesterolemia itself depleted of LDLR. Mice were fed t10c12 CLA over 2 or 4 weeks. We first observed that the treatment induced liver steatosis, even in the absence of LDLR. Mice treated for 2 weeks exhibited hypertriglyceridemia with high levels of VLDL and HDL, whereas a 4 week treatment inversely induced a reduction of serum triglycerides (TGs), essentially through a decrease in VLDL levels. In the absence of LDLR, the mRNA levels of other proteins, such as VLDL receptor, lipoprotein lipase, and fatty acid translocase, usually not expressed in the liver, were upregulated, suggesting their involvement in the steatosis setup and lipoprotein clearance. The data also suggest that the TG-lowering effect induced by t10c12 CLA treatment was attributable to both the reduction of circulating free fatty acids in response to the severe lipoatrophy and the high capacity of liver to clear off plasma lipids.
|
Conjugated linoleic acids (CLAs) refer to a group of dienoic derivatives of linoleic acid. In most feeding studies, CLAs are mainly represented by cis -9, trans -11-C 18:2 , the main natural isomer produced in ruminants, and by trans -10, cis -12-C 18:2 (t10c12 CLA) essentially originating from vegetable oil processes. These isomers of linoleic acid have been shown to exhibit a variety of unique properties such as anticancer ( 1 ), antiatherogenic ( 2 ), and immune response-enhancing ( 3 ) effects in animal models. CLAs have also been reported to reduce total body fat content in mice, rats, and chickens ( 4–6 ). The C57Bl6 mouse is a model largely used to study the biological effects of CLA, to which this strain is very sensitive, and in particular to t10c12 CLA, which was identified recently as the isomer affecting body lipid metabolism ( 7 , 8 ). After a 4 week treatment with t10c12 CLA, C57Bl6 mice exhibit severe lipoatrophy, steatotic liver, hyperinsulinemia, and plasma triglyceride (TG) alteration ( 7 , 9 ). Thus, t10c12 CLA-fed mice constitute an interesting model for the study of steatosis onset in relation to lipid metabolism dysfunctions, nonalcoholic fatty liver disease now being recognized as one of the common features of the metabolic syndrome, with visceral fat obesity, insulin resistance, dyslipidemia, and hypertension ( 10 ). In a previous work, we suggested that a high uptake of plasma lipids by the liver would explain part of the TG accumulation in this organ after t10c12 CLA feeding ( 7 ). As the overexpression of hepatic low density lipoprotein receptor (LDLR) was demonstrated to increase the clearance of apolipoprotein B-100 (apoB-100)-containing lipoproteins in mice ( 11 ), and as CLA treatment was found to induce the expression of LDLR ( 7 ), liver steatosis onset could depend, at least in part, on this lipoprotein receptor. Therefore, in this study, LDLR −/− apoB 100/100 mice, which represent a good model of human familial hypercholesterolemia ( 12 ), were fed t10c12 CLA to induce lipoatrophy to study the consequences on liver and plasma lipid parameters. We particularly focused on the hepatic effects of both the high lipid flux originating from adipose tissue attributable to t10c12 CLA action and on the absence of LDLR in this dyslipidemic model with regard to the expression of other lipid transporters. To address this issue, we also determined the gene expression profile of untreated LDLR −/− apoB 100/100 mice compared with normal wild-type animals. Our results show, first, that LDLR deficiency was unable to prevent the steatosis induced by t10c12 CLA and, second, that other proteins substitute for LDLR in lipoprotein clearance to such an extent that serum TG levels were significantly reduced in these mice usually exhibiting high levels of circulating apoB-100-rich lipoproteins. MATERIALS AND METHODS Animals and treatments Official French regulations (No. 87848) for the use and care of laboratory animals were followed throughout. Control (B6129SF2) and transgenic (B6; 129S-Apobtm2SgyLdlrtm1Her) mice originated from the Jackson Laboratory. Transgenic mice are deficient in LDLR and express only apoB100 (LDLR −/− apoB 100/100 mice). After 1 week of adaptation to the control diet (AO4; Unité d'Appui à la Recherche, Epinay-sur-Orge, France), 7 week old male mice were housed in individual plastic cages. LDLR −/− apoB 100/100 mice were randomly allocated to the control or the CLA diet (n = 5 for each), consisting of a basal diet, whose detailed composition has been described ( 13 ), enriched with 1% C 18:1 n-9 (oleic acid) or t10c12 CLA, both esterified as TG. CLA-fed LDLR −/− apoB 100/100 mice and their corresponding controls were euthanized after 2 or 4 weeks. Wild-type B6129SF2 mice (n = 5), fed only the control diet, were used after 4 weeks. Mice were food-deprived for 4 h before anesthetized with ketamine/xylazine (7.5 mg/100 g body weight) and euthanized. For lipid analysis, liver, heart, gastrocnemius, and blood (collected from the vena cava) were stored at −80°C. Fresh samples of liver were used for immediate FA oxidation measurements on whole liver homogenates and isolated mitochondria. Lipid analysis Total liver, muscle, and heart lipids were extracted according to Folch, Lees, and Sloane Stanley ( 14 ). For liver, total lipids were determined by gravimetry and lipid classes were quantified by the TLC-flame ionization detection method ( 15 ). Phospholipids, cholesteryl esters, and TG were separated by TLC on silica plates (Merck, Darmstadt, Germany). Their constitutive FAs were methylated according to the procedure of Christie, Sebedio, and Juaneda ( 16 ) and analyzed by gas-liquid chromatography as described previously ( 17 ). For skeletal muscle and heart, aliquots of total lipid extracts were resuspended in a solution of Triton X-100 as described previously ( 18 ). Then, TG contents were measured using a commercial kit from Roche Diagnostics Corp. (Indianapolis, IN). Commercial kits were also used for the determination of serum TG and glycerol concentrations (Sigma Diagnostics, Saint-Quentin-Fallavier, France) and of serum free FA (Roche Diagnostics Corp.). Serum lipoprotein analysis Serum lipoprotein analysis was performed by fast-performance liquid chromatography, and total cholesterol was quantified with an inline detection system as described previously ( 19 ). Liver lipolytic activity The procedure used was adapted from that of Iverius and Ostlund-Lindqvist ( 20 ). Lipolytic activity determined on tissue homogenates corresponding to amounts of [ 3 H]oleic acid released from radiolabeled triolein as described previously ( 7 ). Carnitine palmitoyltransferase I activity and palmitate oxidation rate Measurements of carnitine palmitoyltransferase I (CPT I) activity and palmitate oxidation rates were performed as described previously ( 13 ). FA oxidation was measured with whole liver homogenates using two media, the first allowing mitochondrial and peroxisomal activities to occur, the second allowing the peroxisomal activity only ( 21 ), and with liver mitochondrial fractions. Protein concentrations of mitochondrial fractions were measured using the bicinchoninic acid procedure (Sigma) ( 22 ). Western blot analysis of the very low density lipoprotein receptor Approximately 100 mg of frozen liver was quickly homogenized with a mini-beadbeater (BioSpec Products, Inc., Bartlesville, OK) in 10 volumes of a 20 mM Tris buffer containing sucrose (0.2 M), MgCl 2 (2 mM), pepstatin A (1.46 μM), leupeptin (10 μM), aprotinin (0.035 TIU/l), and E64 (1.4 μM). After centrifugation of homogenates at 12,000 g for10 min, supernatants were half-diluted in Laemmli buffer (Bio-Rad S.A., Ivry-sur-Seine, France) ( 23 ) without boiling, and aliquots were size-fractionated on a 7% SDS-polyacrylamide gel using a Mini-Protean 3 electrophoresis cell (Bio-Rad) at 200 V for ∼70 min at room temperature. After electrophoresis, proteins were transferred to a nitrocellulose membrane (Hybond-ECL; Amersham Biosciences, Saclay, France) at 140 V for 1.5 h. For immunodetection, the blots were incubated overnight in TBST [10 mM Tris, 0.15 M NaCl, and 0.05% (v/v) Tween-20] plus 5% (w/v) BSA, for 1 h in TBST, 2% BSA, plus 0.2 μg/ml of a goat anti-mouse VLDL receptor antibody (R&D Systems, Abingdon, UK), and then for 1 h in TBST, 2% BSA, plus a 1:10,000 dilution of rabbit anti-goat IgG peroxidase conjugate antibody (Sigma). The blots were developed with chemiluminescent reagents (ECL; Amersham Biosciences) and subjected to autoradiography. The membrane was stripped using Restore Western Blot Stripping Buffer (Pierce, Rockford, IL) and reprobed in the same conditions with a mouse anti-β-actin antibody and an anti-mouse IgG peroxidase conjugate antibody (Sigma) for standardization. Spot intensities were determined by densitometric analysis with a gel documentation system (Gel Doc 2000) equipped with Quantity One software (Bio-Rad). Protein concentrations of supernatants were measured by the bicinchoninic acid procedure after trichloroacetic acid precipitation to eliminate incompatible substances. Gene expression Total mRNA was extracted from liver by the Tri-Reagent method adapted from the procedure of Chomczynski and Sacchi ( 24 ). Tri-Reagent was provided by Euromedex (Souffelweyersheim, France). Total mRNA were reverse-transcripted using the Iscript cDNA kit (Bio-Rad). Real-time PCR was performed as described previously ( 19 ). Primer pairs were designed using Primers! software and were synthesized by MWG-Biotech AG (Ebersberg, Germany). The sequences of the forward and reverse primers used are as follows: 5′-aattagtagaaccgggccac-3′ and 5′-ccaactcccaggtacaatca-3′, respectively, for fatty acid translocase (FAT/CD36); 5′-ctaaggacccctgaagacaca-3′ and 5′-tctcatacattcccgttaccgt-3′ for LPL; 5′-gtgaatgtggggttagtggac-3′ and 5′-acttcgcagattcctccagc-3′ for HL; 5′-gaccgactggcgaacaaat-3′ and 5′-ctgggtgttggtcctctgta-3′ for low density lipoprotein receptor-related protein (LRP); 5′-agcaccacagatcaatgacc-3′ and 5′-ctctcgtccattttcttcgaga-3′ for very low density lipoprotein receptor (VLDLR); 5′-tcccttcgtgcattttctca-3′ and 5′-gttcatcccaacaaacagg-3′ for scavenger receptor class B type I (SR-BI); and 5′-aatcgtgcgtgacatcaaag-3′ and 5′-gaaaagagcctcagggcat-3′ for β-actin. Statistics Differences in mean values between groups were tested by one-way ANOVA. Significant differences between means were tested by Student's t -test for an independent variable. When variances were unequal, means were tested by the Kruskal-Wallis nonparametric test. RESULTS Effects of t10c12 CLA feeding on body, liver, and serum parameters in LDLR −/− apoB 100/100 mice Table 1 shows that dietary t10c12 CLA did not affect body weights of LDLR −/− apoB 100/100 mice for the two durations of treatment. The drastic reductions of epididymal adipose tissue weights and concomitant liver steatosis usually found in wild-type mice fed t10c12 CLA were also observed in the transgenic model. After 2 weeks of CLA feeding, adipose tissue and liver relative weights were already markedly altered (−62% and +56%, respectively), these effects being even more pronounced after 4 weeks (−82% and +97%, respectively) ( Table 1 ). Liver TG content increased with treatment duration, and the TG enrichment found in mice fed t10c12 CLA for 4 weeks was even greater than that measured under the same experimental conditions with wild-type mice [13-fold vs. 7.5-fold ( 7 ), respectively]. It is worth noting that the t10c12 CLA treatment also increased liver cholesteryl ester contents but did not affect free cholesterol contents. To determine whether lipid accumulation occurred in tissues other than liver, the TG contents of heart and skeletal muscle were measured. Unlike the liver, heart and muscle did not accumulate TG in response to CLA feeding, with muscle TG levels actually being reduced by 6-fold. In LDLR −/− apoB 100/100 mice, as serum lipid parameters are modified with aging, data from control and CLA-fed mice were compared for the same treatment duration. Indeed, Table 1 shows that the effect of t10c12 CLA on serum TG levels was dependent on the duration of treatment, because TGs were increased after 2 weeks and decreased after 4 weeks, relative to the control series. Levels of total cholesterol, free FA, or glycerol in serum were unaltered after 2 weeks of treatment but were decreased significantly when t10c12 CLA was administered for 4 weeks. Lipoprotein profile analysis ( Fig. 1 ) indicates that VLDL-cholesterol and HDL-cholesterol levels were increased in the serum of mice fed t10c12 CLA for 2 weeks (+165% and +22%, respectively), whereas LDL-cholesterol was decreased slightly, but not significantly. Additionally, when mice were fed for 4 weeks, cholesterol levels were decreased in all fractions, particularly in apoB-100 lipoproteins (VLDL-cholesterol, −78%; LDL-cholesterol, −41%; HDL-cholesterol, −26%, relative to controls). Effects of t10c12 CLA feeding on liver FA oxidation in LDLR −/− apoB 100/100 mice Administration of t10c12 CLA improved both peroxisomal and mitochondrial palmitate oxidation rates as measured using liver homogenates after both 2 and 4 weeks of treatment ( Table 2 ). Similarly, carnitine-dependent palmitate oxidation rates measured using isolated mitochondria were also increased, as were CPT I activities in the t10c12 CLA series ( Table 2 ). mRNA expression of proteins involved in liver lipid uptake in LDLR −/− apoB 100/100 mice compared with wild-type mice The impact of the absence of LDLR on the mRNA expression of some proteins involved in lipid uptake (HL, LPL, SR-BI, LRP, VLDLR, FAT/CD36) was estimated in LDLR −/− apoB 100/100 mice in comparison with wild-type mice ( Fig. 2 ). The data indicate that the liver of control transgenic mice overexpressed LPL, FAT/CD36, and VLDLR, which are usually poorly expressed in this organ. In these mice, mRNA levels of HL and two other potential candidates for lipoprotein transport, SR-BI and LRP, were not different between the two genotypes. Effects of t10c12 CLA feeding on the mRNA expression of proteins involved in liver lipid uptake in LDLR −/− apoB 100/100 mice The mechanisms of the steatosis setup in LDLR −/− apoB 100/100 mice fed t10c12 CLA, despite the absence of LDLR, were investigated through the estimation of mRNA levels of enzymes and receptors involved in plasma FA or lipoprotein uptake (SR-BI, LRP, HL, VLDLR and FAT/CD36). Dietary t10c12 CLA decreased mRNA expression of liver HL at both 2 and 4 weeks and increased that of LPL at 4 weeks ( Fig. 3 ). Among the lipoprotein receptors studied, VLDLR was upregulated in the two CLA series, whereas mRNA levels of LRP and SR-BI were significantly upregulated and downregulated, respectively, but only after 4 weeks of CLA treatment. Feeding t10c12 CLA also strongly increased mRNA levels of FAT/CD36, which is usually poorly expressed in the liver, after 2 or 4 weeks of treatment. Liver VLDLR protein levels and lipolytic activity in LDLR −/− apoB 100/100 mice The apparent inductions of mRNA levels of VLDLR and LPL prompted us to study their effects on protein levels and catalytic activity, respectively. Figure 4 indicates that VLDLR protein levels were induced concomitant with mRNA levels. As the regulation of LPL may also occur at the posttranslational level ( 25 ), we measured the actual lipolytic activity of liver extracts. The results presented in Fig. 5 indicate that the liver capacities to hydrolyze TG were greater in LDLR −/− apoB 100/100 mice fed t10c12 CLA for 4 weeks than in control transgenic mice. DISCUSSION In wild-type mice, t10c12 CLA feeding induced severe lipoatrophy with concomitant liver steatosis, and we previously showed that mRNA levels of LDLR were induced, suggesting an increase in lipoprotein uptake by hepatocytes ( 7 ). In this study, the fact that liver TG accumulation was found even in the absence of LDLR raises the question of how hepatocytes manage to face the high flux of lipids that were not stored any longer in adipose tissues of t10c12 CLA-fed mice. Because the liver steatosis seems to be related to lipoatrophy, one could think that hepatocyte TG accumulation did not result from a direct action of t10c12 CLA on liver cells but rather as a consequence of mechanisms altering the adipose tissue. Liver steatosis may also originate from a reduction of lipoprotein secretion rates, from an inhibition of FA β-oxidation, from high rates of de novo lipogenesis, and/or from high lipid uptake. Feeding mice with t10c12 CLA did not reduce liver lipoprotein secretion ( 7 ) or FA oxidation and CPT I activities (this study). De novo lipogenesis might be stimulated by t10c12 CLA feeding, owing to the greater [saturated + monounsaturated]/[polyunsaturated] ratios found in liver lipids of LDLR −/− apoB 100/100 -treated mice than in those of control mice (i.e., 22.3 vs. 5.62, respectively; data not shown). Indeed, in a recent study, it was hypothesized that the conversion of excess glucose to FA and the storage as TG in the liver, rather than in adipose tissue, could be the mechanism leading to liver fat accumulation ( 9 ). Therefore, the data presented here also support the conclusion that lipids diverted from adipose tissues, and available for other organs such as the liver, might contribute to a large extent to hepatic lipid accumulation. Consistent with this hypothesis, we did not observe any lipid accumulation in the other two lipid-utilizing tissues, heart and muscle, suggesting that the liver could be the main acceptor of plasma lipids in CLA-fed mice. Gene expression analysis of control LDLR −/− apoB 100/100 mice compared with wild-type mice indicated that hepatocytes of LDLR-deficient mice overexpressed other genes in response to high levels of TG-rich lipoproteins. Interestingly, LPL, FAT/CD36, and VLDLR, which are usually poorly expressed in liver ( 26–28 ), were induced. Under normal conditions, VLDLR is known to participate in the clearance of VLDL mediated by peripheral organs actively using fat, such as heart or adipose tissue, but not the liver ( 29 ). Nevertheless, it has been demonstrated that the induction of hepatic expression of VLDLR using adenoviral vectors improved lipoprotein clearance ( 30 , 31 ). In this way, in the absence of LDLR, the upregulation of VLDLR mRNA and protein levels observed in the liver of LDLR −/− apoB 100/100 mice compared with wild-type mice strongly suggests that VLDLR is an effective surrogate receptor for the clearance of lipoproteins. A possible mechanism to explain the effect of VLDLR on lipoproteins has been proposed ( 32 ). VLDLR would facilitate the hydrolysis rather than the internalization of particles binding lipoproteins by maintaining them in close interaction with LPL. In our study, the concomitant upregulation of VLDLR and LPL supports this concept, and the increase in FAT/CD36 mRNA levels also supports the possible involvement of this transporter in the uptake of FAs released. Some other studies also suggest close relationships between FAT/CD36 and LPL ( 33 ) and similarly between VLDLR and LPL ( 34 ). Nevertheless, as far as we are aware, this is the first study to report a concomitant induction of the expression of VLDLR, LPL and FAT/CD36 in liver, which suggests a functional cooperation of these proteins to face the lipoprotein abundance. LPL and FAT/CD36 are peroxisome proliferator-activated receptor γ-responsive genes ( 35 ), and recent studies have established a role for hepatic peroxisome proliferator-activated receptor γ in the development and maintenance of liver steatosis ( 36 , 37 ). Therefore, the induction of FAT/CD36 and LPL could be related to the greater delivery of FA to liver cells. This seems to apply particularly to FAT/CD36, whose mRNA levels increased concomitantly with liver TG infiltration ( Fig. 6 ). Interestingly, the comparison of gene expression between wild-type and LDLR −/− apoB 100/100 mice indicates that LRP mRNA levels were comparable, which does not ascribe any apparent role for LRP in the metabolism of apoB-100-containing lipoproteins, even in the absence of LDLR, as was reported previously ( 38 ). However, mRNA levels of LRP increased after 4 weeks of t10c12 CLA treatment, suggesting that LRP stimulation could be secondary to the establishment of CLA-induced hyperinsulinemia ( 9 ), as has been demonstrated in adipocytes ( 39 ), and this receptor likely also participates in the clearance of lipoproteins. Surprisingly, mRNA levels of HL, which could also provide an alternative clearance pathway for apoB-100-containing lipoproteins independent of LDLR ( 40 ), were not induced in LDLR −/− apoB 100/100 mice and even decreased after t10c12 CLA feeding. This supports the possibility that HL would be inversely regulated by the cholesterol supply ( 41 ). The same hypothesis could be retained to explain the SR-BI downregulation, because convergent arguments support the view that HL and SR-BI would be coexpressed to exert coordinated functions in cell cholesterol homeostasis ( 42 ). According to our data, the overexpression of VLDLR, LPL, and FAT/CD36 observed in LDLR −/− apoB 100/100 mice after 4 weeks of CLA feeding accelerated liver lipoprotein clearance to such an extent that the increased serum TG levels observed after 2 weeks of CLA feeding were lower than in controls. It is worth noting that this TG lowering coincides with the nearly complete absence of adipose tissue. Under these conditions, the release of free FA from adipose tissue was necessarily decreased, reducing lipid flux to the liver and the subsequent VLDL secretion rates compared with the 2 week series. On the whole, we suggest that the t10c12 CLA-dependent TG-lowering effect was attributable to both the reduction of a source of FA for liver lipoprotein synthesis and the high capacity of liver to clear off plasma lipids. It is now well established that liver LDLR activity constitutes a key factor for the regulation of apoB-containing lipoproteins ( 43 , 44 ). Therefore, this study provides evidence that, in the absence of LDLR, some efficient alternative regulatory mechanisms also occur (e.g., see control LDLR −/− apoB 100/100 vs. wild-type mice) with convenient upregulation when the fat storage is defective in adipose tissue (e.g., after t10c12 CLA feeding). Acknowledgments The authors thank Mrs. Legendre for fast-performance liquid chromatography analysis and helpful discussions and Mrs. Baudoin for figure construction and typing of the manuscript. This work was supported by grants from the Ministère de la Recherche et de la Technologie and the Région Bourgogne (Dijon, France).
|
[
"FIELD",
"MCLEOD",
"MILLER",
"DELANY",
"PARK",
"WANG",
"DEGRACE",
"PARK",
"IDE",
"ANGULO",
"MURAYAMA",
"SANAN",
"DEGRACE",
"FOLCH",
"MORRISON",
"CHRISTIE",
"SEBEDIO",
"LUND",
"DEGRACE",
"IVERIUS",
"VEERKAMP",
"SMITH",
"LAEMMLI",
"CHOMCZYNSKI",
"DOOLITTLE",
"ABUMRAD",
"KIRCHGESSNER",
"OKA",
"TAKAHASHI",
"CHEN",
"OKA",
"TACKEN",
"FEBBRAIO",
"YAGYU",
"SCHOONJANS",
"INOUE",
"MEMON",
"VENIANT",
"DESCAMPS",
"DICHEK",
"PERRET",
"ACTON",
"HORTON",
"TWISK"
] |
1715a9d0da5a4dffb49feb1967c2bc96_Examining maternal beliefs and human papillomavirus vaccine uptake among male and female children in_10.1016_j.pvr.2016.02.002.xml
|
Examining maternal beliefs and human papillomavirus vaccine uptake among male and female children in low-income families
|
[
"Fuchs, Erika L.",
"Rahman, Mahbubur",
"Berenson, Abbey B."
] |
Purpose
This study examines within-family differences in the uptake of the HPV vaccine and HPV-related beliefs by children׳s sex.
Methods
From a 2011–2013 survey of mothers of children aged 9–17 years in Texas, mothers with both male and female children (n=350) were selected.
Results
Mothers were more likely to report having initiated and completed HPV vaccination for their daughters than sons. Mothers did not express differences by children׳s sex in HPV-related beliefs. Among those who had not completely vaccinated either child, mothers were more likely to report they wanted their daughters compared to sons vaccinated and were more likely to report feeling confident they could get their daughters vaccinated than their sons.
Conclusion
In this population, mothers were more likely to report HPV vaccination of and motivation to vaccinate daughters compared to sons, although maternal beliefs about HPV did not differ by children׳s sex.
|
1 Introduction The human papillomavirus (HPV) is responsible for approximately 18,000 cancers among females and 8000 cancers among males per year in the United States [1] . HPV vaccination has the potential to prevent the majority of HPV-related cancers and genital warts. While the Advisory Committee on Immunization Practices recommends that males and females receive routine HPV vaccination beginning at 11 or 12 years of age [2] , recent estimates from the National Immunization Survey – Teen of the receipt of ≥1 dose were 60.0% in adolescent females and 41.7% in adolescent males [3] . Thus far, interventions aiming to increase HPV vaccination, have had limited success, with mixed results found in two recent reviews [4,5] . Studies have identified differences in barriers to HPV vaccination of sons compared to daughters, including differences in provider recommendation, concerns about safety, and parents not knowing that boys could get the vaccine [6] . Though studies have examined within-family differences in HPV vaccination intention by children׳s sex [7] , no studies have reported on within-family differences in HPV-related beliefs by children׳s sex. The aim of this study was to examine within-family differences by children׳s sex in HPV vaccine uptake and HPV-related beliefs. 2 Methods Between September 2011 and October 2013, women with ≥1 child aged 9–17 years were identified through review of the daily census and approached at four reproductive health clinics operated by the University of Texas Medical Branch (UTMB) to participate in a survey on HPV vaccination. Eligible participants were invited to complete a self-administered survey, available in either English or Spanish, and were reimbursed $5 for their time and effort. The UTMB Institutional Review Board approved this study. Of the 1436 women who met eligibility criteria, 1392 (97%) participated and 44 (3%) declined [8] . A subset of the original study, mothers who had both a son and a daughter 9–17 years old ( n =350), were included in these analyses. Participants responded to questions regarding the HPV vaccine separately for their oldest daughter and oldest son in the 9–17 years age range. Mothers were asked whether their daughter/son had completed the HPV vaccine series, had started (but not completed) the series, had scheduled an appointment to receive it, or had not received any doses. Dichotomous variables were created for initiation (≥1 dose received) and completion (≥3 doses) of the vaccine series. Mothers stated their agreement with statements about their beliefs beginning with, “If my daughter/son gets HPV,” and ending with, “it could harm her/his future health,” “it could harm her/his future relationship with her/his partner,” and, “I will be devastated.” Response options were dichotomized with those who reported they strongly disagreed, disagreed, or were neutral versus those who reported they agreed or strongly agreed. Mothers also responded to the following question on a 0–100% Likert scale with eleven points, “If your 9–17 year old daughter/son does NOT get Gardasil, what are the chances that she/he will contract HPV?” A similar question was asked about their child developing genital warts. Response options were dichotomized with those reporting 0% versus >0%. Mothers also were queried, “I want my daughter/son vaccinated against the human papillomavirus (HPV) within the next year,” and, “I feel confident that I could get Gardasil for my daughter/son.” Response options were dichotomized with those who reported they strongly disagreed, disagreed, or were neutral versus those who reported they agreed or strongly agreed, while mothers with one or both children having completed the vaccine series were excluded from analysis. McNemar׳s chi-squared tests for paired samples were used to examine marginal homogeneity across children׳s sex in maternal beliefs and children׳s HPV vaccination uptake. Statistical significance was assessed at the α =0.05 level. All analyses were performed using Stata Version 14.0 [9] . 3 Results A total of 350 mothers indicated they had both a daughter and a son between 9–17 years of age. Most mothers were between 30 and 39 years of age, Hispanic, and married or cohabitating ( Table 1 ). Mothers were more likely to report their daughters compared to sons had initiated the series and completed it, but overall vaccination was low, with 72.3% reporting no HPV vaccination for either child ( Table 2 ). There were no differences by children׳s sex in mothers׳ beliefs about HPV, perceived risk of their children contracting HPV, or perceived risk of their children developing genital warts. Among those who had not yet completely vaccinated either child ( n =277), mothers were more likely to report they wanted their daughters compared to sons vaccinated in the next year ( Table 2 ). Mothers were also more likely to report feeling confident they could get their daughters vaccinated than their sons. 4 Conclusions/discussion In this population, HPV vaccine uptake differed by children׳s sex, but maternal beliefs about HPV by children׳s sex were similar. These results suggest beliefs may not be driving sex differences in HPV vaccination. Mothers were more likely to report they wanted their daughters vaccinated than their sons and were more likely to report feeling confident they could get their daughters vaccinated, despite similar perceptions of risk. Since some physicians report a preference to vaccinate girls [10] , associations between confidence in getting children vaccinated by sex and provider recommendation should be further explored. This study has several strengths and limitations. While a strength of this study was the inclusion of a diverse, low-income population, the small sample size limited our ability to conduct multivariate analyses. We focused on views and behaviors that differ by children׳s sex within a family, essentially controlling for maternal characteristics, though reliance on maternal report of children׳s HPV vaccination is subject to recall bias. The survey used in this study had not been validated. Mothers did not report different perceptions about how HPV would impact their sons compared to daughters, yet were less likely to vaccinate sons. This may lead to male adolescents being exposed to vaccine-preventable strains of HPV prior to initiating the series. Future interventions should address the disparity in uptake by ensuring parents receive both adequate information about HPV vaccination and equal access to the vaccine for their sons and daughters. Disclaimer This work reflects the opinions of the authors and does not represent the opinions or influences of the National Institutes of Health. Conflict of interest statement The authors declare that there are no conflicts of interest. Acknowledgments Federal support for this study was provided by an institutional training grant ( T32HD055163 : PI AB Berenson) from the Eunice Kennedy Shriver National Institute of Child Health and Human Development to Dr. Fuchs as a postdoctoral fellow.
|
[
"CENTERSFORDISEASECONTROLANDPREVENTION",
"PETROSKY",
"REAGANSTEINER",
"FU",
"NICCOLAI",
"HOLMAN",
"REITER",
"GROSS",
"ALLISON"
] |
9bce4d1e96ec4fe0a99cdaa7d6fce8b4_Microbiota composition data for wild and captive bluestreak cleaner wrasse Labroides dimidiatus Vale_10.1016_j.dib.2020.106120.xml
|
Microbiota composition data for wild and captive bluestreak cleaner wrasse Labroides dimidiatus (Valenciennes, 1839)
|
[
"Okomoda, Victor Tosin",
"Nurul, Ashyikin Noor Ahmad",
"Danish-Daniel, Abdullah Muhd",
"Oladimeji, Abraham Sunday",
"Abol-Munafi, Ambok Bolong",
"Alabi, Korede Isaiah",
"Nur, Asma Ariffin"
] |
The Labroides dimidiatus is known as the “doctor fish” because of its role in removing parasites and infectious pathogens from the body of other fishes. This important role played both in wild and captive conditions could represent a novel form of parasitic transmission process mediated by the cleaning activity of the fish. Yet, there is a paucity of data on the microflora associated with this fish which is important for tracking disease infection and generally monitoring the health status of the fish. This article, therefore, represents the first dataset for the microbiota composition of wild and captive L. dimidiatus. Wild fish samples and carriage water were gotten in Terengganu Malaysia around the corals of the Karah Island. The captive sample, however, was obtained from well-known ornamental fish suppliers in Terengganu Malaysia. Thereafter, bacteria present on the skin, in the stomach and the aquarium water were enumerated using culture-independent approaches and Next Generation Sequencing (NGS) technology. Data obtained from the three metagenomic libraries using NGS analysis gave 1,426,740 amplicon sequence reads which are composed of 508 operational taxonomic units (OTUs) for wild samples and 3,238,564 valid reads and 828 OTUs for captive samples. All sequence reads were deposited in the GeneBank (Accession numbers SAMN14260247, SAMN14260248, SAMN14260249, SAMN14260250, SAMN14260251, and SAMN14260252). The dataset presented is associated with the research article “16S rDNA-Based Metagenomic Analysis of Microbial Communities Associated with Wild Labroides dimidiatus From Karah Island, Terengganu, Malaysia” [1]. The microbiota data presented in this article can be used to monitor the health and wellbeing of the ornamental fish, especially under captivity, hence preventing possible cross-infection.
|
Specifications Table Subject Biological Science Specific subject area Aquatic Science Type of data Figures and Tables How data were acquired DNA extraction and sequencing Microsoft Excel software for computation of bacterial composition Data format Raw and Analyzed Parameters for data collection Fishes for the study had no physical abnormality or showed signs of stress. Description of data collection In this data article, DNA extraction was done from samples of the skin, gut, and carriage water samples collected from the Labroides dimidiatus fish gotten from both wild and captive environments. The 16S rRNA gene was obtained from the samples, amplified, sequenced, and deposited in the GeneBank. Data source location Institution: Universiti Malaysia Terengganu City/Town/Region: Terengganu Country: Malaysia Data accessibility Deposited in the GeneBank (Accession numbers SAMN14260247, SAMN14260248, SAMN14260249, SAMN14260250, SAMN14260251, and SAMN14260252) and With the article Related research article A.N.A., Nurul, A., Muhd Danish-Daniel, V.T., Okomoda, A. A. Nur, 2019. 16S rDNA-Based Metagenomic Analysis of Microbial Communities Associated with Wild Labroides dimidiatus From Karah Island, Terengganu, Malaysia. Biotechnology Reports. 21: e00303. https://doi.org/10.1016/j.btre.2019.e00303 [1] Value of the Data • Microbiota associated with Labroides dimidiatus was presented for the very first time. • Data can be used by ornamental fish hobbyists and other scientists working in the area of fish microbiota especially as it relates to ornamental fishes. • The data is a reference for future studies and useful for comparison with the microbiota of other ornamental fishes obtained from the wild or maintained in captivity. • Data can assist in the monitoring of the health status of the fish as any substantial variation in the structure as well as the abundance of the bacteria presented in this research can be used as an early sign for disease infection in the species (especially under captivity). • The analysis of the data as given in the Microsoft excel can serve as a guide for future studies in, processing data for presentation and publication. 1 Data Description The raw data deposited in the GeneBank represent the sequence reads of the bacterial from the fish skin (SAMN14260247), stomach (SAMN14260248) and carriage water (SAMN14260249) in captivity as well as those from the wild (SAMN14260250, SAMN14260251, and SAMN14260252 respectively). Data presented in the Microsoft excel (Filename: Chart in Microbial of Labroides dimidiatus ) are the various representations of the compositions in graphs. The percentage of the bacterial phyla associated with L. dimidiatus in both environments is presented in Table 1 , while the relative abundance of all the bacterial phyla is presented in Figure 1 . The bacterial phyla abundance as obtained in the captive and wild environment is as presented in Figs. 2 and 3 respectively. Also, Fig. 4 denotes the vein diagram of numbers of shared and exclusive bacterial families observed in the captive and wild samples of L. dimidiatus. Lastly, the standard Illumina forward and reverse primers used for this research are presented in Table 2 . 2 Experimental Design, Materials and Methods L. dimidiatus samples with a weight range of 0.5 and 2.8 g were obtained from Terengganu Malaysia. The wild samples were gotten from the coral of the Karah Island while captive samples were obtained from well-known ornamental fish suppliers in Terengganu who had also obtained it from the wild and had maintained them in the aquarium for a month. For the water samples, the collection was done for the ocean and aquarium water in sterilized blue cap bottles (1 L volume), placed on ice [2] . The fish and the carriage water were subsequently taken to the AQUATROP Laboratory for further analysis. In the laboratory, ten healthy fish were killed by pitching after been appropriately tranquilized with tricaine methane sulphonate (MS222) at 150 mg/1 solutions [3] . Skin mucus samples were obtained by dorsolaterally scraping the surface of the dead specimens using an already sterile scalpel [1] . The samples were then processed using the method by Balcázar et al. [4] before storage at −80 °C for further analysis. Also, the same technique used by Balcázar et al. [4] was adopted for gut sample collection, processing, and storage for analysis. The DNA from the skin and gut samples were extracted using a commercial DNA kit (NucleoSpin® Tissue Kit Machery-Nagel, Germany) without any modification of the manufacturer's protocol. However, water samples were first conditioned according to the method previously used by Wolf et al. [5] before DNA was extracted from them. The amplification of the 16S rRNA gene was achieved using the universal bacteria primer set 63F (5‟-CAGGCCTAACACATGCAAGTC-3‟) and 1389R (5‟-ACGGGCGGTGTGTACAAG-3‟) reported by Hongo et al. [6] following the PCR reaction volume and protocol earlier used by Nurul et al. [1] . In line with the method previously used by Nurul et al., [1] , a second PCR was done using 1 μL of the amplicon. Thereafter, the V3 hypervariable region of the 16S rRNA genes was selected according to Bartram et al. [7] . The V3 region amplification of the 16S rRNA gene was then done with the 341F and 518R universal primers reported by Muyzer and de Waal [8] . All the primers used for the construction of the Illumina library are presented in Table 1 . Because the V3 specific priming regions were complementary to the standard Illumina primers, they were composed of a 6-bp indexing sequence to allow for multiplexing. The amplification of the primers was then designed with Illumina adapters. PCR amplification condition was according to an earlier report by Nurul et al. [1] . Using gel electrophoresis of 2% agarose, the PCR products were viewed to see if the desired size was gotten and clean-up was done accordingly. Adapter sequences necessary for binding to the flow cell were denoted by Lowercase letters, while binding sites for the Illumina sequencing primers are the underlined lowercases. Bold uppercase, however, highlighted the indexed sequences while the V3 region primers for the 341F and 518R primers are presented in regular uppercases [7] . The generated “reads” were processed according to the method adopted by Schloss et al. [9] (i.e. trimming and assembling using the software “Mothur”). Overlapping regions within Illumina paired-end reads were aligned to generate “contigs”. The paired-end sequences of a mismatch and those with ambiguous base calls were not used, hence discarded. Thereafter, based on naïve Bayesian classification (RDP classifier) followed by Wang et al. [10] , the sequences were assigned taxonomic affiliations. The sequences were then assigned to operational taxonomic units of six samples of the 16S rRNA gene fragments shortly after trimming, screening, and alignment of the same. Thereafter they were connected to the server to download the fastq file. A tab-delimited “oligos” file containing the primer and barcode information was created. Then, the data were analyzed using the Greengenes reference files obtained from the Mothur website. Following the method according to Cole et al. [11] , a pairwise similarity cutoff of 97% using the Ribosomal Database Project pyrosequencing pipeline was used to define the operational taxonomic units (OTU) of the bacteria colonies. All the sequence reads generated were deposited in the GeneBank with Accession numbers SAMN14260247, SAMN14260248, SAMN14260249, SAMN14260250, SAMN14260251, and SAMN14260252. Ethics Statement The approval for the experimental protocols used for this research was obtained from the Universiti Malaysia Terengganu committee on research. This includes and not limited to methods used for the care and use of animal specimens which were aligned with guidelines of international, national, and institutional standards. Declaration of Competing Interest The authors wish to declare that there are no conflicts of interest whatsoever, be it financial or personal. Hence, none of this was perceived to have influenced the outcome of the research reported herein in this data article. Acknowledgments The authors owe a debt of gratitude to the management and staff of the AQUATROP as well as the School of Fisheries and Food Sciences, University Malaysia Terengganu in whose facility the data presented in this research was obtained. We are also grateful to Miss Nor Aiffa Wahyu Abu Bakar and appreciate the assistant rendered by the staff of Net loft during the sample collection for this research. The financing of this research was made possible by a grant obtained from the Ministry of Higher Education Malaysia and it was utilized by Ashyikin Noor Ahmad Nurul as part of her MSc. thesis. Supplementary materials Supplementary material associated with this article can be found, in the online version, at doi:10.1016/j.dib.2020.106120 . Appendix Supplementary materials Image, application 1 Image, application 2
|
[
"NURUL",
"SMITH",
"WAGNER",
"BALCAZAR",
"WOLF",
"HONGO",
"BARTRAM",
"MUYZER",
"SCHLOSS",
"WANG",
"COLE"
] |
893deefc46c24ae1ae5aa8f513166638_Evaluation of optimum adsorption conditions for Ni II and Cd II removal from aqueous solution by mod_10.1016_j.bjbas.2016.03.001.xml
|
Evaluation of optimum adsorption conditions for Ni (II) and Cd (II) removal from aqueous solution by modified plantain peels (MPP)
|
[
"Garba, Zaharaddeen N.",
"Ugbaga, Nkole I.",
"Abdullahi, Amina K."
] |
The most ideal conditions for the adsorption of Ni (II) and Cd (II) ions onto modified plantain peel (MPP) from aqueous solution were investigated. The effects of three adsorption variables (pH, MPP dose and initial adsorbate concentration) were studied using central composite design (CCD), a subset of response surface methodology (RSM). Quadratic models were developed for both Ni (II) and Cd (II) percentage removals. The prime adsorption conditions obtained were pH of 4.36, MPP dose of 0.82 g and initial concentration of 120 mg/L with desirability of 1.00 which gave good monolayer adsorption capacities of 77.52 and 70.92 mg/g for Ni (II) and Cd (II) respectively. The adsorption data were modelled using Langmuir and Freundlich adsorption isotherms; the equilibrium adsorption of both Ni (II) and Cd (II) on MPP obeyed Langmuir model, and pseudo-second-order kinetics was the order that best described the two adsorption processes.
|
1 Introduction Air, food, soil and water were narrated to be the media where heavy metals such as copper, cadmium, nickel, lead, and zinc are introduced into the environment ( Garba et al., 2015c; Sadaf et al., 2015 ). These heavy metals are reported to be hazardous resulting in damage to ecosystems as well as human health ( Ozdes et al., 2009; Tuzen et al., 2009 ) especially if their concentration is more than the accepted limit ( Alslaibi et al., 2013 ). Their main sources include wastewater discharged from hospitals ( Verlicchi et al., 2010 ), different industries such as Cd–Ni battery, metal plating and alloy manufacturing ( Khavidaki and Aghaie, 2013; Kobya et al., 2005; Krishnan et al., 2011; Kula et al., 2008 ). Presence of these metals in waste stream and ground water is a very serious environmental concern since these metal ions are toxic to various life forms; therefore, removing them as well as controlling their levels in waste waters is very crucial ( Serencam et al., 2008 ). Chemical precipitation, ion exchange, electrodialysis, solvent extraction, coagulation, evaporation and adsorption are among the most prevalent technologies for the removal of metal ions from aqueous solutions ( Garba and Afidah, 2014; Garba et al., 2014, 2015b; Mohammadi et al., 2015; Mohan et al., 2008; Mondal et al., 2015 ), with adsorption being the most widely used method for removing contaminants from wastewater ( Farghali et al., 2013; Garba et al., 2015a ). Sorption methods are considered flexible and easy to operate with much less sludge disposal problems ( Cao et al., 2014; Mohammadi et al., 2015 ). Various adsorbents were narrated in the literature for the removal of heavy metal ions; however, new adsorbents with local availability, high adsorption capacity as well as economic suitability are still needed. This prompted many researchers into investigating cheaper substitutes such as zeolites, silica gel, chitosan, clay materials and agricultural wastes ( Mekatel et al., 2015; Shirzad-Siboni et al., 2015; Tsai et al., 1998 ). Response surface methodology (RSM) is a mathematical model that was reported to be a very useful tool in optimizing the preparation conditions of activated carbons ( Garba and Afidah, 2015 ), but not much was reported on its application in optimizing adsorption process parameters. Therefore, the innovative aspect of this research is to optimize the paramount parameters for an effective adsorption of Ni (II) and Cd (II) from an aqueous solution using CCD. CCD was chosen to evaluate the interaction of the most crucial adsorption parameters such as pH, MPP dose as well as initial concentrations. 2 Materials and methods 2.1 Reagents All the chemicals used in this work were of analytical reagent grade purchased from Sigma-Aldrich and Merck (Darmstadt, Germany); they were used without any further purification. All the glassware used was washed and rinsed several times. Nickel and cadmium solutions and standards were prepared by using analytical grade nickel chloride (NiCl 2 ⋅6H 2 O) and cadmium chloride (CdCl 2 ) with distilled water. The solutions of Ni (II) and Cd (II) were prepared from stock solutions containing 1000 mg/L of Ni (II) and Cd(II), respectively. 2.2 Preparation of adsorbent material Plantain peels used in this study were collected from local food sellers, restaurants and eateries around Samaru and Sabon Gari Local Government of Kaduna state, Nigeria. They were washed and sun dried for 7 days. The dried plantain peels were then crushed into smaller particles in a mortar and sieved with 150 µm sieve until a reasonable quantity of that particle size is obtained, followed by repeated washing to eliminate dust and other impurities. It was then dried in an oven at 25 °C for about 48 h after which it was stored in sterilized closed glass bottles prior to use as an adsorbent. The powdered plantain peels were then modified by immersing in 5% solution of NaOH and autoclaved at 121 °C for 15 min at 10 psi. After keeping at 25 °C for 48 h, it was filtered and washed many times with distilled water until clear water with neutral pH was obtained ( Ashrafi et al., 2014 ). Then, the modified plantain peel (MPP) was dried at 25 °C for 48 h. The MPP was applied for all the adsorption experiments. 2.3 Metal ions adsorption experiments In order to study and evaluate the significance of variables on the percentage removal of Ni (II) and Cd (II), the adsorption experiments were carried out using a batch procedure by shaking 100 mL of the metal ions solutions in a 250 mL Erlenmeyer flask according to the pH, MPP dose and initial concentration as shown in Table 1 . The coded points and their corresponding values are presented in Table 2 . During the adsorption process, the flasks were agitated on a mechanical shaker at 150 rpm. The aqueous samples were analysed using an inductively coupled plasma-atomic emission spectrometer. The adsorption efficiencies were evaluated using the following equation: where C (1) Adsorption efficiency ( % ) = C o − C e C o × 100 o and C e are the liquid-phase concentrations at initial and equilibrium states (mg/L), respectively. The equilibrium amounts q (mg/g) adsorbed per unit mass of adsorbent were evaluated using Equation e (2) : where (2) q e = ( C o − C e ) V W q (mg/g) is the equilibrium amount of the metal ions adsorbed per unit mass of MPP; V (L) is the volume of the solution and W (g) is the mass of MPP used. e The kinetic tests were identical to those of equilibrium. The aqueous samples were taken at preset time intervals and the metal ions concentrations were measured. The amount adsorbed at time t, q (mg/g) was calculated using Equation t (3) : where C (3) q t = ( C o − C t ) V W o and C t (mg/L) are the liquid-phase concentration at the initial and any time t, respectively. 2.4 Adsorption isotherms and kinetic models 2.4.1 Adsorption isotherm The equilibrium characteristics of this adsorption study were described through Langmuir (Lang) and Freundlich (Freund). Lang model presumes monolayer adsorption onto a surface containing finite number of adsorption sites ( Langmuir, 1916 ). Its linear form is given as: (4) C e q e = 1 K L ⋅ Q a 0 + C e Q a 0 and Q a 0 ( mg / g ) K (L/mg) are Lang constants related to adsorption capacity and rate of adsorption, respectively. L The essential characteristics of Lang model can be described by dimensionless separation factor, R L , given as: where (5) R L = 1 1 + K L C o C is the highest initial solute concentration. o R values indicate whether the adsorption is unfavourable ( L R > 1), linear ( L R = 1), favourable (0 < L R < 1), or irreversible ( L R = 0). L Freund model on the other hand assumes heterogeneous surface energies. Its linear form is given by the following equation ( Freundlich, 1906 ): where K (6) log q e = log K F + 1 n log C e F and n are Freund constants. Generally, n > 1 suggests favourable adsorption. It has also been used to evaluate whether the adsorption process is physical (n > 1), chemical (n < 1) or linear (n = 1) ( Martins et al., 2015 ). 2.4.2 Kinetic models The kinetic data were fitted using the pseudo-first-order and pseudo-second-order models. The rate constant of adsorption is determined from the pseudo-first-order equation given as ( Lagergren and Svenska, 1898 ): where q (7) log ( q e − q t ) = log q e − k 1 2.303 t e and q t are the amount of metal ions adsorbed (mg/g) at equilibrium and at time t (h), respectively while k 1 is the adsorption rate constant (h −1 ). The pseudo-second-order equation based on equilibrium adsorption is expressed as ( Ho and Mckay, 1998 ): where k (8) t q t = 1 k 2 q e 2 + 1 q e t 2 (g/mgh) is the rate constant of second-order adsorption. As the pseudo-first-order and pseudo-second-order kinetic models could not identify the sorption mechanism, the kinetic results were further analysed for the diffusion mechanism by applying the intraparticle diffusion model. The intraparticle diffusion equation is expressed as ( Weber and Morris, 1963 ): where k (9) q t = k ip t 0.5 + C ip is rate constant of the intra-particle diffusion equation and C gives information about the boundary layer thickness: larger value of C is associated with the boundary layer diffusion effect. If the adsorption process follows the intraparticle diffusion model, then q t versus t 0.5 will be linear; if the plot passes through the origin, then intraparticle diffusion is the sole rate limiting step. Otherwise, some other mechanism along with intraparticle diffusion is also involved ( Tan et al., 2009 ). 2.5 Design of experiments using response surface methodology (RSM) In this work, a standard RSM design known as central composite design (CCD) was applied to study the Ni (II) and Cd (II) adsorption parameters (pH, MPP dose and initial adsorbate concentrations). The detailed CCD process was described in our previously published paper ( Garba and Afidah, 2014 ). Design expert statistical software (version 6.0.8, Stat-Ease, Inc., Minneapolis, MN, USA) was used for the model fitting and significance for the Ni (II) and Cd (II) adsorption efficiencies. 3 Results and discussion 3.1 Development of regression model equations using CCD The design matrix comprising the preparation variables, their ranges and the responses (Y Ni and Y Cd ) respectively were displayed in Table 2 . In order to compare and correlate the responses, CCD was applied for the development of the polynomial regression equations which were all quadratic expressions as suggested by the software. The model expression was selected in accordance with sequential model sum of square that is based on the polynomial's highest order where the model was not aliased and the additional terms were significant ( Sahu et al., 2010 ). The correlation between predicted and experimental data was blatant as shown by the model's R 2 values of 0.9448 for Ni (II) and 0.9383 for Cd (II) which were within desirability range ( Gómez Pacheco et al., 2012 ). The final empirical model's equations for percentage removal of both Ni (II) (Y Ni ) and Cd (II) (Y Cd ) responses are given as Equations 10 and 11 respectively. (10) Y N i = 86.37 + 8.31 x 1 + 9.84 x 2 + 9.96 x 3 − 1.37 x 1 2 − 3.65 x 2 2 − 4.79 x 3 2 − 6.64 x 1 x 2 − 5.76 x 1 x 3 − 4.62 x 2 x 3 (11) Y C d = 83.96 + 9.24 x 1 + 15.51 x 2 + 3.21 x 3 − 0.28 x 1 2 − 7.30 x 2 2 + 0.90 x 3 2 − 11.95 x 1 x 2 − 3.37 x 1 x 3 − 6.06 x 2 x 3 The positive and negative signs before the terms indicate synergetic and antagonistic effect of the respective variables ( Garba and Afidah, 2014 ). The appearance of a single variable in a term signified a uni-factor effect; two variables imply a double factor effect and a second order term of variable appearance indicate the quadratic effect ( Ahmad and Alrozi, 2010 ). The Ni (II) and Cd (II) percentage removals range from 22.46 to 99.79% and from 10.44 to 99.43% respectively; these can be found on the total experimental design matrix, and the values of the responses obtained are presented in Table 1 . Quadratic model was used as selected by the software for the two responses. The six replicate variables at the centre points, run 15–20, were conducted to determine the experimental error and the reproducibility of the data. 3.2 Statistical analysis In order to evaluate the individual, interaction as well as quadratic effects of the variables influencing the removal efficiency of both Ni (II) and Cd (II), analysis of variance (ANOVA) was performed. The sum of squares and mean square of each factor, F-value as well as Prob. > F values are shown in Table 3 for both Ni (II) and Cd (II) percentage removals. ANOVA validated the importance and adequacy of the models. From Table 3 , dividing the sum of the squares of each of the variation sources, the model and the error variance by the respective degrees of freedom gives the mean square values. The model terms with value of Prob.>F less than 0.05 are considered as significant ( Ahmad and Alrozi, 2010 ). With respect to Ni (II) percentage removal from Table 3 , it can be seen that the model F-value is 19.00 and Prob. > F of <0.0001 signifies the model's significance. The significant model terms were , x 1 , x 2 , x 3 , x 2 2 with only x 3 2 , x 1 x 2 , x 1 x 3 and x 2 x 3 insignificant to the response. Still from x 1 2 Table 3 , F-value of 16.91 as well as Prob.>F of <0.0001 indicated that the model was also significant. In this case were the significant model terms with the insignificant terms being x 1 , x 2 , x 2 2 , x 1 x 2 and x 2 x 3 . From the statistical results obtained, it can be seen that the models were suitable in predicting both Ni (II) and Cd (II) removals within the range of the studied variables. Additionally, x 3 , x 1 2 , x 3 2 and x 2 x 3 Fig. 1(a) and (b) shows the predicted values versus the experimental values for Ni (II) and Cd (II) removals respectively, portraying that the developed models successfully captured the relation between the adsorption process variables and the responses. 3.3 Individual and interaction effects of the variables From Table 3 , it can be observed that the individual effects inflicted by initial concentration and MPP dose on Ni (II) percentage removal were superior with the highest F-values of 49.61 and 45.03 respectively, whereas pH effect was inferior on this response with F-value of 34.50. The quadratic effect of solution pH was more pronounced with F-value of 12.11 while that of MPP dose and initial concentration were low with F-values of 6.43 and 0.99 respectively. The interaction effects between pH–MPP dose and that of pH–initial concentration were analogous with F-values of 11.67 and 10.08 respectively, while that of interaction between MPP dose–initial concentration was less significant with F-value of 5.66. Fig. 2(a) and (b) showed the 3D response surface plots for the studied variables, with Fig. 2(a) demonstrating the effect of pH and MPP dose with initial concentration fixed at zero level (Co = 88 mg/L), whereas Fig. 2(b) demonstrates the effect of pH and initial concentration with MPP dose fixed at zero level (W = 0.6 g), on the same response (Y Ni ). From both figures, the percentage Ni removal can be seen to increase with upsurge in all the studied variables. Also from Table 3 , the three variables (pH, MPP dose and initial concentrations) had uneven impact on the Cd (II) percentage removal. Initial concentration had the least effect as its F-value was smaller and also its variation did not have a significant effect on the process. The individual factors of pH and MPP dose as well as their interactions had the most significant effect on the Cd (II) adsorption as can be seen by their largest F-values as shown in Table 3 . The F-values for pH (x 1 ), MPP dose (x 2 ) and initial concentration (x 3 ) were 27.17, 71.15 and 3.28 respectively. The 3-D surface response analysis of pH and MPP dose interaction effect when the initial concentration was fixed (C o = 88 mg/L) and that of MPP dose and initial concentration when pH was fixed (pH = 7) for Cd (II) adsorption are shown in Fig. 3(a) and (b) respectively. Increase in pH and MPP dose was proportional to high adsorption of Cd (II). 3.4 Process optimization The optimization of Ni (II) and Cd (II) adsorption onto MPP was carried out by a multiple response method called the function of desirability, which was applied using design-expert software (Stat-Ease, Inc., Minneapolis, MN, USA). In the optimization analysis, the target criterion was set as maximum values for the two responses. The optimum adsorption conditions obtained were initial concentration of 120 mg/L, MPP dose of 0.82 g at pH of 4.36 with desirability of 1.00. At the optimum conditions, the Ni (II) and Cd (II) removals were found to be 94.88% and 94.82%, respectively. However, the experimental values obtained at optimum conditions for Ni (II) and Cd (II) removals were 93.05% and 94.21% respectively, showing good agreement between the experimental values and those predicted from the models, with relatively small errors which were only 1.83 and 0.61, respectively for Ni (II) and Cd (II) adsorption. Mohammadi et al. (2015 ) reported in their work a pH of 5.5 as the optimum pH for the adsorption of Ni (II) and Cd (II) onto dolomite powder, observing the appearance of a metal precipitation at a pH greater than 6 ( Mohammadi et al., 2015 ). Alslaibi et al. (2013 ) and Subbaiah et al. (2011 ) also reported optimum pH of 5 in their work of Cd (II) adsorption onto activated carbon from olive stone ( Alslaibi et al., 2013 ) as well as its biosorption by fungus ( Trametes versicolor ) biomass ( Subbaiah et al., 2011 ). Gutha et al. (2015 ) also observe no appreciable increase in the percentage removal of Ni (II) onto tomato leaf powder at a pH and adsorbent dose greater than 5.5 and 0.4 g respectively, revealing them as the optimum adsorption conditions ( Gutha et al., 2015 ). 3.5 Adsorption isotherm To select the best fitted model for the experimental data, chi square (χ 2 ) was incorporated since correlation coefficient (R 2 ) may not justify the basis for selection of the best adsorption model because it only represents the fit between experimental data and linearized forms of the isotherm equations while chi square (χ 2 ) represents the fit between the experimental and the predicted values of the adsorption capacity. The lower the χ 2 value, the better the fit. Table 4 summarizes all the constants; R 2 and χ 2 values obtained from the isotherm models applied for the two metal ions adsorption on MPP. The values obtained for Ni (II) and Cd (II) from the linear Langmuir plot ( Q a 0 Fig. 4a ) were 77.52 and 70.92 mg/g respectively. According to the fitting results listed in Table 4 , Langmuir isotherm model appeared to be much more applicable than the Freundlich having the highest R 2 as well as lowest χ 2 values. The fitness of the Langmuir model to the adsorption process connotes that the metal ion molecules from bulk solution were adsorbed on specific monolayer which is homogeneous in nature. As can also be seen from Table 4 , all the R L values lie between 0 and 1 which confirms the adsorption processes to be favourable under the studied conditions. The n values obtained from the Freundlich plot ( Fig. 4b ) were found to be greater than unity for the adsorbates, further indicating favourable adsorption conditions as well as physical adsorption processes for the two metal ions in aqueous solution. The monolayer adsorption capacity ( ) values of 77.52 mg/g for Ni (II) and 70.92 mg/g for Cd (II) observed in this study compared well with some other adsorbents reported from literature such as 5.41 mg/g from dolomite powder ( Q a 0 Mohammadi et al., 2015 ), 42.41 mg/g by modified chitosan ( Cheng et al., 2014 ), 44.44 mg/g from Bacillus laterosporus MTC C 1628 ( Kulkarni and Shetty, 2014 ) and 58.82 mg/g from tomato leaf powder ( Gutha et al., 2015 ) for Ni (II) adsorption as well as 11.72 mg/g using olive stone activated carbon ( Alslaibi et al., 2013 ), 1.62 mg/g obtained from dolomite powder ( Mohammadi et al., 2015 ), 18.34 mg/g obtained using chemically modified onion skin ( Agarry et al., 2015 ) and 85.47 mg/g from B. laterosporus MTC C 1628 ( Kulkarni and Shetty, 2014 ) for the adsorption process of Cd (II). 3.6 Kinetic studies The values of q e cal , k 1 , R 2 and χ 2 obtained from the plot of pseudo-first-order and q ecal , k 2 , R 2 and χ 2 obtained from the plot of pseudo-second-order kinetic models for the two metal ions adsorption on the MPP were tabulated in Table 5 . It can be seen that the R 2 values obtained from the pseudo-first-order model did not show a consistent trend and also the experimental q e (q e exp ) values did not agree with the calculated values (q e cal ) obtained from the linear plot ( Fig. 5a ). This shows that adsorption of the two metal ions onto MPP does not follow a pseudo first-order kinetic model. However, all the R 2 values obtained from the pseudo-second-order model were closer to unity with good agreement between the experimental and the calculated q e values obtained from the linear plot ( Fig. 5b ), further confirming that the adsorption of the two metal ions on MPP fitted well into the pseudo-second-order model. The values of k pi , C i as well as the correlation coefficients, R 2 , obtained from the intra particle plot ( Fig. 5c ) are also given in Table 5 . Higher diffusion rate constant for Cd (II) can be observed from the table, indicating that the diffusion of Cd (II) was more rapid than that of Ni (II). It can also be observed from Fig. 5(c) that the linear lines of the plot for both adsorbates did not pass through the origin which suggested the presence of intraparticle diffusion but was not the only rate controlling step, some other rate controlling steps might be involved in the process ( Garba et al., 2014 ). 4 Conclusion Three adsorption parameters were optimized with the help of CCD, a subset of RSM for the adsorption of two heavy metal ions onto modified plantain peel (MPP) with their percentage removals (Y Ni and Y Cd ) as the analysis responses. Based on the results obtained, the three factors (pH, MPP dose and initial concentration) have varying impacts on the adsorption processes with MPP dose and initial concentration posing analogous influence on the Ni (II) adsorption while MPP had the greatest effect on Cd (II) adsorption. Highest removal percentage of the adsorbates was obtained at the optimum conditions of pH (4.36), MPP dose (0.82 g) and initial concentration (120 mg/L) with desirability of 1.00. Equilibrium and kinetic data analysed show Langmuir and pseudo-second-order to be the best fitted models respectively. Presence of intraparticle diffusion was also suggested to be involved in the adsorption process along with some other rate controlling steps. Acknowledgement Zaharaddeen N. Garba would like to express his gratitude to the Tertiary Education Trust Fund and Ahmadu Bello University , Zaria, Nigeria for the study fellowship offered to him.
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"AGARRY",
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"HO",
"KHAVIDAKI",
"KOBYA",
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"KULA",
"KULKARNI",
"LAGERGREN",
"LANGMUIR",
"MARTINS",
"MEKATEL",
"MOHAMMADI",
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591a83b34d4c447693a35880470dcb4e_Prevalence profile and associations of cognitive impairment in Ugandan first-episode psychosis patie_10.1016_j.scog.2021.100234.xml
|
Prevalence, profile and associations of cognitive impairment in Ugandan first-episode psychosis patients
|
[
"Mwesiga, Emmanuel K.",
"Robbins, Reuben",
"Akena, Dickens",
"Koen, Nastassja",
"Nakku, Juliet",
"Nakasujja, Noeline",
"Stein, Dan J."
] |
Introduction
The MATRICS consensus cognitive battery (MCCB) is the gold standard for neuropsychological assessment in psychotic disorders but is rarely used in low resource settings. This study used the MCCB to determine the prevalence, profile and associations of various exposures with cognitive impairment in Ugandan first-episode psychosis patients.
Methods
Patients and matched healthy controls were recruited at Butabika Hospital in Uganda. Clinical variables were first collated, and after the resolution of psychotic symptoms, a neuropsychological assessment of seven cognitive domains was performed using the MCCB. Cognitive impairment was defined as two standard deviations (SD) below the mean in one domain or 1SD below the mean in two domains. Descriptive statistics determined the prevalence and profile of impairment while regression models determined the association between various exposures with cognitive scores while controlling for age, sex and education.
Results
Neuropsychological assessment with the MCCB found the burden of cognitive impairment in first-episode psychosis patients five times that of healthy controls. The visual learning and memory domain was most impaired in first-episode psychosis patients, while it was the working memory domain for the healthy controls. Increased age was associated with impairment in the domains of the speed of processing (p < 0.001) and visual learning and memory (p = 0.001). Cassava-rich diets and previous alternative and complementary therapy use were negatively associated with impairment in the visual learning (p = 0.04) and attention/vigilance domains (p = 0.012), respectively. There were no significant associations between sex, history of childhood trauma, or illness severity with any cognitive domain.
Conclusion
A significant burden of cognitive impairment in Ugandan first-episode psychosis patients is consistent with prior data from other contexts. However, the profile of and risk factors for impairment differ from that described in such work. Therefore, interventions to reduce cognitive impairment in FEP patients specific to this setting, including dietary modifications, are required.
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1 Introduction The MATRICS consensus cognitive battery (MCCB) has been suggested as the gold standard for neuropsychological assessment in patients with psychotic disorders ( Green et al., 2004 ; Nuechterlein et al., 2004 ). Developed during the Measurement and Treatment Research to Improve Cognition in Schizophrenia (MATRICS) initiative in 2002, the MCCB assesses for impairment in the seven cognitive domains of i) working memory, ii) attention/vigilance, iii) verbal learning and memory, iv) visual learning and memory, v) reasoning and problem-solving vi) information processing speed, and vii) social cognition ( Kern et al., 2007 ; Nuechterlein et al., 2008 ). In psychosis populations from high-income countries (HIC) where the MCCB has been used, the prevalence of cognitive impairment has been found to range from 36% to 78%, primarily in the domains of processing speed and verbal learning and memory ( Lystad et al., 2014 ; Mesholam-Gately et al., 2009 ). Notable differences as significant as two standard deviations (2SDs) exist between the mean domain scores of first-episode psychosis (FEP) patients versus scores of healthy controls ( Green et al., 2019 ). Cognitive impairment is also associated with various clinical, environmental, and sociodemographic variables, and these associations differ across the seven domains. For example, older age has been associated with impairment in the visual learning and speed of processing domains, while reasoning and problem solving and working memory were associated with female sex ( Lee et al., 2020 ; Rodriguez-Jimenez et al., 2015 ; Atake et al., 2018 ; Li et al., 2019 ; Navarra-Ventura et al., 2018 ). There is also an association between childhood trauma with impairment in the verbal learning and memory domain ( Ayesa-Arriola et al., 2020 ). Long durations of untreated psychosis have been associated with impairment in selected cognitive domains in patients from HIC but primarily among chronically medicated and not first episode psychosis patients ( Stone et al., 2020 ; Bora et al., 2018 ). There is limited research on the prevalence, profile and associations of cognitive impairment in FEP patients from low and middle-income countries (LMICs) ( Green, 2016 ; Vinogradov, 2019 ; Kline et al., 2019 ). It is crucial to determine how FEP patients compared to their healthy controls when assessed with the MCCB in LMICs as it prevents wrongly assigning cognitive impairment ( Reichenberg, 2010 ). There are also differing clinical, environmental, and sociodemographic exposures in low resource settings, yet how they are associated with cognitive impairment is still limited. For example, previous work and education history may be the best source of a patient's previous level of cognitive functioning when determining if there is a current decline, yet their association with cognitive impairment has not been well described in low resource settings ( Stone et al., 2020 ; Stone et al., 2016 ). The association between cognitive impairment and clinical characteristics that are more prevalent in FEP patients from low resource settings like longer duration of untreated psychosis (DUP), higher rates of childhood trauma, and greater psychosis severity are unclear ( Aas et al., 2013 ; Kilian et al., 2018 ; Lezak et al., 2004 ; Fawzi et al., 2013 ; Hecker et al., 2015 ). Diet is closely associated with cognitive function, yet the association of different dietary patterns like carbohydrate-rich diets with cognitive impairment have not been reviewed ( Beilharz et al., 2015 ; Jakobsen et al., 2018 ). Finally, many FEP patients use alternative and complementary therapies before presenting later to care, and understanding if these therapies are associated with cognitive impairment is essential ( Woolhouse, 2007 ). To address these gaps in the current literature, we investigated the prevalence, profile and clinical variables associated with cognitive impairment in FEP patients from a resource-limited setting. These findings may be crucial in developing interventions for cognitive impairment that is a more significant driver of psychosis disease burden than positive, negative or affective symptoms ( Vigo et al., 2016 ; Mihaljević-Peleš et al., 2019 ). 2 Methods 2.1 Study design, setting and participants These have been previously described ( Mwesiga et al., 2021 ). Briefly, this was a cross-sectional study design undertaken at the National Psychiatric Mental referral hospital in Uganda (Butabika hospital). The participants were in-patients aged 18–60 years with confirmed first-episode of psychosis. Additional inclusion criteria included never having been treated with antipsychotic medication or on medication for less than six weeks' duration. The six-week cut-off (as opposed to twelve weeks) was informed by prior evidence that untreated psychosis may resolve more quickly in low- and middle-income countries (LMICs) versus high-income countries ( Chiliza et al., 2012 ; Rangaswamy et al., 2012 ; Kaminga et al., 2018 ; Emsley et al., 2006 ). A cut-off of 18 years was applied to mitigate the challenges of neuropsychological assessment in adolescents versus adults. In Uganda, patients older than 60 are deemed elderly, and these individuals were excluded from participation to eliminate the potential effects of normal aging and dementia ( UBOS, 2012 ). In addition, patients with HIV/AIDS, syphilis and substance use were excluded from participation, as these are common clinical presentations in this setting; and may each also be associated with cognitive impairment ( Nakasujja et al., 2012 ; Sacktor et al., 2005 ; Nakimuli-Mpungu et al., 2006 ). Age, sex and education matched healthy controls were recruited from the outpatient dental department at Butabika Hospital and assessed on the day of recruitment to generate normative values for cognitive function in this population. Inclusion criteria for control participants were 1) no evidence of psychosis or substance use, as assessed by the Mini International Neuropsychiatric Interview (MINI), and 2) no evidence of HIV/AIDS or syphilis. 2.2 Instruments The consent forms, sociodemographic questionnaire, Mini International Neuropsychiatric Interview (MINI) version 7.0 ( Sheehan et al., 2010 ), Positive and Negative Signs and Symptoms of Schizophrenia (PANSS) ( Kay et al., 1987 ) and Childhood trauma questionnaire (CTQ) ( Bernstein et al., 1998 ) used in this study were previously described ( Mwesiga et al., 2021 ). The MATRICS consensus cognitive battery is the gold standard for assessment of cognition in patients with psychosis ( Nuechterlein et al., 2008 ). It assesses for cognitive impairment in the seven cognitive domains of i) working memory, ii) attention/vigilance, iii) verbal learning and memory, iv) visual learning and memory, v) reasoning and problem-solving vi) information processing speed, and vii) social cognition ( Green et al., 2004 ; Nuechterlein et al., 2008 ). The complete battery can be completed in approximately 90 min, excluding the time needed to score. The neuropsychological assessment procedure with the MCCB was performed as previously described Nuechterlein et al. (2008) . Briefly, the MCCB comprises ten different neuropsychological tests; the Trail Making Test (TMT): Part A; Brief Assessment of Cognition in Schizophrenia (BACS): symbol coding; Hopkins Verbal Learning Test-Revised (HVLT-R); Wechsler Memory Scale-Third Edition (WMS-III): Spatial Span; Letter-Number Span (LNS); Brief Visuospatial Memory Test-Revised; Category Fluency: Animal Naming; Mayer-Salovey-Caruso Emotional Intelligence Test (MSCEIT): Managing Emotions (D & H); Continuous Performance Test-Identical Pairs (CPT-IP), MATRICS International Version 2. The ten neuropsychological tests of the MATRICS are administered in the order above to ensure 1) patients start the battery with less cognitively taxing activities that are relatively straightforward to understand to facilitate optimal test-taking performance; and 2) alternate verbal with nonverbal measures, thus aiming to alleviate processing burden and minimize interference among tests ( Nuechterlein et al., 2008 ). The MCCB was administered by two experienced clinical psychologists currently pursuing their doctoral studies. The MCCB was not translated to any Ugandan local language. However, adjustments were needed in the administration of the MCCB tests since the study population composed of a mixed population with people from different ethnic groups and mixed age ranges. The education level of the population was also varied with majority having less than 9 years of formal education. The language of choice in most cases was one of the many local dialects even among individuals with a relatively high education. Most participants had not used a computer before, which was required for administration of the CPT-IP. The participants had never participated in psychological testing and a single reading of the MCCB instructions was often not enough for them to understand the test expectations. If we had used the age and educational criteria of the MCCB, we would have needed to exclude more than 75% of the desired population, giving us an unrepresentative sample and perpetuating the theoretical and ethical problem of excluding the most vulnerable individuals. We administered this cognitive battery to all consenting eligible participants with first-episode psychosis but revised the administration procedures to improve the validity of test scores. The formal scored portion of each test remained unchanged, but test administrators repeated or rephrased instructions for each test up to 5 times until respondents understood the test expectations. If respondents were not sure, the administrators asked them to describe the test expectations before beginning the formal test. We also added a training maze before administering the NAB Mazes, and we trained respondents to use a computer mouse before starting the CPT-IP. Despite these considerations, several patients had difficulty understanding the test requirements or were otherwise unable to complete some of the tests. Standard practice when scoring the MCCB is to use the worst score (i.e., 300 s for the TMT-A and 0 points for all other tests); however, given our sample's demographic differences from participants in almost all previous studies that used the MCCB, it was important to determine whether respondents understood the assessment tasks. Therefore, we developed test-specific rules to make sure respondents understood the test expectations and the distinction was made by the objective view of the interviewer during the assessment of the individual respondents' comprehension of the required task and their ability to complete the task. For tests that required multiple trials (i.e., the HVLT-R, WMS-III Spatial Span, BVMT-R, and CPT-IP), each trial had to have an initial simplified instruction before the test administration. Scoring of all subtest was not adjusted. 2.3 Research procedure First-episode psychosis patients were enrolled into the observational study. After obtaining informed consent, the diagnosis was confirmed using the MINI. Sociodemographic information was compiled using a standard questionnaire, and illness severity was assessed using the PANSS. Patients were then followed up weekly with the PANSS until resolution of psychotic symptoms, at which point the MCCB was administered. In addition, data on previous traumatic experiences were assessed using the CTQ. Consenting healthy controls (matched for age and level of education) were also recruited from the hospital's dental wards and assessed using the MCCB. 2.4 Data analysis Data were analyzed using Stata version 14 ( Stata, 2018 ). Raw scores of the ten tests of the MCCB were first tested for normality. Scores of the mazes sub-test of the Neuropsychological Assessment Battery (NAB-mazes) and trail making test deviated from normal and were log-transformed. The trail making test was also reverse-scored, with lower scores suggesting more inferior cognitive function. These raw scores were then standardized using the means and standard deviations of the healthy controls after matching for age, sex and level of education. Next, composite scores were generated for each of the seven domain scores by summing the standardized scores of individual tests per domain. Standardized test scores of the Trail Making Test (TMT): Part A and Brief Assessment of Cognition in Schizophrenia (BACS): symbol coding and Category Fluency: Animal Naming were combined to represent the speed of processing domain. Hopkins Verbal Learning Test-Revised (HVLT-R) sum scores represented the verbal learning and memory domain. Wechsler Memory Scale-Third Edition (WMS-III): Spatial Span and the Letter-Number Span (LNS) were combined for the working memory domain. Brief Visuospatial Memory Test-Revised sum scores represented the visual learning and memory domain. Mayer-Salovey-Caruso Emotional Intelligence Test (MSCEIT): Managing Emotions (D & H) represented social cognition and the Continuous Performance Test- Identical Pairs (CPT-IP), MATRICS International Version 2 represented attention/vigilance domain. Cognitive impairment was classified as a categorical variable to determine the prevalence and profile of impairment. For the burden of a general cognitive impairment, participants with mean domain scores two standard deviations (SD) below the mean in one domain of the MCCB; or as 1SD below the mean in two or more domains of the MCCB were classified as impaired ( Revell et al., 2015 ). Standardized scores of 2SD below the mean signified cognitive impairment in a specific domain. Duration of untreated psychosis was calculated by subtracting the age at which patient symptoms first presented from the patient's age at admission. Participants with diagnoses of schizophrenia, schizophreniform and schizoaffective disorder on the MINI were classified as non-affective psychosis. Patients with diagnoses of bipolar (irrespective of the phase or type) and depression with psychotic features were classified as affective psychoses. All other psychosis diagnoses were classified as non-affective psychoses. Descriptive statistics were employed for the prevalence and profile for both a general cognitive impairment and impairment in particular cognitive domains. In determining the mean differences between cases and healthy controls and factors associated, cognitive impairment was classified as a continuous variable (higher scores implying better cognitive function). Student t -tests determined if mean cognitive domain scores differed across the FEP patients and healthy controls. Regression coefficients were calculated for the associations between various clinical variables and the seven different standardized domain scores in the FEP patients while controlling for sex and level of education. Due to multiple comparisons, a Bonferroni adjusted significance level was calculated to account for the increased possibility of type-1 errors. A level of significance of 0.05 was used for all analyses. 3 Results After data cleaning, the final sample included 129 FEP patients and 52 healthy controls. The median age of the sample was 29 years (IQR 22–34). Most participants were female [108/181, 64%], single [75/181, 45%] and in non-formal employment [64/181, 38%]. Among the FEP patients, the median age for first seeking help was 26 years [IQR 21–32]. The mean time between the onset of symptoms and presenting to the hospital was 0.932 years [SD 2.798, range (0–18)]. Most participants [76/120; 63%] presented with symptoms for the first time, while 95/113 (84%) presented to a hospital for the first time. Those who had previously presented to a hospital largely used the regional referral hospitals [8/13, 61.5%]. Approximately 13% of FEP patients had previously received antipsychotic medication for less than six weeks' duration. Most participants ate diets rich in legumes (93.3%) and grains (90.8%) in the week before admission. Most participants reported no history of previous trauma in all the domains. The proportions of participants that reported no prior history of childhood trauma in the different domains were physical neglect (36.0%), emotional neglect (42.7%), sexual abuse (72.0%), physical abuse (58.7%), emotional abuse (46.7%). 36% of participants had scores suggestive of underreporting traumatic events ( Table 1 ) . 3.1 Comparison of the burden of cognitive impairment in patients and healthy controls We found that 80/129 (62%) of the FEP patients and 6/52 (12%) of the healthy controls had a general cognitive impairment. There were no statistical differences in the proportions of participants with a general cognitive impairment across sex [prevalence ratio (PR) = 1.15 (p = 0.79)], age [PR = 0.46 (p = 0.19)] or diagnosis (affective versus non-affective psychosis) [PR = 1.17 (p = 0.76)]. 3.2 The burden of impairment in specific cognitive domains Most FEP patients were impaired (2 SD below the mean) in the visual learning and memory domain [38% (CI 30.0–47.5)], while most healthy controls were impaired in the working memory domain [6.1% (CI 1.9–17.80)]. Conversely, the social cognition domain was least impaired in the FEP patients [17% (CI 10.9–24.6)]. No healthy controls were assigned as impaired in visual learning and memory or verbal learning and memory ( Fig. 1 ). 3.3 Profile of impairment Statistically significant differences in mean cognitive scores between FEP patients and healthy controls were found across all domains, except social cognition. The most significant difference was in the reasoning and problem-solving domain, a statistically significant decrease of 1.834 (p ≤ 0.0001). By contrast, the difference in mean scores between cases and controls was lowest in the social cognition domain, a statistically significant decrease of 0.189 (p = 0.62). Other comparisons are shown in Table 2 and Fig. 2 . 3.4 Clinical variables associated with impairment in different cognitive domains For standardized z scores on visual learning and memory domain (most impaired domain), significant associations were found with increased age (p = 0.001), more years of education (p = 0.042), being married (p = 0.016), Hamitic ethnicity (p = 0.017), living with non-family members (p = 0.001), cassava diet in the week before admission (p = 0.041) and a non-affective psychosis diagnosis (p = 0.026). In addition, there were significant associations in the sociodemographic variable of living with a family member (p = 0.001) and wage incomes for the household primary income earner (p = 0.024) with the reasoning and problem-solving domain. There were no significant associations between trauma exposures and standardized z scores across the seven domains except for a positive association between the attention/vigilance domain and the physical abuse domain (p = 0.024). Complete results for the visual learning and memory domain are shown in Table 3 . Raw tables for associations between various clinical variables and the other cognitive domains are in the supplementary files at the end of this article. 4 Discussion The main findings were 1) the prevalence of cognitive impairment in FEP patients was five times higher than age, sex and level of education matched healthy controls. 2) The most frequently impaired domains were visual learning and memory in FEP patients and working memory in healthy controls. 3) Strength of associations differed across the seven different cognitive domains. Increased age was associated with impairment in the speed of processing and visual learning and memory domains. Having a wage income was associated with higher cognitive scores in all domains except the social cognition domain. Cassava-rich diets and previous alternative and complementary therapy use were negatively associated with cognitive impairment in the visual learning and attention/vigilance domains. There were no significant associations between sex, history of childhood trauma, or illness severity with any cognitive domain. 4.1 Comparison of cognitive impairment between patients and healthy controls In line with prior work conducted in diverse settings, the prevalence of cognitive impairment at the first episode of psychosis in our study sample was higher than in the healthy controls ( Lystad et al., 2014 ; McCleery et al., 2014 ; Rodriguez-Jimenez et al., 2019 ; Holmén et al., 2010 ). However, unlike studies reporting the most significant burden in the attention/vigilance and working memory domains, most patients with first-episode psychosis in our study sample were found to have impairment in the visual learning and memory domain ( Braw et al., 2008 ; Rhinewine et al., 2005 ). We found the most significant difference in mean scores in the reasoning and problem-solving domain unlike studies from HIC which reported the most considerable mean differences in the working memory domain ( Aas et al., 2014 ). One explanation is that – given that reasoning and problem solving is a higher-order domain – performance in this sphere is often dependent on lower-order domains such as processing speed ( Kalkstein et al., 2010 ). Thus, the cumulative effect of impairment in lower order domains may be responsible for this finding. In our study, the prevalence of 17% impairment in the social-cognitive domain among FEP patients was relatively low. Further, no statistically significant differences were evident between the mean scores of FEP patients and healthy controls in this domain. This finding is consistent with work from other LMICs suggesting poor psychometric properties of the MSCEIT in such settings ( Kurtz et al., 2018 ; Mehta et al., 2011 ; Emsley et al., 2005 ; Lim et al., 2020 ; Stone et al., 2020 ). There were no healthy controls categorized as impaired in visual learning and memory and verbal learning and memory. There are few studies on this domain in LMIC with a limited number of validated tools for assessing patients with psychotic disorders ( Vingerhoets et al., 2013 ). Thus, further research on neuropsychological testing of the visual learning and memory domain in first-episode psychosis patients is warranted. 4.2 Sociodemographic risk factors for cognitive impairment A 48% increase in standardized scores of the visual learning and memory domain was observed for every unit increase in age. For the speed of processing domain, a unit increase in age was associated with a 57% increase in cognitive scores. This age-associated difference is consistent with literature from high-income countries ( Lee et al., 2020 ; Rodriguez-Jimenez et al., 2015 ; Rajji et al., 2009 ; Atake et al., 2018 ). The lack of associations between sex and impairment in any cognitive domain differs from literature in HIC that often highlight considerable heterogeneity in associations of cognitive impairment in men and women ( Mendrek and Mancini-Marïe, 2016 ). For example, in Hong Kong, the reasoning and problem solving and working memory domains were associated with the female sex, while processing speed was associated with the male sex. In addition, both sexes were associated with impairment in the attention/vigilance domain, and negative symptoms mediated the relationship ( Li et al., 2019 ; Navarra-Ventura et al., 2018 ; Zhang et al., 2017 ). These sex differences have been linked to a disturbance in typical sexual dimorphism (males having larger ventricles and smaller frontal lobes) due to hormonal and immunological factors ( Mendrek and Mancini-Marïe, 2016 ). In all domains except the social cognition domain, having a wage income was associated with higher cognitive scores, keeping with elsewhere literature ( Tan, 2009 ). However, the direction of this association needs further review as it is unclear from this study design if better cognitive function ensures employment through more excellent job opportunities and income, or rather employment and income is protective of cognitive function ( Llerena et al., 2018 ; McGurk et al., 2009 ). 4.3 Diet and cognitive impairment There was a positive association between meat and legume-rich diets with impairment in the working memory domain consistent with other published studies ( Wonodi and Schwarcz, 2010 ; Cao et al., 2021 ). Among 195 Chinese patients with schizophrenia, kynurenic acid (KYNA) was associated with worse performance in the working memory domain, while 5-hydroxy indole was associated with improved performance ( Huang et al., 2021 ). Meat and legumes are rich in tryptophan, whose metabolites include KYNA and 5-hydroxy indole 75, 76. Going forward, better quantification of these metabolites in Ugandan FEP patients may elucidate the underlying mechanisms of this association. Fruit rich diets were not associated with impairment in any cognitive domain. High flavonoids found in citrus may be associated with improved cognitive functioning in schizophrenia patients from other settings ( Bruno et al., 2017 ; Pontifex et al., 2021 ). Previous research has shown that different fruits have different quantities of flavonoids content ( Stangeland et al., 2009 ). This flavonoid content also differs depending on the size of the portion and the part of the fruit (peelings of pomegranate, for example, have more content) ( Shams Ardekani et al., 2011 ). The flavonoid content in the fruits could be quantified in future studies. Cassava was associated with an increased risk for cognitive impairment in the visual learning domain. This cassava association with cognitive impairment is due to thiocyanate toxicity in poorly processed cassava ( Boivin et al., 2017 ; Rivadeneyra-Domínguez and Rodríguez-Landa, 2020 ). To our knowledge, this is the first study to highlight an association between cassava diets and a specific cognitive domain in FEP patients. Given that cassava is a staple diet in Uganda, further work examining this association is required. 4.4 Trauma and its association with cognitive impairment This study found only one association between the attention/vigilance cognitive domain and the physical abuse trauma domain. One possibility is underreporting of traumatic experiences ( Church et al., 2017 ; Read et al., 2001 ; Radhakrishnan et al., 2017 ; Mall et al., 2020 ). Previous studies associated childhood trauma and cognitive impairment in the working memory and reasoning and problem-solving domains. The few studies that have highlighted an association in the attention/vigilance domain reported an association with physical neglect, not physical abuse ( Mørkved et al., 2020 ; Olivier et al., 2015 ). 4.5 Clinical risk factors for cognitive impairment There was a positive correlation between shorter DUP and increased impairment in the domains of attention vigilance which differs from other studies that correlated increased DUP with increased impairment in reasoning and problem-solving and verbal learning and memory domains ( Fraguas et al., 2014 ; Bora et al., 2018 ; Lappin et al., 2007 ; Stone et al., 2020 ). This finding may support evidence that the attention/vigilance domain is impaired earliest during psychotic disorders, as shown in other settings ( Hou et al., 2016 ). Longitudinal studies and studies in the psychosis prodrome are recommended. To our knowledge, this is the first study to report a negative association between previous use of alternative and traditional therapies and cognitive impairment in the attention/vigilance domain. Previous work in Uganda showed that patients with psychotic disorders are treated with herbs and rituals ( Abbo et al., 2012 ; Abbo et al., 2019 ). However, it is unclear if the herbs used by alternative and complementary therapies are associated with cognitive impairment. Recently a study in China highlighted an association between oxidative damage and cognitive impairment in FEP patients treated with herbal remedies ( Xie et al., 2019 ). The nature of the herbs used needs assessment to determine if they cause oxidative damage and cognitive impairment. It is also vital to document previous use of alternative therapies and the medication provided during neuropsychological assessment. Significant associations were observed between non-affective psychoses with impairment in visual learning and memory and the working memory domains. However, among 64 Croatian patients, the association between non-affective psychoses and impairment in the working memory domain were not replicated ( Žakić Milas and Milas, 2019 ). This finding might be due to a more considerable burden of affective psychoses in high-income countries than low-income countries ( Rodriguez-Jimenez et al., 2015 ; Rodriguez-Jimenez et al., 2019 ; Reichenberg et al., 2009 ; McCleery and Nuechterlein, 2019 ; Mwesiga et al., 2020 ). 4.6 Strengths and limitations Several limitations should be borne in mind when interpreting the current study findings. First, the cross-sectional study design undertaken here does not allow a determination of causality. Second, the descriptions for the duration of untreated psychosis were prone to recall bias. Future studies should use standardized instruments like the Nottingham Onset schedule for the duration of untreated psychosis (NOS-DUP) ( Singh et al., 2005 ) and the Interview for retrospective assessment of Schizophrenia onset (IRAOS) ( Mwesiga et al., 2019 ; Haefner and Maurer, 2006 ). We also used the Childhood Trauma Questionnaire, which assesses for trauma retrospectively and is prone to recall bias ( Aas et al., 2011 ; Charak et al., 2017 ; Kilian et al., 2018 ). Third, the diet was not assessed using standardized tools like the 24-hour dietary recall or cluster analysis of dietary patterns, which may have led to misclassification bias in defining the exposure ( Hu, 2002 ; Reedy et al., 2010 ; Thompson and Subar, 2001 ). Also, patients with psychotic disorders are at higher risk for lifestyle disorders like diabetes and hypertension, which are also risk factors for cognitive impairment ( Pillinger et al., 2017 ). This increased risk is thought to be due to patients with psychotic disorders often preferring starch-rich diets and an underlying genetic risk ( Perry et al., 2016 ). These need to be assessed in future studies. These limitations notwithstanding, this is one of few studies in Africa to use the gold standard for neuropsychological assessment in FEP patients ( Kilian et al., 2018 ). The literature on cognitive impairment has primarily focused on schizophrenia, so including both affective and non-affective psychoses highlight an important field for future study. This study also determined associated factors for cognitive impairment specific to this setting, such as dietary patterns, early childhood trauma and previous use of alternative therapies. There is an exciting basis for future studies on cognition and diet in patients with psychotic disorders from low resource settings. Future studies determining the role of various effect modifiers on the association between diet and cognitive impairment are required ( Chen et al., 2016 ; Bioque et al., 2021 ). First, diet is one of the known exposures that can change genetic expression ( Bottero and Potashkin, 2020 ). Second, the microbiome and gut-brain axis may modify the association between a diet with cognitive impairment ( Luca et al., 2020 ). 5 Conclusion Consistent with literature from high-income countries, there is a significant burden of cognitive impairment in Ugandan first-episode psychosis patients than their healthy controls. However, in this setting, the prevalence profile and clinical variables associated with cognitive impairment differ from the literature in HIC. Therefore, neuropsychological assessment in first-episode psychosis patients in this setting must consider the different domains impaired and exposures associated with impairment in this setting when developing interventions to reduce the burden of cognitive impairment. Interventions to improve cognitive function like atypical antipsychotics and cognitive remediation must be undertaken ( Houthoofd et al., 2008 ; Meltzer and McGurk, 1999 ; Linssen et al., 2014 ; Koola et al., 2017 ; Fountoulakis, 2020 ; Bowie et al., 2020 ; Zaytseva et al., 2013 ; Revell et al., 2015 ). Dietary interventions deserve study as a cheap intervention for reducing cognitive impairment. CRediT authorship contribution statement Conceptualization: EKM, DA, NK, NN, DJS; Methodology: EKM, RR; Validation: EKM, RR; Formal analysis: EKM, RR; Investigation: EKM, JN; Data curation: EKM; Writing original draft: EKM, RR, DA, NK, JN, NN, DJS; Visualization: EKM; Supervision: EKM, DA, NK, NN, DJS; Project Administration: EKM, JN, NN; Funding acquisition: DA, DJS. Declaration of competing interest The authors declare no conflict of interest. Acknowledgements We are indebted to the participants who consented to participate in the study. Miss Joy Louise Gumikiriza and Miss Shubaya Kasule are clinical psychologists who administered the MCCB. Ethics approval and consent to participate The study obtained ethical approval from the Human Research Ethics Committee (HREC) of the Faculty of Health Sciences, University of Cape Town (UCT) (#574/2017), the Ugandan National Council of Science and Technology (UNCST) (#HS142ES) and the School of Medicine Research and Ethics committee (SOMREC) (#REC REF 2017-153) of the College of Health Sciences, Makerere University. Institutional permission to carry out the study was obtained from the administration of Butabika hospital. Patients were reimbursed $3 for their time, either completing the entire study assessment or withdrawing consent. Data and material availability All data generated or analyzed during this study are available from the corresponding author. Funding This work was supported by the Neuropsychiatric Genetics in African Populations (NeuroGAP) Study ( Stevenson et al., 2019 ). The content of the protocol is solely a responsibility of the authors, and the funder had no role in the development of the protocol. Appendix A Supplementary data Supplementary tables Image 1 Appendix A Supplementary data Supplementary data to this article can be found online at https://doi.org/10.1016/j.scog.2021.100234 .
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d79d3fbb87054501aa42c094963edd4f_Clinical phenotypes of patients with non-valvular atrial fibrillation as defined by a cluster analys_10.1016_j.ijcha.2021.100885.xml
|
Clinical phenotypes of patients with non-valvular atrial fibrillation as defined by a cluster analysis: A report from the J-RHYTHM registry
|
[
"Watanabe, Eiichi",
"Inoue, Hiroshi",
"Atarashi, Hirotsugu",
"Okumura, Ken",
"Yamashita, Takeshi",
"Kodani, Eitaro",
"Kiyono, Ken",
"Origasa, Hideki"
] |
Background
Atrial fibrillation (AF) is a heterogeneous condition caused by various underlying disorders and comorbidities. A cluster analysis is a statistical technique that attempts to group populations by shared traits. Applied to AF, it could be useful in classifying the variables and complex presentations of AF into phenotypes of coherent, more tractable subpopulations.
Objectives
This study aimed to characterize the clinical phenotypes of AF using a national AF patient registry using a cluster analysis.
Methods
We used data of an observational cohort that included 7406 patients with non-valvular AF enrolled from 158 sites participating in a nationwide AF registry (J-RHYTHM). The endpoints analyzed were all-cause mortality, thromboembolisms, and major bleeding.
Results
The optimal number of clusters was found to be 4 based on 40 characteristics. They were those with (1) a younger age and low rate of comorbidities (n = 1876), (2) a high rate of hypertension (n = 4579), (3) high bleeding risk (n = 302), and (4) prior coronary artery disease and other atherosclerotic comorbidities (n = 649). The patients in the younger/low comorbidity cluster demonstrated the lowest risk for all 3 endpoints. The atherosclerotic comorbidity cluster had significantly higher adjusted risks of total mortality (odds ratio [OR], 3.70; 95% confidence interval [CI], 2.37–5.80) and major bleeding (OR, 5.19; 95% CI, 2.58–10.9) than the younger/low comorbidity cluster.
Conclusions
A cluster analysis identified 4 distinct groups of non-valvular AF patients with different clinical characteristics and outcomes. Awareness of these groupings may lead to a differentiated patient management for AF.
|
1 Introduction Atrial fibrillation (AF) poses a significant public health burden and is caused by underlying processes and disorders leading to a very heterogeneous patient population [1] . A large variety of risk factors for non-valvular AF have been identified, including the age, male sex, hypertension, diabetes, obesity, sleep apnea, heart failure, and coronary artery disease [1] . Racial differences have also been reported to affect the incidence of AF and risk of bleeding from oral anticoagulants [2,3] . Currently, AF is classified based on the symptoms or duration of the AF episodes (e.g., paroxysmal, persistent, and permanent). Although this classification has several prognostic roles, we believe a more sophisticated classification of AF is highly desirable, not only to prevent strokes and bleeding events, but also to provide more individualized adjustments to rhythm- or rate-control therapy. A cluster analysis, an unsupervised data-driven approach, has been used in the cardiovascular realm [4–9] . It successfully classifies subjects from heterogeneous populations into similar groups based on the clinical information. Recent data using heart failure with a reduced (preserved) ejection fraction has indicated that clustering techniques analyzed by standard clinical features can classify patients into several different phenotypes (clusters) that exhibit a different mortality, hospitalization rate, and response to pharmacological therapy or exercise training [4–7] . A recent cluster analysis study using a prospective registry of AF patients in the US demonstrated an improvement in the phenotypic categorization of the disease [8] . That study, though unique and useful, was lacking in having a significant Asian cohort. In this study, we set two objectives: [1] to perform the cluster analysis to identify unique clinically relevant phenotypes of AF using a prospective Japan-wide AF registry and [2] to examine the phenotype-based clinical outcomes. 2 Methods 2.1 Data source and study population The study design and the main outcome analysis of the J-RHYTHM Registry have been reported elsewhere [10–12] . Briefly, the J-RHYTHM Registry is an observational, prospective cohort study that enrolled patients with AF between January 2009 and July 2009 at 158 sites in Japan. Eligible patients were those ≥20 years of age who had at least one episode of AF captured on a standard 12-lead electrocardiogram, who were able to provide informed consent, and who adhered to a local follow-up. This post-hoc study included 7406 patients after excluding patients with mitral stenosis or that had undergone a mechanical valve replacement (n = 410). Warfarin was used as an oral anticoagulation therapy because no direct oral anticoagulant was available when this registry was carried out. The study protocol conformed to the 1975 Declaration of Helsinki and was approved by the institutional review board of the participating institutions. All patients gave their written informed consent. 2.2 Outcomes The primary outcome was defined as all-cause mortality, thromboembolisms, or major bleeding. Thromboembolisms included ischemic strokes, transient ischemic attacks, and systemic embolisms. Major bleeding included intracranial hemorrhages, gastrointestinal bleeding, and other causes of bleeding requiring hospitalization. We defined an ischemic stroke as a sudden neurological deficit lasting >24 h, corresponding to a vascular territory in the absence of a primary hemorrhage that was not explained by other causes such as trauma or an infection. The diagnosis of a stroke was made with computed tomography or magnetic resonance imaging. The patients were followed for 2 years, or until an endpoint, whichever occurred first. All analyses of the rates of the endpoints were based on the first event during the follow-up. A local investigator ascertained the events. 2.3 Definitions The components of the CHA 2 DS 2 -VASc score [13] was defined by congestive heart failure, hypertension, age ≥ 75 (2 points), diabetes, strokes (2 points), vascular disease, an age 65–74, and the sex category (female). With regard to the CHA 2 DS 2 -VASc score, we modified the “V” criterion to include coronary artery disease only, because no data were available regarding peripheral artery disease or aortic plaque. The components of the HAS-BLED bleeding risk score for major bleeding [14] were defined by hypertension, abnormal renal/liver function (1 point each), strokes, a bleeding history or predisposition, a labile international normalized ratio (INR) (therapeutic time in a range [TTR] < 60%), elderly (>65 years), and the use of drugs (antiplatelet agents and nonsteroidal anti-inflammatory drugs) or alcohol > 8 U/week (1 point each). Abnormal renal function was defined as the presence of chronic dialysis, renal transplantation, or serum creatinine > 200 mmol/L was classified as abnormal kidney function. Abnormal liver function was defined as biochemical evidence of significant hepatic derangement (eg, bilirubin > 2x upper limit of normal, in association with aspartate aminotransferase/alanine aminotransferase > 3x upper limit normal). The time in a therapeutic range (TTR) was determined by the method of Rosendaal et al. [15] . For this determination, the target INR level was set at 1.6–2.6 for patients aged 70 years or older and at 2.0–3.0 for patients aged younger than 70 years, according to the Japanese guidelines [16] . 2.4 Statistical analysis The baseline variables of the patients are presented as the number and frequency or mean ± standard deviation (SD) values. There were several variables with missing data including the height (13.8%), body weight (13.1%), hemoglobin (11.5%), platelets (11.6%), creatinine (11.1%), creatinine clearance (11.1%), aspartate aminotransferase (11.1%), and alanine aminotransferase (11.1%). These numerical missing data were imputed with a sequential regression multivariate imputation [17] . In this study we used a hierarchical cluster analysis (Ward’s method) using 40 data items recorded for each patient in the J-RHYTHM Registry shown in the Supplementary file (Appendix S1). We show dendrogram, cubic clustering criterion and constellation tree diagram to estimate the number of likely clusters within our population (Supplementary file, Figs. S1–S3). Between-cluster comparisons were performed using analysis of variance or χ 2 test. To compare the outcomes between the clusters, Kaplan-Meier estimates with log-rank testing were applied to assess the equality of the survival distributions for each endpoint. A logistic regression model was used to test the association between clusters and outcomes, and whether the type of AF (paroxysmal vs. non-paroxysmal [persistent or permanent]) was associated with outcomes for each cluster and all patients. The models were adjusted by the age and sex for all-cause death, by the CHA 2 DS 2 -VASc score for thromboembolisms, and by the HAS-BLED scores for major bleeding. The odds ratios (ORs) for each cluster are presented with 95% confidence intervals (CIs). We used JMP 15 software (SAS Institute, USA) and R-project (R foundation, Vienna, Austria) for the analyses, including the cluster analysis. A two-tailed p-value of <0.05 was considered significant. 3 Results 3.1 Clinical characteristics of the identified phenotypes In the overall study population at baseline (n = 7406), the mean age was 70 ± 10 years, with 29.2% women and 100% Asian participants. A total of 6382 (86.1%) patients were taking warfarin, the mean CHA 2 DS 2 -VASc score was 2.8 ± 1.6, and the mean HAS-BLED score was 2.7 ± 1.2. The cluster analysis identified 4 clinical phenotypes, and Table 1 shows the clinical characteristics across them. 3.2 Younger/low comorbidity cluster This cluster (n = 1876) was composed of younger patients (mean age 67 ± 10 years) with a relatively lower body weight (mean 59 ± 13 kg) and higher rates of paroxysmal AF (45%). They had considerably lower rates of risk factors and comorbidities, including the lowest rates of heart failure (14%), hypertension (12%), diabetes (13%), a prior stroke or transient ischemic attack (TIA) (13%), coronary artery disease (1%), cardiomyopathy (4%), and malignancy (7%). The key characteristic of this cluster was highest rate of alcohol use > 8U/week. Notably, they had a relatively preserved renal function (mean creatinine clearance 67 ± 32 ml/min) and the highest total cholesterol level (193 ± 30 mg/dL). The rate of class I antiarrhythmic drug use (22%) was the highest, but antiplatelet agent (19%) and statin (16%) use was lowest. Reflecting the younger age of the patients in this cluster, they had the lowest CHA 2 DS 2 -VASc score (1.8 ± 1.4) and HAS-BLED score (2.2 ± 1.1). 3.3 Hypertensive cluster This was the largest cluster (n = 4579). The distinguishing characteristic of this cluster was that it had the highest proportion of hypertension (79%) and angiotensin converting enzyme inhibitor or angiotensin II type 1 receptor blocker use (73%). However, the mean value of the office systolic blood pressure (127 ± 17 mmHg), though statistically higher than that of the other clusters, was only 4 mmHg greater than the mean value of the lowest cluster. This cluster had the highest percentage of females (32%). It had the second lowest rates of diabetes, coronary artery disease, and chronic obstructive pulmonary disease after the younger/ low comorbidity cluster. It also had the second lowest CHA 2 DS 2 -VASc and HAS-BLED scores. 3.4 High bleeding risk cluster This was the smallest cluster (n = 302) and exhibited an intermediate age (mean age 71 ± 9 years). The key characteristic of this cluster was that 100% of the patients had a history of some bleeding compared to 1 % or less for the other 3 clusters. Reflecting the presence of a bleeding history, they had the highest HAS-BLED score (3.6 ± 1.1). Ninety percent of the patients were on warfarin and had the highest TTR. Of the four clusters, this cluster had the highest percentage of permanent AF (56%), a history of a stroke or TIA (22%), malignancy (15%), hepatitis (10%), abnormal renal function (5.3%) and abnormal liver function (5.0%). 3.5 Atherosclerotic comorbid cluster This cluster (n = 649) had the oldest patients (mean age 73 ± 8 years) and highest proportion of male patients (84%). A major feature of this cluster was that 99.2% of the patients had coronary artery disease as compared to less than 2% for the younger/low comorbidity and hypertensive clusters and 15% for the high bleeding risk cluster. They also had the highest rates of congestive heart failure (45%) and diabetes (36%), and lowest creatinine clearance (55 ± 27 ml/min). They had the highest rate of antiplatelet agent (70%) and statin (49%) use. Reflecting the presence of multiple comorbidities, this cluster demonstrated the highest CHA 2 DS 2 -VASc score (4.3 ± 1.5). 3.6 Association with conventional grouping We examined the relationship between the four clusters and conventional AF classifications including the AF subtype, CHA 2 DS 2 -VASc score, and HAS-BLED score (Supplementary files, Figure S4. The differences in the distribution of the AF subtype, CHA 2 DS 2 -VASc score, and HAS-BLED score varied significantly across the clusters. These results suggest that the cluster analysis included and integrated information on the AF subtype, CHA 2 DS 2 -VASc score, and HAS-BLED score. 3.7 Prognostic relationship between AF clusters and the outcomes The Kaplan-Meier curves of 3 outcomes across the 4 clusters are shown in Fig. 1 . For all-cause death (Panel A) and thromboembolisms (Panel B), the patients in the younger/low comorbidity cluster had the lowest risk, followed by the hypertensive cluster, high bleeding risk cluster, and atherosclerotic comorbid cluster in that order. For major bleeding (Panel C), the pattern was the same except that the order of the high bleeding risk cluster and atherosclerotic comorbid cluster were flipped. To reiterate, the patients in the younger/low comorbidity cluster demonstrated the lowest risk followed by the hypertensive cluster for all 3 endpoints. A logistic regression analyses showed the difference in outcomes across the clusters after an adjustment for the covariates ( Fig. 2 ). Compared to the younger/low comorbidity cluster, the adjusted risk of all-cause mortality was significantly higher in the atherosclerotic comorbid cluster (OR, 3.70; 95% CI, 2.37–5.80). While there was no significant difference in the risk of thromboembolisms among the 4 clusters, the risk of major bleeding was significantly higher in the 3 other clusters as compared to the younger/low comorbidity cluster: hypertensive cluster (OR, 2.79; 95% CI, 1.58–5.40), high bleeding risk cluster (OR, 14.6; 95% CI, 7.45–30.3), and atherosclerotic cluster (OR, 5.19; 95% CI, 2.58–10.9). A comparison of the C-indices among the models are shown in the Supplementary file (Table S1). The combination of the existing risk scores and cluster analysis improved the prediction accuracy of the three endpoints. 3.8 Prognostic relationship between AF types and the outcomes We further examined whether the type of AF has an impact on outcomes in all patients and each cluster ( Fig. 3 ). A multivariate logistic regression analyses showed that patients with non-paroxysmal AF had a worse prognosis than paroxysmal AF regarding the risks of all-cause mortality (OR, 1.38; 95 %CI, 1.01–1.91), thromboembolism (OR, 1.61; 95 %CI 1.07–2.40), and major bleeding (OR 1.50; 95 %CI, 1.03–2.17) in all patients. The non-paroxysmal AF was prognostic for major bleeding in atherosclerotic comorbid cluster (OR, 3.62; 95 %CI 1.05–12.4). 4 Discussion 4.1 Major findings We performed a cluster analysis on a nationwide cohort of AF patients. The major findings were as follows: a cluster analysis identified four clinically distinct phenotypes and those four clusters were associated with a significantly different risk for the outcomes. Physicians tracking large numbers of AF patients have long been accustomed to discrepancies between the type of AF, presence or absence of heart failure, and patient outcomes. This is due to the current crude phenotype of a highly heterogeneous disease as AF and the effects of comorbidities. A cluster analysis has been used to define the specific subtypes of various diseases with homogeneous clinical characteristics. In a recent study, Inohara et al. reported a cluster analysis of 9749 AF patients enrolled in the Outcomes Registry for Better Informed Treatment of Atrial Fibrillation (ORBIT-AF) registry [8] . They identified 4 clinically distinct AF phenotypes, each of which was significantly associated with the clinical outcome. In their study, the largest cluster, which they named the low comorbidity cluster (n = 4673), had a considerably lower burden of risk factors and comorbidities than the other three clusters, and experienced the lowest mortality. Second, the younger/ behavioral disorder cluster (n = 963) included the youngest AF patients (median 69 years), and they were most likely to be male. The distinguishing behavioral features included a higher prevalence of liver disease, alcohol abuse, drug abuse, and current smoking. They exhibited the second lowest rates of mortality. Third, the device implantation cluster (n = 1651) included patients receiving cardiac electrical devices due to sinus node dysfunction or atrioventricular node ablation. They had the highest median age (77 years) and a considerably higher burden of risk factors and comorbidities. Fourth, the atherosclerotic comorbid cluster (n = 2462) was the second largest group and included predominantly elderly men with ischemic cardiomyopathy. They also had multiple risk factors and comorbidities that resulted in the highest mortality rate. Another cluster analysis using the Japanese AF cohort identified 3 AF phenotypes, each of which was significantly associated with the adverse events including all-cause death, myocardial infarction, and stroke. The 3 AF phenotypes were younger/ paroxysmal AF (n = 1190), persistent/permanent AF with light atrium enlargement (n = 1143), and atherosclerotic comorbid AF in elderly patients (n = 125). They found that conventional risk factors, such as those included in the CHA 2 DS 2 -Vasc score, contribute to cluster formation, whereas AF type or left atrial size, rather than behavioral risk factors, contribute to cluster formation. In our study, we identified 4 specific clusters, namely, the younger/low comorbidity cluster, hypertensive cluster, high bleeding risk cluster, and atherosclerotic comorbidity cluster. The younger/low comorbidity cluster was equivalent to parts of the low comorbidity cluster and younger/ behavioral disorder cluster in the ORBIT-AF registry [8] . The younger/low comorbidity cluster had a considerably lower burden of risk factors but had a higher alcohol consumption. A previous meta-analysis showed that alcohol was associated with a dose-related increased risk of incident AF [18] , and a recent randomized study confirmed that abstinence from alcohol reduced AF burden [19] . This cluster was likely to receive rhythm control therapy as was shown in the ORBIT-AF registry. This may be because physicians believe younger patients are more likely to benefit from maintaining sinus rhythm using class I or class III antiarrhythmic therapies. Accumulating evidence suggests that a lifestyle modification (weight loss and sleep apnea treatment) has a significant role in mitigating the AF burden and maintenance of sinus rhythm after catheter ablation [20,21] . The hypertensive cluster was the largest cluster and was characterized by a higher prevalence of female patients and both systolic and diastolic hypertension. Much previous research has identified hypertension as a highly prevalent and modifiable risk factor for AF patients [22] . A previous randomized controlled study showed that new-onset AF occurred less in the patients assigned to a target systolic blood pressure of less than 130 mm Hg than less than 140 mm Hg [23] . Further, a recent meta-analysis suggests that blood pressure lowering treatment reduces the risk of major cardiovascular events similarly in individuals with and without AF [24] . We identified a high bleeding cluster that was not defined in the previous AF cluster studies [8,9] . The distinguishing feature of this cluster was that all patients had a history of bleeding and had the highest rate of major bleeding events during the follow-up despite a relatively well-controlled TTR. A history of previous bleeding is a well validated risk factor considered in many bleeding scores [25,26] . Further, the higher prevalence of renal or liver dysfunction, hepatitis and malignancy have been shown to be associated with this cluster. Assessment of bleeding history and minimizing modifiable risk factors, together with correct dose of anticoagulants based on a patient’s characteristics and concomitant medications help reduce the risk of bleeding and mortality. We identified an atherosclerotic comorbid cluster that had the highest mortality rate. This cluster was also identified in the previous studies [8,9] , which were characterized by older male patients and high rates of comorbidities including hypertension, diabetes, reduced renal function, and heart failure. The atherosclerotic comorbid cluster seemed to be a high-risk group across several AF registries, including different races. Given that the atherosclerotic comorbid cluster had the highest mortality rate despite appropriate use of antithrombotic drugs and statin, an interdisciplinary team approach would be an optimal clinical approach. The relationship between AF types and outcomes has shown conflicting results regarding its impact on outcomes [27–29] . Therefore, the current risk scoring schemes do not include the type of AF and current practice guidelines provide the same recommendations for anticoagulant therapy, regardless of the type of AF. We showed that patients with non-paroxysmal AF were at higher risk of three outcomes than paroxysmal AF, and this could be explained by older age and comorbidities. The type of AF, however, was no longer prognostic for outcomes in 4 clusters except for a significantly increased risk of major bleeding in patients with non-paroxysmal AF in the atherosclerotic comorbid cluster compared to patients with paroxysmal AF. In recent subgroup analyses of the ENSURE-AF cardioversion trial [30] and ENTRUST-AF PCI trial [31] , Goette et al. showed that patients with paroxysmal AF had a higher incidence of myocardial infarction than those with non-paroxysmal AF. Future research is required to test whether type of AF or cluster analysis can improve risk assessment in various clinical setting and provide optimal treatment for patients with AF. 4.2 Study limitations This study was a prospective cohort study in warfarin era and may represent a selected population within the larger group of AF patients. This study was conducted with patients of Asian origin only, and therefore our results are less generalizable to the overall population. We did not collect any data on the symptoms, physical activity, caffein intake, biomarkers, echocardiography, device implantations, catheter ablation, sleep apnea, or genetic information. We used the data imputed by sequential regression multivariate substitution. The distinctive phenotypes identified in this study need further validation in an external AF cohort. The selection of the 4 clusters and 40 variables used for the cluster analysis were somewhat arbitrary. 5 Conclusions Our study highlighted a significant heterogeneity present in AF patients in Japan and the need to improve the identification of the phenotypes of this disorder. A cluster analysis can be used to take advantage of the various clinical variables in the AF cohort to find relevant patterns that enable new groupings of AF patients. Given the heterogeneity of risk factors and outcomes in patients with AF, future trials should focus on different interventions in the distinct phenotypes of patients with AF. Declaration of Competing Interest The authors declare the following financial interests/personal relationships which may be considered as potential competing interests: Dr. Watanabe received a lecture fee from Daiichi-Sankyo; Dr. Inoue reports receiving research funds from Boehringer Ingelheim and Daiichi-Sankyo and remuneration from Daiichi-Sankyo, Bayer Healthcare and Boehringer Ingelheim; Dr. Atarashi , receiving lecture fees from Daiichi-Sankyo; Dr. Okumura , receiving research funds from Boehringer Ingelheim and Daiichi -Sankyo and remuneration from Boehringer Ingelheim, Bayer Healthcare, Daiichi-Sankyo, and Pfizer; Dr. Yamashita , receiving research funds from Daiichi-Sankyo, Bayer Healthcare and Bristol-Myers Squibb, and remuneration from Boehringer Ingelheim, Daiichi -Sankyo, Bayer Healthcare, Pfizer, Bristol-Myers Squibb, Ono Pharmaceutical and Toa Eiyo; Dr. Kodani received a lecture fee from Daiichi-Sankyo and Ono Pharmaceutical; and Dr. Origasa , receiving lecture fees from Daiichi -Sankyo. Acknowledgment The authors thank the J-RHYTHM Registry staff and participants for their important contribution to this work. Appendix A Supplementary material Supplementary data to this article can be found online at https://doi.org/10.1016/j.ijcha.2021.100885 . Appendix A Supplementary material The following are the Supplementary data to this article: Supplementary data 1
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2bb080d8e1c34a1d97dd8ff44e84b686_Assessing the impact of forest conversion to plantations on soil degradation and forest water conser_10.1016_j.geoderma.2023.116712.xml
|
Assessing the impact of forest conversion to plantations on soil degradation and forest water conservation in the humid tropical region of Southeast Asia: Implications for forest restoration
|
[
"Jiang, Xiao-Jin",
"Wang, Haofei",
"Zakari, Sissou",
"Zhu, Xiai",
"Kumar Singh, Ashutosh",
"Lin, Youxing",
"Liu, Wenjie",
"Liu, Jiaqing",
"Chen, Chunfeng"
] |
The deterioration of soil and water resources resulting from tropical rainforest (TR) conversion to monoculture plantations (e.g., rubber monoculture; RM) could be restrained and restored through intercropping. However, the response of soil properties and forest water conservation function to forest conversion, i.e., the conversion of RM to rubber rainforest (RR: derived from the invasion of wild native plants in abandoned RM), is still unclear. We involved four forests types, TR, RM, rubber-tea agroforestry (RTA), and RR, as transitional steps of forest conversion through a space-for-time substitution approach to examine the dynamic of soil physical, hydrological and chemical properties during the forest conversion (from TR to RM, RM to RTA, RTA to RR, and retransformation into TR). The results show that SOC, TN, TP, and TK decreased in the order of TR > RR > RTA > RM, which was followed by the trend of soil hydrological and physical properties among these forest types. The interrelation between soil physical and chemical properties was mediated by water flow behaviours. High macroporosity and related low Ks
in TR favoured the occurrence of water flow behaviours. Water flow behaviours not only influenced the distribution of soil chemical elements but also played a crucial role in forming appropriate conditions for nutrient turnover. The co-occurrence of preferential and matrix flow was more prevalent in the rainy season than dry season due to the higher frequency and higher amount of rainwater. The preferential flow promoted the soil water flow in the water flow paths and enhanced water storage in the soil pores. In short, the soil properties and soil water supply decreased in the following order: TR > RR > RTA > RM, suggesting that the severe soil degradation that occurred after TR conversion to RM can be restored back to the extent of TR after a period of succession. The results provided new insights for understanding the forest water conservation function and soil properties in response to forest conversion and highlighted that the RR appeared as a transitional stage during the course of forest restoration from RM to TR under low rubber demand. These findings improve the current knowledge of the relationship among soil physical, hydrological and chemical properties in the rubber-growing humid tropical region of Southeast Asia.
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1 Introduction As the center of global biodiversity, TRs are important sources of renewable energy ( Zambelli et al., 2012 ) and regulate the global carbon cycle ( Heiskanen et al., 2019 ). They have been exposed to several constraints, such as deforestation, overexploitation, fragmentation, farmland reclamation, and forest conversion ( Tilman et al., 2017 ). Indeed, large areas of TR have been converted into rubber plantations in Southeast Asia for natural rubber production ( Ahrends et al., 2015 ). This land conversion has degraded the soil’s hydrological, physical, and chemical properties and water conservation functions ( Brinck et al., 2017; Rahman et al., 2019 ). Soil degradation is the deterioration of soil’s hydrological, physical and chemical properties, leading to loss of soil organic matter, decreased fertility, unbalanced elements, reduced aggregate stability, structure abnormality, acidification, salinization, high soil erosion, and declines in regional biodiversity ( Chaudhary et al., 2009; Mann, 2009 ). The water conservation function refers to the process and ability of soil to retain, intercept, redistribute, and store water ( Xu et al., 2022 ). Soil properties and water conservation function are facing severe challenges in the rubber-growing region of Xishuangbanna (Southwest China), part of a global biodiversity hotspot ( De Bruyn et al., 2014 ). As a result, the local government and scientists established intercropping with rubber plantations to improve biodiversity and ecosystem services ( van Noordwijk et al., 2012 ). However, these policies still limits the improvement of soil restoration and water conservation function as the planted area of rubber-based agroforestry is sensitive to factors such as field management and the economic benefits of intercrop ( Wu et al., 2016 ). Due to the limited economic benefits, most rubber plantation located at high elevations and steeper slopes have been abandoned and converted to RR with the current tendency to return to the natural ecosystem ( Fang et al., 2020 ). In the near future, RR could naturally become TR, more adapted to the local soil and climatic conditions. Therefore, it is necessary to understand and master the soil restoration and water conservation function during the conversion from RM to RR. Several parameters, such as canopy interception rate, evapotranspiration, soil saturated hydraulic conductivity ( K ) and non-capillary porosity, and maximum water holding capacity, are used to evaluate water conservation function ( s Li et al., 2021 ). However, these parameters fail to express partial processes of the water conservation function, such as dynamic features of soil water, preferential flow, matrix flow, and water interaction ( Lin et al., 2018; Jiang et al., 2019 and 2020). Preferential flow is the process by which water moves unevenly through soils via a preferred path rather than uniform flow ( Bundt et al., 2001 ). Matrix flow in forest soil is the process of water infiltrating through the soil matrix and is solely controlled by capillary action ( Zhang et al., 2017 ). Water interaction refers to the water drawn from macropores into the surrounding soil matrix by capillary forces during infiltration ( Weiler and Flühler, 2004 ). High and low levels of water interaction through the macropore walls can be traced and identified as strong and weak water interaction based on different dye concentrations ( Weiler and Flühler, 2004; Jiang et al., 2015 ). Soil hydrological properties, i.e., soil K and water flow behaviors, are closely related to soil chemical properties ( s Bundt et al., 2001; Jarvis et al., 2012 ). For instance, preferential flow can substantially transport soil nutrients under high water infiltration rates into deep soil ( Shen et al., 2019 ). Thus, the partial fluctuation of soil chemical properties depends on the soil water content and water flow behaviors ( Wang et al., 2019 ). Moreover, soil chemical properties, such as organic matter content, can affect soil water content and water flow behaviors. For instance, decreased organic matter content can reduce soil porosity ( Li et al., 2007 ), lowering soil water infiltration and storage capacity ( Celik, 2005 ). Soil hydrological, physical, and chemical properties usually exhibit conflicting results after the conversion of TR to RM ( Zakari et al., 2020 ). For instance, the C content can increase ( Maggiotto et al., 2014 ), decrease ( Chiti et al., 2014 ), or not change ( Frazão et al., 2013 ) after forest conversion. While soil water content could increase ( Liu et al., 2019 ) or decrease ( Tan et al., 2011 ) in RM. These inconsistencies may arise by limiting the number of studied forests (i.e., from TR to RM and mixed rubber plantation, and RR) as the inherent forest conversion mechanisms could influence the soil hydrological, physical, and chemical properties ( Rahman et al., 2019 ). To date, there have been few studies that provide useful guidance on how to restore RM or mixed rubber plantations to RR. Therefore, the interaction among soil physical, hydrological, and chemical properties could be more complex in the process of forest conversion from TR to RM, RM to a mixed rubber plantation, mixed rubber plantation to RR, and retransformation into TR over time through natural succession. This study aims to explore the effect of forest conversion on soil degradation and water conservation function during forests conversion in the humid tropical region of Xishuangbanna (Southwestern China). Thus, soil temperature and soil volumetric water content, soil organic carbon (SOC), total nitrogen (TN), total phosphorus (TP), total potassium (TK), bulk density (BD), macroporosity, soil water flow behaviors, and K were measured and determined in the four forests ecosystems including TR, RM, RTA and RR (RM and RTA were developed and converted from TR, RR was converted from abandoned RM). Implying a space-for-time substitution approach, these forests ecosystems were regarded as stages of forward and backward forest conversion that began with TR to RM, RM to RTA, and RTA to RR and were expected RR would be retransformed into TR over time through natural succession ( s Fig. 1 E). Our specific objectives were to examine i) the dynamics of soil volumetric water content; ii) the soil chemical properties (i.e., SOC, TN, TP, TK); iii) the soil physical and hydrological properties (i.e., macroporosity, K , water flow behaviors); and iv) the relationship among soil physical, hydrological and chemical properties during forests conversion. The findings of this study would be useful in the sustainable management of RM and mixed rubber plantations under low rubber demand scenarios and would be used as a reference for forest restoration from plantation to natural forest in the rubber-growing humid tropical region of Southeast Asia. s 2 Materials and methods 2.1 Experimental site The experimental site is located in the Xishuangbanna Tropical Botanical Garden (21°55′39″ N, 101°15′55″ E; 594 m asl), Mengla County, SW China. This region is characterized by a tropical monsoon type of climate, with a rainy season starting from May to October and a dry season from November to April. The mean annual precipitation is approximately 1500 mm (from 2005 to 2018), and the monthly mean air temperature is 22.5 °C ( Lin et al., 2018 ). The soil is classified as Oxisol (USDA-SCS, 1994) or Acric Ferralsols type ( IUSS Working Group WRB, 2014 ), which is derived from Cretaceous yellow sandstone ( Zhou et al., 2019 ). The soil is approximately 2 m deep and rich in iron (Fe) and aluminum (Al) oxides due to intensive weathering and leaching ( Zhao et al., 2017 ). Four plots (30 m × 18 m) were established in each studied forest type (i.e., TR, RM, RTA, RR). Field sampling was conducted in the four plots in both rainy and dry seasons ( Fig. 1 A). The dominant trees in TR were Pometia tomentosa , Terminalia myriocarpa , Gironniera subaequalis , and Garcinia cowa , forming a climax community after decades of succession ( Fig. 1 B). RM site was established after the clearance of native vegetation in 1989 ( Liu et al., 2015 ). Rubber trees ( Hevea brasiliensis ) in RM are arranged in a double row and planted at a distance of 3 m × 4 m, and each set of double rows is separated by a gap (width) of 20 m. Tea is intercropped in the gaps at a distance of 4 m × 4 m in 2010 to form the RTA. RM and RTA were subjected to regular land management practices, such as latex tapping (approximately 120 times year −1 ), herbicide (applied at least once a year) and fertilizer applications to remove weeds and promote rubber tree growth, respectively. According to the local farming practices, at rate of 0.5 kg of mineral fertilizer containing 15 % N as (NH 2 ) 2 CO, 15 % P as NH 4 H 2 PO 4 , and 15 % K as KCl to a trench of 100 cm (long) × 20 cm (wide) × 10 cm (deep) between two rubber trees at the end of March and at the beginning of September. Some abandoned RMs at high elevation were recently invaded by native species (i.e., Indosasa hispida , Callicarpa bodinieri , and Millettia pulchra ) to form the RR. Detailed information about the stand characteristics of the four plots is shown in Table 1 . The trees heights were determined utilizing a portable laser distance meter (T60G+; THINRAD, China). Canopy cover and leaf area index were measured using an LAI-2200 plant canopy analyzer (Li-Cor Inc., USA). The particle size of soil samples was determined by the laser granulometry method (Mastersizer E, Malvern) ( Pieri et al., 2006 ). The roots were collected in 0.1 m intervals down to the 0.5 m depth with a root sampler (inner diameter, 25 mm; height, 150 mm) from fifteen random points in each plot. The root samples from the same plot were pooled to form a composite sample for each plot. 2.2 Measurement of rainfall, soil volumetric water content and soil temperature The rainfall record was obtained from the Xishuangbanna Meteorological Station, which is located near the study site ( Fig. 1 A). Soil volumetric water content and soil temperature at a depth of 20 cm were measured using 5TE sensors (Decagon Devices, Pullman, WA, USA). The 5TE sensors (10.0 cm length, 3.7 cm width, 0.7 cm thickness) have three prongs to enable simultaneous measurement of soil temperature and soil volumetric water content ( Rosenbaum et al., 2010 ). The sensor data were collected at an interval of 5 min by the ECH2O Utility software (Decagon Devices, Inc©, Pullman, WA) through an Em50 data logger. Given that the slope could affect soil water flow to the subsurface, the four 5TE sensors were inserted at the downhill slope of the four plots ( Fig. 1 C and D). The impact of the sensor installation on water flow and soil properties was almost negligible after four months during which several rainfall events saturated the soil; afterward, we started to collect the data from 5TE sensors. The accuracy (0.01 cm 3 cm −3 ) of the 5TE sensor for measuring soil volumetric water content was calibrated using repacked core samples in the laboratory. 2.3 Measurement of soil properties Bulk density (BD) and macroporosity are important predictors of soil thermal, hydraulic, and mechanical properties ( Assouline, 2006 ). In our studied site, many cracks and fissures emerged in the dry season and disappeared in the rainy season. Porosity is linked to the presence of cracks and fissures, so we used BD and macroporosity to express the size of cracks and fissures quantitatively. The BD and macroporosity at a soil depth of 20 cm in each plot (nine replicates per plot) were measured by cutting ring (inner diameter, 70.00 mm; height, 52.00 mm; and volume, 200 cm 3 ) in dry and rainy seasons ( Fig. 1 C and D). The porosity (i.e., total porosity, capillary and macroporosity) was calculated involving the bulk density data. The soil samples were collected from nine quadrats in each plot during the rainy and dry seasons to measure soil chemical properties (SOC, TN, TP, TK) ( Wang et al., 2007 ). The soil sample was mixed, stored and shipped the same day to the Biogeochemistry Laboratory of the Xishuangbanna Tropical Botanical Garden. Soil clods were manually broken into smaller pieces, and air-dried at room temperature (about 25 °C) for 30 days ( Wang et al., 2007 ). The air-dried soil was separated into two parts. The first part was sieved through 0.25 mm mesh for SOC, TN, and TK analysis; and the rest passed through 0.15 mm mesh for TP analysis ( Wang et al., 2007 ). The soils of the study area were free of inorganic carbon, as the soil samples did not react with HCl; therefore, all the measured carbon was considered SOC ( Chen et al., 2017 ). The elemental carbon concentration was measured by dry combustion with a Vario MAX CN elemental analyzer (Langenselbold, Germany). TN and TK were measured using a carbon–nitrogen analyzer (Vario MAX CN, Elementar Analysensysteme, Germany); and inductively coupled plasma spectrometers after melting with sodium hydroxide (ICP; SPECTRO ARCOS EOP, Germany), respectively. TP concentration in soil was determined using the molybdate colorimetric method following perchloric acid digestion and reduction by ascorbic acid ( O'Halloran and Cade-Menun, 2006 ). 2.4 Interpretation of soil water flow behaviors Three dye-tracer experiments were conducted in each studied plot to visualize the infiltration pattern and water flow paths in the dry season ( Fig. 1 C and D). Water flow paths include root channels, soil cracks, macropores and earth worm burrows ( Flury and Wai, 2003 ). In this experiment, a four-sided metal frame of 2 m × 0.5 m × 0.3 m (lbh) was carefully inserted into the soil. Minor fissures between the frame and soil were sealed using wet soil to prevent dye solution leakage, and the field surface was kept intact simultaneously. The surface vegetation and a thin layer of the soil (less than 2.0 cm) in the plot was carefully removed to ensure a horizontal surface. Each metal-frame was filled with Brilliant Blue FCF dye solution at a concentration of 4.0 g L −1 ( Flury and Wai, 2003 ). A filter screen (1.95 m × 0.45 m) mesh of 0.2 cm diameter was previously placed in the plots to ensure similar flooding conditions in all subplots. Water was successively added to the plot to maintain the water head at a constant head of 2.0 cm during the infiltration period. The total dye infiltration volume was 117 L for each subplot. Three vertical soil sections were dug 24 h in each plot after the end of dye infiltration experiment. Each soil section and its dye-stained patches were photographed using a digital camera (Canon EOS Rebel T3, Japan) ( Weiler and Flühler, 2004 ). The obtained images were separated into two parts: nonstained areas as matrix flow ( Bundt et al., 2001 ) and the dye-stained areas. The dye-stained areas were further separated into three water flow behaviors: preferential flow, strong water interaction, and weak water interaction which correspond to concentration > 2.0, 0.5–2.0, and 0.05–0.5 g L −1 , respectively, based on dye staining intensity using ERDAS IMAGINE version 9.0. Detailed information on the image processing of the vertical soil sections is provided by Cey and Rudolph (2009) , and Forrer et al. (2000) , and additional information on the field measurements and image processing is given by Jiang et al. (2015) . 2.5 Measurement of saturated hydraulic conductivity (K s ) Nine single-ring infiltrometer experiments were conducted in each plot at depths of 20 cm to estimate the soil saturated hydraulic conductivity ( K ) in dry and rainy seasons ( s Fig. 1 C and D). Stainless-steel cylinders were carefully inserted 5.0 cm into the soil one month before K experiments to minimize the disturbance of infiltrometer installation on soil pores. The sidewalls and edges of cylinders were kept water-tight. Each cylinder was initially filled with an equivalent water head of 10.0 cm (using a reference ruler). The time taken for the water level to decrease to 1.0 cm in the cylinder was recorded. Thereafter, a volume equivalent to 1.0 cm depth was successively added to the cylinder until a constant infiltration time for three consecutive measurements at 5-minutes intervals, at which we assumed a steady-state flow ( s Zhu et al., 2019 ). The refilling procedure took approximately 1.2 h. The steady-state infiltration rate ( I , cm min s −1 ) and K (cm s s −1 ) were calculated based on the last three consecutive measured values ( Reynolds and Elrick, 1990; Bodhinayake et al., 2004 ) (Eq. (1) ). where (1) K s = I s π r 2 H C 1 d + C 2 r + 1 α C 1 d + C 2 r + 1 I (cm s 3 s −1 ) is the quasi-steady state infiltration rate, r (cm) is the radius of the ring, H (cm) is the average ponding depth, d (cm) is the insertion depth of the cylinder into the soil, C and 1 C are dimensionless quasi empirical constants, and 2 α is the soil macroscopic capillary length. For this work, both r and d are 5 cm. The sorptive number ( α = 0.12 cm −1 ) was estimated based on textural classes (using laboratory particle size analysis). The constants C and 1 C were 0.316 2 π and 0.184 π , respectively, for d ≥ 3 cm and H ≥ 5 cm ( Reynolds and Lewis, 2012 ). 2.6 Statistical analysis First, soil physical, hydrological, chemical properties were tested for normality, and a log- or square root transformation was performed for variables with non-normal distribution data. Then, a one-way analysis of variance was applied to evaluate the effects of four plots (RM, TR, RTA, and RR) on the dye-stained area. Simultaneously, two-way analysis of variance was performed to assess the effects of season and studied plot on the soil properties (BD, macroporosity, K , SOC, TN, TP, TK). Significant differences between means were detected based on the least significant difference test at s P < 0.05. ANOVA was successful performed to detect the difference among the four plots, assuming that ANOVA would not introduce any systematic error into the statistical analysis due to similar edaphic-climatic conditions of the studied sites. Spearman’s correlation was employed to analyze the relationship between soil physical or hydrological properties and soil chemical properties. The analyses were performed with SPSS 20.0 (Statistical Package for the Social Sciences, USA). In addition, we applied linear redundancy analysis (RDA) to explore the relationships between soil physical, hydrological, and soil chemical properties. For this RDA analysis, we conducted a Monte Carlo permutation test based on 499 random permutations to evaluate the significance of the canonical axes eigenvalues ( ter Braak and Smilauer, 2002 ). This ordination analyses was performed with CANOCO 4.5. Moreover, we conducted a structural equation modelling to analyze the best possible explanatory relationship among soil physical, hydrological and chemical properties. Data were fitted to the model using the maximum likelihood estimation method. The adequacy of the model was determined using the χ 2 test, root square mean errors of approximation (RMSEA), and Akaike information criteria (AIC). Adequate model fits are indicated by a non-significant χ 2 test ( P > 0.05), low RMSEA (<0.08), and AIC ( Grace, 2006 ). The structural equation model was computed using AMOS 22.0 (SPSS Software, Chicago, IL). 3 Results 3.1 Rainfall and soil volumetric water content In 2018, a total of 75 and 50 rainfall events were recorded in the rainy and dry seasons, respectively. The rainfall events were dominated by lower rain intensity in the dry season and higher rain intensity in the rainy season. The total rainfall amount was 630.8 mm in the rainy season and 198.4 mm in the dry season ( Fig. 2 A). The rainfall amount in the four sampling plots was not statistically correlated with soil temperature ( P > 0.05), but significantly correlated with soil volumetric water content ( P < 0.05) ( Fig. 2 B, and C). Both the season and plot type significantly affected the mean soil volumetric water content ( Table 2 ). The average soil volumetric water content was higher in TR, followed by RR, RTA, and RM during the whole year (2018) ( Fig. 2 C). The lowest soil volumetric water contents occurred in RM and RTA in the rainy and dry seasons; and ranged from 0.16 to 0.25 cm 3 cm −3 in the rainy season and 0.11 to 0.20 cm 3 cm −3 in the dry season. However, the highest soil volumetric water contents recorded in TR and RR; and ranged from 0.26 to 0.35 cm 3 cm −3 in the rainy season and 0.21 to 0.25 cm 3 cm −3 in the dry season ( Fig. 3 C and D). In a word, the highest values and widest range of the soil volumetric water content occurred in TR, and the lowest and narrowest values were found in RM both in rainy and dry seasons ( Fig. 3 and Table 2 ). Besides, correlation analysis shows that the relationship between the soil temperature and soil volumetric water content was significantly negative in the rainy season and positive in the dry season ( P < 0.05) ( Fig. 2 D). Both the season and plot type significantly affected the mean soil temperature ( Table 2 ), which followed the decreasing order of RM > RTA > RR > TR in the rainy season and TR > RR > RTA > RM in the dry season ( Table 2 ). The soil temperature ranged between 24.1 °C and 26.0 °C in the rainy season, and 18.1 °C and 24.0 °C in the dry season ( Fig. 2 B). The highest frequencies of soil temperature (24.1 to 26.0 °C) were in the decreasing order of RM > RTA > TR > RR in the rainy season ( Fig. 3 A). Simultaneously, the lowest frequencies of soil temperature (18.1 °C to 20.0 °C) were dominated by RR in the dry season, followed by RM and RTA ( Fig. 3 B), the medium frequencies (20.1 °C to 24.0 °C) by TR, and the highest frequencies (22.1 °C to 24.0 °C) ranged in the decreasing order of RR > RTA > RM > TR. 3.2 Soil chemical properties The SOC and TN were higher in TR than RM and RTA ( Table 3 ). The SOC was 38.0 % (rainy season) and 37.6 % (dry season) lower in RM compared to TR. Both the SOC and TN did not change ( P > 0.05) in the two seasons after RM conversion to RTA. However, the SOC increased by 40.1 % (rainy season) and 41.8 % (dry season), and TN by 63.1 % (rainy season) and 64.7 % (dry season) after RM conversion to RR. The TP significantly decreased by 44.9 % in RM, 34.7 % in RTA, and 12.2 % in RR compared to TR in the rainy season. Moreover, significant differences in TP occurred after TR conversion to other forests systems in the dry season, and the TP ranged in the order TR > RR > RTA > RM. The TK was higher in TR compared to other forests during the two seasons; but TK did not significantly change ( P > 0.05) after RM conversion to RTA. Finally, TK increased by 101.1 % (rainy season) and 103.4 % (dry season) after RM conversion to RR. 3.3 Soil physical properties and hydrological properties The soil BD and macroporosity also significantly differ with plot types and seasons ( Table 3 ). The lowest BD occurred in TR, and the highest BD occurred in RM. The soil macroporosity decreased by 15.4 % (rainy season) and 17.2 % (dry season) after TR conversion to RM; but increased by 14.8 % (rainy season) and 14.7 % (dry season) after RM conversion to RR. Both macroporosity and K did not significantly ( s P > 0.05) differ between RM and RTA, irrespective of the rainy or dry season. The K , however, was 40.5 % (rainy season) and 28.6 % (dry season) higher in TR compared to RM; and 48 % (rainy season) and 30 % (dry season) lower in RM compared to RR. Overall, the s K followed the decreasing order of TR s RR > RM ≅ RTA in the two seasons. ≅ Water infiltration patterns exhibit that various water flow behaviors emerged in the soils of the four forest ecosystems ( Fig. 4 A). Preferential flow occurred as patch distribution pattern in all plots across the four forest types. Strong and weak water interactions (i.e., the intensity of water flow from the macropores into the surrounding soil) occur when water moves through the water flow path (e.g., macropores and cracks). Preferential flow bypassed the soil matrix with low permeability to reach the deep soil, but matrix flow slowly moved downward into the soil matrix. In top soil layers (0–20 cm), preferential flow followed the decreasing order of TR > RR > RTA > RM. The strong water interaction ranged in the decreasing order of RM > RTA > RR > TR, and the weak water interaction followed the order of RR > TR > RM RTA. The matrix flow ranged in the order RM ≅ RTA > RR ≅ TR ( ≅ Fig. 4 B). The water flow behaviors and soil volumetric water content were correlated at different levels ( Fig. 5 ). The preferential flow had significant positive correlations with S(1/4) (1/4 sum of soil volumetric water content reorder from high to low) (R = 0.996, P < 0.01), S(1/4–2/4) (R = 0.957, P < 0.05), S(2/4–3/4) (R = 0.926, P < 0.05), S(3/4–4/4) (R = 0.973, P < 0.05). The strong water interaction had significant negative correlations with S(1/4–2/4) (R = -0.941, P < 0.05), S(2/4–3/4) (R = -0.912, P < 0.05), S(3/4–4/4) (R = -0.961, P < 0.05). 3.4 Relationships among soil physical, hydrological and chemical properties Redundancy analysis shows that the first and second axes explained 76.5 % and 0.2 % of the variation in soil chemical properties, respectively; most selected variables were highly linked to the first axis ( P = 0.002) ( Fig. 6 A). The first axis was mainly related to macroporosity, K and BD; and the second axis was only linked to soil volumetric water content. The eigenvalue followed the order macroporosity (eigenvalue = 0.721, V = 38.88) > s K (eigenvalue = 0.556, V = 29.97) > bulk density (eigenvalue = 0.390, V = 21.02) > soil volumetric water content (eigenvalue = 0.187, V = 10.08) > soil temperature (eigenvalue = 0.001, V = 0.05). It reflects that the soil chemical properties (SOC, TN, TP, and TK) were affected by these factors in decreasing order of influence strength: macroporosity > s K > bulk density > soil volumetric water content > soil temperature ( s Tables 4 and 5 ). Furthermore, structural equation model supports that macroporosity positively influences the soil volumetric water content and K , and these soil hydrological factors positively influenced SOC, TN, TP, and TK. However, the SOC and TN negatively affected BD, which negatively affected macroporosity. In short, the relationship between soil physical and chemical properties was mediated by soil water features ( s Fig. 6 B). 4 Discussion 4.1 Soil hydrological properties mediate the relationship between soil physical and soil chemical properties The redundancy analysis and spearman's correlation ( Fig. 6 A and Tables 4 and 5 ) show that the most important variables affecting soil chemical properties were related to macroporosity, followed by K , BD, and soil volumetric water content, and the interactions among soil physical and chemical properties were mediated by soil hydrological functions ( s Fig. 6 B). Our results of the negative correlation between BD and soil chemical properties correspond to the results from Joshi and Garkoti (2023) . The litterfall is intercepted by soil cracks and tree trunks during runoff ( Sayer and Tanner, 2010 ) and decomposed into soil chemical elements and fine organic compounds, which are easily mobilized and carried into subsurface soil by preferential flow ( Dibbern et al., 2014 ). As a result, the high accumulation of SOC, TN, TP, and TK was beneficial to soil aggregate formation, causing higher porosity and low BD. However, among the soil chemical properties, SOC and TN negatively affected BD, which further negatively influenced the macroporosity ( Fig. 6 B). In other words, lower BD promoted higher macroporosity. High macroporosity and related low K beneficially favored the occurrence of different water flow behaviors that mediates the distribution of soil chemical properties. As a result, some soil chemical elements reach the deep soil layers during water infiltration and accumulate there and improve soil pores, which further enhance the soil infiltration capacity ( s Bundt et al., 2001 ); particularly higher SOC can promote the soil water storage in micropores ( Li et al., 2007 ). Based on these findings, we can point out that the relationship between soil physical properties and soil chemical properties is mediated by water flow behaviors. 4.2 Effects of forest conversion on soil degradation Water flow behaviors not only mediated the distribution of soil chemical elements but also played a key role in the formation of appropriate conditions for nutrient turnover. In the present humid tropical zone, soil temperature (20.79 °C to 25.75°C) and soil volumetric water content (0.18 to 0.29 cm 3 cm −3 ) were suitable ( Table 2 ); simultaneously, the aeration (oxygen) can be replenished during the appearance-disappearance process of water flow behaviors ( Fig. 4 ), and a part of substrate (or organic matter) had transported into deep soil by preferential flow ( Fig. 6 ). Moreover, the alternative occurrence of preferential flow and matrix one led to high variation in soil moisture, oxygen, and substrate, leading to fluctuation of soil chemical properties. This fluctuation in soil chemical properties depended on forest structure (or types), with their decreasing order of TR > RR > RTA > RM corresponding to the order of soil hydrological and physical properties in these four forest types. Our findings corroborate a previous study reported that the soils suffering severe degradation after TR conversion to RM reach better chemical levels after 10 years of agroforestry (or intercropping) practices ( Chen et al., 2019 ). We found that soil chemical properties increased with increasing soil water content, which was oppsite to the previous findings where soil moisture increases up to a threshold lowered the soil elements accumulation (e.g., soil carbon) ( Maggiotto et al., 2014 ). In fact, higher soil water content or soil water saturation without fluctuation usually inhibits aerobic microbial activity or organic matter mineralization. However, if the availability of water and oxygen alternatively fluctuates due to preferential flow, this favors nutrient turnover and microbial activities ( Mu et al., 2021 ). 4.3 Effects of forest conversion on water conservation function The water infiltration patterns ( Fig. 4 ) and related parameters (macroporosity and K ) were significantly varied with forest ecosystems ( s Table 3 ). The preferential flow was the dominant water flow behavior since the beginning of rainwater infiltration, and later on, both preferential flow and matrix flow occurred once the soil became saturated with infiltrated rainwater ( Fig. 4 and Table 2 ). This co-occurrence of preferential flow and matrix flow was more prevalent during the rainy season due to the high frequency and high amount of rainwater ( Fig. 3 ), although macroporosity and K were higher during the dry season than the rainy season ( s Table 3 ). Further, the positive correlations between preferential flow and S(1/4), S(1/4–2/4), S(2/4–3/4), and S(3/4–4/4) indicate that preferential flow not only channeled water to follow the soil water flow paths (e.g., soil macroporosity), but also enhanced soil water storage ( Fig. 5 ). Simultaneously, the negative correlations between strong water interaction and S(1/4–2/4), S(2/4–3/4), and S(3/4–4/4) imply that this water flow behavior (strong water interaction) did not help soil water storage into soil ( Fig. 5 ). Namely, the soil volumetric water content in the unsaturated soil matrix highly depended on preferential flow and associated characteristic or parameters, especially the soil macroporosity but not K ( s Fig. 6 ). This finding may contradict the previous study’s results where the soil volumetric water content was found to be mainly affected by water infiltration capacity ( K ) ( s Zhu et al., 2019 ). When soil was unsaturated, the rainwater only flowed into the soil pores via preferential flow paths. Once the soil had become saturated with rainwater, both preferential flow and matrix flow determined the soil water transport, and the infiltrated water was simultaneously redistributed and stored into the adjacent soil through water interactions ( Figs. 4 and 5 ). The stored water can therefore be transported to the root zone by capillary force for plant uptake during the dry season ( Jiang et al., 2020 ). These water transport and storage mechanisms were more pronounced in old-growth and undisturbed primary forests (i.e., TR). Further, a substrantial amount of the soil volumetric water content in TR and RR during the dry season comes from underground sources through capillary rise ( Jiang et al., 2020 ). In our case, the synergistic effect of various water flow behaviors (preferential flow, matrix flow, water interaction, and upward capillary water) on soil water supply was in the order TR > RR > RTA > RM. As a result, the soil volumetric water content significantly varied with forest ecosystems ( Fig. 2 ). Based on these findings, we affirmed that the low water supply efficiency in RM has resulted in water stress during the long-lasting dry season in this region. However, water stress has been markedly alleviated in RTA and in RR, especially in TR because of its high water supply efficiency. We found that forest water conservation function has alleviated and improved temperature on the forest floor. The high soil temperature occurred in the rainy season ( Fig. 2 B), and the correlation analysis suggests that the relationship between soil temperature and soil volumetric water content was significantly negative in the rainy season ( P < 0.05) ( Fig. 2 D). This relationship between the soil temperature and soil volumetric water content has likely appeared due to three processes: (1) water evaporation from soil carries heat away from soil ( Zhang et al., 2022 ); (2) water supply characteristics, especially the water flow under high-frequency could disperse the extreme soil temperature to the surrounding soil; and (3) air and soil temperature are regulated by forest crown that intercepts sunlight ( Lin et al., 2018 ), and this depends on forest type and forest structure ( Li et al., 2015; Lin et al., 2020 ). As a result, the temperature regulation processes were more pronounced in RR, especially in TR. In short, extreme soil temperatures could occur in RM both in the rainy and dry seasons, and this could be improved by the robust temperature regulation mechanisms in RTA and RR. 5 Conclusions Variations in soil properties and forest water conservation function were investigated during the forest conversion (from tropical rainforest to rubber monoculture, rubber monoculture to rubber-tea agroforestry, rubber-tea agroforestry to rubber rainforest, and rubber rainforest retransformation into tropical rainforest) in the humid tropical region of Southeast Asia. The soil’s physical and chemical properties were interdepended, and many of these interrelationships were mediated by water flow behaviors. The accumulation of SOC TN, TP, and TK was beneficial to formation of soil aggregate which exhibited different levels of porosity and BD. However, macroporosity and K favored the occurrence of different water flow behaviors that controlled the distribution of soil chemical elements and played a vital role in the formation of appropriate conditions for nutrient turnover. Thus, soil physical and chemical properties followed the decreasing order of tropical rainforest > rubber rainforest > rubber-tea agroforestry > rubber monoculture. These findings revealed that degraded soil under rubber monoculture converted from tropical rainforest could be restored greatly by converting them into rubber rainforest and then to a climax stage of tropical rainforest after several years of natural succession. s At the start of the rainwater infiltration experiment, preferential flow was the primary water flow behavior. However, both preferential and matrix flow occurred after the soil was saturated with infiltrated water. This co-occurrence of preferential and matrix flow was more prevalent in the rainy season due to the high frequency and amount of rainwater. The preferential flow promoted soil water transport in the water flow paths (e.g., soil macroporosity) and enhanced soil water storage into soil pores. Therefore, the water supply capacity declined in the following order throughout the year: tropical rainforest > rubber rainforest > rubber-tea agroforestry > rubber monoculture. As a result, water stress occurred in RM but was alleviated in RTA and RR. Thus, the potential effects of water flow behaviors on soil properties and forest water conservation function should be considered when converting forests. These results are important for forest management decisions to recover tropical landscapes from devastating rubber plantation (pure and mixed) under a low rubber-latex demand scenario. Declaration of Competing Interest The authors declare that they have no known competing financial interests or personal relationships that could have appeared to influence the work reported in this paper. Acknowledgments The meteorological data was provided by Xishuangbanna Station for Tropical Rainforest Ecosystem Studies. Content determination of available nutrient in soil was accomplished by Institutional Center for Shared Technologies and Facilities of XTBG, CAS. We also thank Mr. Liu MN for his help in the field and laboratory experiments. This research was supported by the National Natural Science Foundation of China ( 32271648 , 32371608 , 32101380 , 32001221 , 32001168 , 32360367 ), the Yunnan Fundamental Research Projects (grant NO. 202201AT070216, 202101AT070056, 202101AS070010, 202101AT070572, 202001AU070131), the ‘Yunnan Revitalization Talent Support Program’ in Yunnan Province, the Youth Innovation Promotion Association CAS (2018430), and the Chinese Academy of Sciences (CAS) ‘‘Light of West China’’ program.
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