title
stringlengths
1
1.19k
keywords
stringlengths
0
668
concept
stringlengths
0
909
paragraph
stringlengths
0
61.8k
PMID
stringlengths
10
11
3.10. Ethical Considerations
Ethical approval was obtained from the University of KwaZulu-Natal Biomedical Research Ethics Committee (BREC), Makerere University, School of Public Health Higher Degrees Research and Ethics Committee (MaKSPH-HDREC), and the Uganda National Council of Science and Technology (UNCST). The UNSCST has guidelines that support primary data collection, and the COVID-19 risk management plan for this project has been developed within the required guidelines.
PMC10454402
4. Conclusions
DISEASE
HPV self-sampling at the HIV clinic could be effective, and would increase the number of women using the service. The prospective implementation of the study will provide insights into the merits and disadvantages of the HPV self-sampling approaches for disease stratification, hence contributing to the best service design for Sub-Saharan Africa. The findings will also be used to guide a step-by-step process for providing HPV self-sampling services at HIV clinics.
PMC10454402
Author Contributions
A.N. conceptualized and designed the study, and prepared the initial draft of the study under the supervision of R.W.M.; T.G.G., R.W.M. and T.G.G. all assisted with the manuscript preparation. All authors have read and agreed to the published version of the manuscript.
PMC10454402
Institutional Review Board Statement
The study was conducted in accordance with the Declaration of Helsinki and approved by the Institutional Review Boards (or Ethics Committee) of Biomedical Research Ethical Committee Higher Degrees (BREC/00002754/2021 and approved on 29 October 2021), Makerere University School of Public Health Higher Degrees Research and Ethics Committee (protocol code SPH-2021-157 approved on 10 January 2022) and Uganda National Council of Science and Technology (HS2084ES approved on 8 June 2022) for studies involving humans.
PMC10454402
Informed Consent Statement
The study was approved by Makerere University School of Public Health Higher Degrees Research and Ethics Committee (SPH-2021-157), and the Uganda National Council of Science and Technology (HS2084ES). All participants provided informed consent, and were allowed to withdraw consent at any time.
PMC10454402
Data Availability Statement
The data from this study are the property of the University of KwaZulu-Natal (UKZN) and Makerere University. All interested readers are required to request the data from Makerere University, School of Public Health through the Principal Investigator, Agnes Nyabigambo. Email:
PMC10454402
Conflicts of Interest
The authors declare no conflict of interest.
PMC10454402
References
The synopsis of the Health Promotion Model for the study.The map shows the location of Luweero district and Luweero district hospital.Process of recruiting women into the study.Description of the clinic-based (intervention) group and home-based (control) group.Sample size estimation for IDI.
PMC10454402
Summary
infection
INFECTION
Joint first authors; contributed equallyJoint senior authors; contributed equallyContributorsNHLL and BJC are the principal investigators of this trial and wrote the study protocol. NHLL, GML, and BJC initiated the trial and acquired funding. NHLL, SMSC, CAC, JSMP, SAV, and BJC designed the laboratory testing. NHLL, SMSC, DKMI, LLMP, JSMP, SAV, and BJC supervised trial activities and laboratory testing. NYMA, LWCF, and YYN managed and conducted trial activities. CAC, LLHL, LCHT, KKHK, SC, AWLC, KCKC, JKCL, PK, and JZJ conducted the laboratory testing. NHLL, CAC, MM-S, NYMA, LWCF, SAV, and BJC performed the data cleaning and analyses. NHLL, SMSC, CAC, MM-S, JSMP, SAV, and BJC wrote the original draft of the manuscript. NHLL, NYMA, and BJC verified underlying data on demographics, vaccination history, reactogenicity, infection, and other epidemiological data of the study. SMSC and JSMP verified underlying data for antibody response. CAC and SAV verified underlying data for cell-mediated response. All authors had full access to all the data in the study and had final responsibility for the decision to submit for publication.
PMC10528748
Background
SARS-CoV-2 infection
SARS-COV-2 INFECTION
Few trials have compared homologous and heterologous third doses of COVID-19 vaccination with inactivated vaccines and mRNA vaccines. The aim of this study was to assess immune responses, safety, and efficacy against SARS-CoV-2 infection following homologous or heterologous third-dose COVID-19 vaccination with either one dose of CoronaVac (Sinovac Biotech; inactivated vaccine) or BNT162b2 (Fosun Pharma–BioNTech; mRNA vaccine).
PMC10528748
Methods
VIRUS, PLAQUE
This is an ongoing, randomised, allocation-concealed, open-label, comparator-controlled trial in adults aged 18 years or older enrolled from the community in Hong Kong, who had received two doses of CoronaVac or BNT162b2 at least 6 months earlier. Participants were randomly assigned, using a computer-generated sequence, in a 1:1 ratio with allocation concealment to receive a (third) dose of CoronaVac or BNT162b2 (ancestral virus strain), stratified by types of previous COVID-19 vaccination (homologous two doses of CoronaVac or BNT162b2). Participants were unmasked to group allocation after vaccination. The primary endpoint was serum neutralising antibodies against the ancestral virus at day 28 after vaccination in each group, measured as plaque reduction neutralisation test (PRNT
PMC10528748
Findings
We enrolled participants from Nov 12, 2021, to Jan 27, 2022. We vaccinated 219 participants who previously received two doses of CoronaVac, including 101 randomly assigned to receive CoronaVac (CC-C) and 118 randomly assigned to receive BNT162b2 (CC-B) as their third dose; and 232 participants who previously received two doses of BNT162b2, including 118 randomly assigned to receive CoronaVac (BB-C) and 114 randomly assigned to receive BNT162b2 (BB-B) as their third dose. The PRNT
PMC10528748
Interpretation
infections
INFECTIONS
Similar levels of incidence of, presumably, omicron BA.2 infections were observed in each group despite very weak antibody responses to BA.2 in the recipients of a CoronaVac third dose. Further research is warranted to identify appropriate correlates of protection for inactivated COVID-19 vaccines.
PMC10528748
Funding
Health and Medical Research Fund, Hong Kong.
PMC10528748
Introduction
infection
INFECTION, CNS INFECTIONS, SARS-COV-2 INFECTION
An unprecedented global effort has led to the rapid development and deployment of COVID-19 vaccines.The COVID-19 vaccination programme in Hong Kong (Special Administrative Region, China) initially offered either two doses of CoronaVac (Sinovac Biotech) 28 days apart or two doses of BNT162b2 (Fosun Pharma–BioNTech in mainland China, Hong Kong, Macau, and Taiwan; Pfizer–BioNTech in other regions) 21 days apart, with broad eligibility criteria and availability. Subsequently, adults were recommended to receive a third dose of either vaccine (ie, allowing crossover) as soon as 90 days after the second dose.Safety, immunogenicity, and efficacy are the main aspects evaluated before vaccines are licensed. Few trialsIn addition, Hong Kong had a large wave of infections in early 2022. Most of the population in Hong Kong was unexposed to SARS-CoV-2 infection by any strain until the end of 2021 due to stringent travel restrictions and community-wide non-pharmaceutical interventions. This lack of exposure allowed us to evaluate the comparative efficacy of these different vaccine combinations against infection with the prevalent omicron BA.2 subvariant in a population in whom any previous immunity was from vaccination only.
PMC10528748
Methods
PMC10528748
Study design
This study was an open-label, randomised trial of third-dose COVID-19 vaccine (either BNT162b2 or CoronaVac) conducted in the community in Hong Kong. The study protocol was approved by the institutional review board of the University of Hong Kong (ethics approval number UW 21–492), and is available in
PMC10528748
Participants
allergies
SARS-COV-2 INFECTION, ALLERGIES
Community-dwelling adults were eligible to participate in this study if they were Hong Kong residents, aged 18 years or older at enrolment, and had previously received a complete primary series of either BNT162b2 or CoronaVac, with the second dose received at least 180 days earlier. Exclusion criteria included a history of confirmed SARS-CoV-2 infection; a delay of 43 days or more between the first two vaccine doses; contraindication for COVID-19 vaccination, such as severe allergies, use of medication that could impair the immune system in the past 6 months (except topical steroids or short-term oral steroids), use of immunoglobulins, or any blood products within 90 days of enrolment; and being pregnant or breastfeeding, or planning to become pregnant (
PMC10528748
Randomisation and masking
ADVERSE REACTIONS
The field investigation team (research assistants and study nurses) performed final participant eligibility screening before enrolling participants during the vaccination visit. The intervention (ie, third-dose vaccination with CoronaVac or BNT162b2) was randomly preassigned to each individual who passed initial eligibility assessment by the online questionnaire system REDCap. The randomisation was based on computer-generated sequences of random numbers produced by NHLL using R software under a block randomisation structure, with block sizes of 2, 4, and 6. Two separate random sequences were generated, one for participants who had previously received two doses of CoronaVac and another for BNT162b2; ie, the four study groups included participants who previously received two doses of CoronaVac and were randomly assigned to receive a third dose of CoronaVac (hereafter CC-C) or BNT162b2 (hereafter CC-B), and participants who previously received two doses of BNT162b2 and were randomly assigned to receive a third dose of CoronaVac (hereafter BB-C) or BNT162b2 (hereafter BB-B). For logistical reasons, individuals were randomly assigned to the intervention at the time vaccination appointments were made; ie, eligible individuals were provided a list of vaccination appointment dates for the same assigned intervention to choose from. There were dropouts after the vaccination appointment was made and before vaccination. However, both the participants and front-line study staff liaising with participants were not aware of the assigned intervention until after vaccination (ie, allocation was concealed) because the vaccination was administered by separate nurses for whom allocation was not concealed: the appointment dates were randomised by computer, and the study principal investigator informed the nurses of the assigned intervention for a vaccination appointment date only a few days beforehand. Nurses with knowledge of group allocation had no further involvement in the trial after administering the intervention. Participants and front-line study staff were unmasked to the type of vaccine received after vaccination through the mandatory government vaccination record. The staff conducting laboratory tests for immunogenicity data were masked to the third-dose allocation until after the laboratory tests were completed. Data on adverse reactions were self-reported by participants with knowledge of group allocation. Data on COVID-19 status based on self-administered rapid antigen tests were self-reported by participants with knowledge of group allocation.
PMC10528748
Procedures
RBD
VIRUS, PLAQUE
Participants received the assigned intervention (ie, intramuscular administration of one dose of CoronaVac or BNT162b2), during the enrolment and vaccination visit (day 0) at the community vaccination centre. CoronaVac is a Vero cell-based, aluminium hydroxide-adjuvanted, β-propiolactone-inactivated monovalent vaccine, and each 0·5 mL dose includes 600 SU of inactivated SARS-CoV-2. BNT162b2 is a nucleoside-modified mRNA monovalent vaccine encoding the trimerised SARS-CoV-2 spike glycoprotein formulated in lipid nanoparticles, and each 0·3 mL dose contains 30 μg of mRNA. Both vaccines were of the ancestral virus formulation. We collected 20 mL blood samples immediately before vaccination and scheduled follow-up blood draws at 28 days, 182 days, and 365 days after vaccination. In a voluntary subset of participants (Details of serological testing, including our in-house ELISA for the receptor binding domain (RBD) of the spike protein, a surrogate virus neutralisation test (sVNT; GenScript, Piscataway, NJ, USA) and a plaque reduction neutralisation test (PRNT), have been described in our earlier studies.
PMC10528748
Outcomes
VIRUS, PLAQUE
The primary outcome measure was vaccine (humoral) immunogenicity at 28 days after the third dose of either BNT162b2 or CoronaVac, measured as geometric mean titre (GMT) of SARS-CoV-2 serum neutralising antibodies against the vaccine strain (ancestral virus) using a plaque reduction neutralisation test (PRNT
PMC10528748
Statistical analysis
infection
ADVERSE EVENTS, INFECTION, SARS-COV-2 INFECTION
Based on our preliminary data, assuming a GMT of 27 with an SD of logFor vaccine immunogenicity (primary outcome), we included data from all participants who received the assigned vaccination and provided days 0 and 28 sera samples in our trial (ie, per-protocol analysis). For adverse events, we included all available data. For SARS-CoV-2 infection, we included data from participants who agreed to participate in active surveillance and had reported at least once self-administered rapid antigen test result from the systematic monitoring, and had also reported information on any infection that occurred before active surveillance started.For SARS-CoV-2 serum neutralising antibody PRNTWe conducted complete case analyses for reactogenicity and incidence of SARS-CoV-2 infection. Rates of solicited local and systemic adverse events or symptoms were compared between study groups using Pearson’s χA data monitoring committee was deemed unnecessary because both vaccines had obtained emergency use approval in the community. The study is registered in
PMC10528748
Role of the funding source
The funder of the study had no role in study design, data collection, data analysis, data interpretation, or writing of the report.
PMC10528748
Results
SARS-CoV-2 infection, infections
MAY, SARS-COV-2 INFECTION, INFECTIONS
From Nov 12, 2021, to Jan 27, 2022, we screened 994 individuals, and 818 (82%) passed the initial eligibility assessment (We collected information on post-vaccination reactions in 424 (94%) of 451 participants, including 193 (46%) of 424 who reported ever feeling unwell after vaccination, with significantly more frequent reactions in recipients of a third dose of BNT162b2 that mostly subsided within 7 days (We measured sera neutralising antibodies from third-dose vaccination in 435 participants who provided paired day 0 and day 28 sera after vaccination (In a random subset of 20 participants from each group (Data on SARS-CoV-2 infection from 378 (84%) of 451 participants were analysed, including 85 (84%) of 101 in the CC-C group, 104 (88%) of 118 in the CC-B group, 96 (81%) of 118 in the BB-C group, and 93 (82%) of 114 in the BB-B group. After receiving third-dose vaccination, and before active surveillance started, 42 infections were identified either by rapid antigen test or PCR, including in ten participants in the CC-C group, 11 in the CC-B group, 11 in the BB-C group, and ten in the BB-B group. During active surveillance from March 11 to May 31, 2022, participants reported a rapid antigen test result, on average, every 4·5 days for a median of 69 days (IQR 60–76). 24 infections were identified either by systematic rapid antigen test or self-reported PCR, including three participants in the CC-C group, eight in the CC-B group, five in the BB-C group, and eight in the BB-B group. A daily symptom diary was initiated for 53 illness episodes from 52 participants, from which 22 infections were identified by rapid antigen test or PCR, including three participants in the CC-C group, nine in the CC-B group, three in the BB-C group, and seven in the BB-B group. Together, we identified 58 SARS-CoV-2 infections by May 31, 2022 (
PMC10528748
Discussion
infection, hypertension
ADENOVIRUS, INFECTION, VIRUS, HYPERTENSION
Here, we have conducted a comprehensive assessment of the reactogenicity, antibody response, T-cell responses and risk of omicron BA.2 infection in a randomised trial of homologous and heterologous boosting with BNT162b2 and CoronaVac, both of which used ancestral virus as the vaccine strain. Our population had minimal COVID-19 history before all three doses of vaccination,Neutralising antibodies were shown to be correlates of protection when comparing mRNA and adenovirus vectored vaccines, and in comparisons between vaccinated and unvaccinated individuals.Our study has several limitations. First, due to logistical challenges, we were only able to randomise at the time vaccination appointment was made, but not at vaccination, and nearly half of randomly assigned individuals dropped out before vaccination. However, the rates of dropout were similar across study groups, and individuals dropping out were not aware of their allocated vaccine type. Comparisons between study groups did not identify significant differences in most baseline characteristics measured, nor any significant differences in antibody and cell-mediated response measured at baseline. Second, there were baseline age differences between the CC-C and CC-B groups, and differences in the proportion of participants with hypertension between the BB-C and BB-B groups, but the differences in neutralising antibodies after third-dose vaccination of CoronaVac versus BNT162b2 remained statistically significant after adjusting for age and hypertension status. Third, we did not include an unvaccinated control group, nor a two-dose comparison group, to evaluate the additional benefits of third dose over existing two doses. Fourth, we have only studied neutralising antibodies and T-cell response, and other branches of immunity, such as non-neutralising antibodies,Most populations received a primary series with mRNA or inactivated COVID-19 vaccines; thus, our findings have wide relevance to booster vaccination policies around the world. Differences in neutralising antibody response are interpreted as indicative of superior efficacy against infection, and have been used as correlate of protection in immunobridging studies for COVID-19 vaccines. The observed discrepancy between neutralising antibody response and vaccine efficacy against infection in our trial might indicate the challenge of using neutralising antibody as the only correlate or mediator of protection against infection,In conclusion, our results suggest there is immune benefit in both administering a homologous or heterologous third dose 6 months after two doses of inactivated or mRNA vaccination, especially in adults who initially received two doses of an inactivated vaccine, with similar levels of protection against infection provided by all four combinations. Mass vaccination programmes that offer both inactivated and mRNA vaccines will allow flexibility in vaccine deployment and encourage vaccine uptake. Our finding that neutralising antibody might not be the dominant correlate of protection for inactivated vaccines, especially against SARS-CoV-2 variants, such as omicron, that have significant capacity to evade neutralising antibody, needs to be considered in the development of variant-proof COVID-19 vaccines or vaccines broadly protective against sarbecoviruses currently in development.
PMC10528748
Supplementary Material
PMC10528748
Acknowledgments
INFECTIOUS DISEASES, ALLERGY
This project was supported by the Health and Medical Research Fund (number COVID19F09), and the Theme-based Research Scheme of the Research Grants Council (RGC) of the Hong Kong Special Administrative Region, China (grant number T11–705/21-N). NHLL is supported by a Health and Medical Research Fund Research Fellowship Scheme grant (number 07210157) from the Health Bureau of the Hong Kong Special Administrative Region, China, and the Takemi Program in International Health (2022–23) at the Harvard T H Chan School of Public Health, Boston, MA, USA. BJC is supported by the National Institute of Allergy and Infectious Diseases, National Institutes of Health, Department of Health and Human Services, under contract number 75N93021C00015, and a RGC Senior Research Fellow Scheme grant (grant number HKU SRFS2021–7S03) from the RGC of the Hong Kong Special Administrative Region, China. We gratefully acknowledge colleagues, including Teresa So, Eileen Yu, Anson Ho, Julie Au, and Lilly Wang for technical and administrative support.
PMC10528748
Declaration of interests
BJC consults for AstraZeneca, Fosun Pharma, GlaxoSmithKline, Haleon, Moderna, Pfizer, Roche and Sanofi Pasteur. BJC has received research funding from Fosun Pharma. All other authors declare no competing interests.For the Chinese translation of the abstract see Online for See Online for
PMC10528748
Data sharing
The individual participant data and data dictionary that underlie the results reported in this Article will be shared after de-identification (ie, text, tables, figures, and appendices). Anonymised individual participant data, the data dictionary, and other supporting clinical documents (eg, study protocol and questionnaires) will be made available with publication to collaborators at local or international universities or research institutes. Proposals for request to collaborate and data access should be directed to BJC (
PMC10528748
References
PMC10528748
Trial profile
A more detailed flow chart with reasons for exclusion at each stage is provided in
PMC10528748
Serum neutralising antibodies measured by live virus PRNT (A–C) or by sVNT (D–F) against ancestral SARS-CoV-2, omicron BA.1, and omicron BA.2, respectively, at baseline and 28 days after randomised third-dose CoronaVac or BNT162b2 vaccination
PRNT titres were evaluated with endpoint at 50% inhibition (PRNT
PMC10528748
IFNγ-producing CD4
The four study groups included participants who previously received two doses of CoronaVac and were randomly assigned to receive a third dose of CoronaVac (CC-C) or BNT162b2 (CC-B), and participants who previously received two doses of BNT162b2 and were randomly assigned to receive a third dose of CoronaVac (BB-C) or BNT162b2 (BB-B). Data were available from a random subset of 20 participants selected from each study group (
PMC10528748
Cumulative incidence of SARS-CoV-2 infection after third-dose CoronaVac or BNT162b2 vaccination in adults who previously received two doses of CoronaVac (A) or BNT162b2 (B) within 4–6 months after vaccination and when the omicron BA.2 subvariant was locally circulating
respiratory illness, COPD, fever
ADVERSE REACTIONS, SARS-COV-2 INFECTION, CHRONIC OBSTRUCTIVE PULMONARY DISEASE, MAY, COPD
COVID-19 was identified by rapid antigen test or PCR between third-dose vaccination (administered from Nov 12, 2021, to Jan 27, 2022) until May 31, 2022. The four study groups included participants who previously received two doses of CoronaVac and were randomly assigned to receive a third dose of CoronaVac (CC-C) or BNT162b2 (CC-B), and participants who previously received two doses of BNT162b2 and were randomly assigned to receive a third dose of CoronaVac (BB-C) or BNT162b2 (BB-B). Data from 378 (84%) of 451 participants who agreed to participate in active surveillance for respiratory illness were included. The date of a positive test for the first SARS-CoV-2 infection identified in these participants was Feb 11, 2022. HR=hazard ratio.Baseline characteristicsData are n (%) or mean (SD). The four study groups included participants who previously received two doses of CoronaVac and were randomly assigned to receive a homologous third dose of CoronaVac (CC-C) or a heterologous third dose of BNT162b2 (CC-B), and participants who previously received two doses of BNT162b2 and were randomly assigned to receive a heterologous third dose of CoronaVac (BB-C) or a homologous third dose of BNT162b2 (BB-B). NA=not applicable. COPD=chronic obstructive pulmonary disease.Solicited local and systemic reactions during the 7 days after third-dose CoronaVac or BNT162b2 vaccinationData are n (%), mean (SD), or median (IQR). The four study groups included participants who previously received two doses of CoronaVac and were randomly assigned to receive a third dose of CoronaVac (CC-C) or BNT162b2 (CC-B), and participants who previously received two doses of BNT162b2 and were randomly assigned to receive a third dose of CoronaVac (BB-C) or BNT162b2 (BB-B). Data from 424 (94%) of 451 participants who reported adverse reactions for at least 7 days post vaccination were included. According to the stratified randomisation, comparison was made between CC-C and CC-B groups, and separately between BB-C and BB-B groups. No participants in the CC-C and BB-C groups reported fever.
PMC10528748
Research in context
PMC10528748
Evidence before this study
infection
INFECTION, VIRUS, SECONDARY
Many low-income and middle-income countries use inactivated COVID-19 vaccines in their existing vaccination programmes, and the use of these vaccines has been proposed in high-income countries; however, data comparing inactivated vaccine efficacy with other vaccine platforms are scarce. We searched PubMed and Web of Science for publications between Jan 1, 2019, and June 22, 2023, with the following search strategy and no restriction on language nor publication type: “((covid) OR (sars-cov-2)) AND (((inactivated vaccine) OR (coronavac) OR (sinovac) OR (BIBP) OR (BBIBP) OR (sinopharm)) AND ((booster) OR (third)) AND (((randomised) OR (randomized)) AND (trial)))”. Included within the 55 identified articles were six randomised trials on heterologous COVID-19 vaccination using inactivated vaccines and mRNA vaccines, including three that studied homologous versus heterologous third-dose (booster) vaccination and included live virus neutralising antibodies as primary or secondary outcomes. These three studies compared third-dose heterologous mRNA vaccination to homologous inactivated vaccination after two doses (primary series) of inactivated vaccines, and suggested third-dose heterologous mRNA vaccination led to higher neutralising antibody response. Only one of the studies also included an efficacy outcome (ie, infection), and showed a relative vaccine efficacy of 38% against symptomatic clinical cases with lower risk of infection in the heterologous mRNA vaccination group. None of the six identified randomised trials included comparisons between third-dose mRNA and inactivated vaccine after a primary series of mRNA vaccination.
PMC10528748
Added value of this study
infection, infections
ADVERSE EVENTS, INFECTION, VIRUS, INFECTIONS
We conducted a comprehensive comparative assessment of homologous versus heterologous COVID-19 vaccination using inactivated vaccines and mRNA vaccines, after both primary series of inactivated vaccines or mRNA vaccines, and simultaneously included safety (adverse events and hospitalisations), immunogenicity (live virus neutralising antibody response and cell-mediated response), and efficacy (breakthrough infections) outcomes. Our results suggest immune benefit, through antibody-mediated or cell-mediated response, or a combination of these responses, in both administering a homologous or heterologous third dose after two doses of inactivated or mRNA vaccination. All four combinations provide similar levels of protection against infection, even in individuals receiving homologous third-dose inactivated vaccine who have low levels of neutralising antibodies against the (mismatched) circulating strain. This finding suggests that neutralising antibody titres might not be the dominant correlate of protection for inactivated vaccines.
PMC10528748
Implications of all the available evidence
Our findings support the benefit of homologous and heterologous booster doses after a primary series of inactivated and mRNA vaccines. All available evidence on vaccine efficacy and effectiveness of inactivated vaccines against variants, compared with the weak neutralising antibody responses conferred by these vaccines, suggest that neutralising antibody levels might not be a sufficient proxy of vaccine efficacy (ie, correlate of protection) in immunogenicity trials or immunobridging studies for inactivated vaccines. Further research is needed to identify how different SARS-CoV-2 vaccine platforms might provide protection via different immune mechanisms. There is an urgent need to identify a correlate of protection for inactivated COVID-19 vaccines, or correlates that might provide information on breadth of protection for all vaccine platforms.
PMC10528748
Background
Edited by: Agnes Szilagyi, Semmelweis University, HungaryReviewed by: Morayma Reyes-Gil, Montefiore Medical Center, United States; Giuseppe Remuzzi, Istituto di Ricerche Farmacologiche Mario Negri IRCCS, Italy†These authors share senior authorshipConestat alfa (ConA), a recombinant human C1 inhibitor, may prevent thromboinflammation.
PMC10641758
Methods
DISEASE, SECONDARY
We conducted a randomized, open-label, multi-national clinical trial in which hospitalized adults at risk for progression to severe COVID-19 were assigned in a 2:1 ratio to receive either 3 days of ConA plus standard of care (SOC) or SOC alone. Primary and secondary endpoints were day 7 disease severity on the WHO Ordinal Scale, time to clinical improvement within 14 days, and safety, respectively.
PMC10641758
Results
The trial was prematurely terminated because of futility after randomization of 84 patients, 56 in the ConA and 28 in the control arm. At baseline, higher WHO Ordinal Scale scores were more frequently observed in the ConA than in the control arm. On day 7, no relevant differences in the primary outcome were noted between the two arms (
PMC10641758
Conclusion
The study results do not support the use of ConA to prevent COVID-19 progression.
PMC10641758
Clinical trial registration
PMC10641758
Introduction
CORONAVIRUS DISEASE 2019
Numerous efforts have been made to develop effective treatments for individuals who have been hospitalized with Coronavirus disease 2019 (COVID-19) (Conestat alfa (Ruconest
PMC10641758
Materials and methods
PMC10641758
Study design and patients
obesity, pneumonia, allergy, renal disease, shortness of breath
OBESITY, DISEASE PROGRESSION, PNEUMONIA, ALLERGY, LIVER DISEASE, RENAL DISEASE
This was a randomized, parallel-group, open-label, multi-center trial. The study protocol was published elsewhere (Male and non-pregnant female patients (18–85 years of age) were eligible and approached by study physicians of the participating centers if they had a diagnostic specimen that was positive for SARS-CoV-2 on reverse-transcriptase–polymerase-chain-reaction (RT-PCR), had pneumonia confirmed by chest imaging, and onset of symptoms ≤10 days or shortness of breath ≤5 days. The latter criterion was adapted/added with an amendment 4 months after approval of the first study protocol, because of the changing patient behaviors over time when seeking for medical help after a positive SARS-CoV-2 test. In addition, at least one of the following risk factors for disease progression was required for enrollment: arterial hypertension, age ≥ 50 years, obesity (BMI ≥ 30.0 kg/mExclusion criteria included refusal to participate, history or suspicion of allergy to rabbits or the study drug, pregnant or breast-feeding individuals, known severe liver disease, and renal disease requiring dialysis. Patients who received tocilizumab or another IL-6 or IL-6 receptor inhibitor prior to enrollment were not eligible for this study. Patients currently requiring intensive care (or expected to do so) within 24 h after initial presentation were not eligible for this study, because “prevention of disease progression” was investigated. Hospitalized patients requiring high-flow oxygen therapy on medical wards were eligible for inclusion.
PMC10641758
Standard-of-care therapy, randomization, and study medication
PMC10641758
Randomization
Study participants were randomized in a 2:1 ratio using permuted-block allocation with varying block sizes. Randomization was stratified by the study site, generated by an independent statistician, and implemented via the electronic data capture system software SecuTrial
PMC10641758
Intervention arm
Patients allocated to the intervention arm received a total of nine intravenous ConA doses over 72 h (8,400 U followed by 4,200 U every 8 h), in addition to SOC treatment.
PMC10641758
Control arm
Patients allocated to the control arm received SOC only.
PMC10641758
Monitoring, outcomes, and follow-ups
death, acute lung injury
ADVERSE EVENTS, DISEASE, SECONDARY
Data on vital signs, disease severity according to WHO scale, clinical improvement, admission to ICU, and requirement for non-invasive or invasive ventilation were prospectively obtained. Virological clearance (time from positive to negative PCR test results in nasopharyngeal samples), hematological, liver, renal, and inflammatory parameters in laboratory examinations were monitored during the first 14 days of hospitalization or until discharge. C1INH antigen and C4 concentrations were determined on semi-automated platforms in the clinical laboratories in all except two study centers (not monitored in Monterrey, Mexico and Zurich, Switzerland). Additional EDTA- and citrate-plasma as well as serum samples were frozen at −80°C and subsequently analyzed for concentrations of C4d (Svar Life Sciences, Malmö, Sweden), sC5b-9 (BD Biosciences Pharmingen, San Diego, CA, USA), VCAM-1 and E-selectin (ProteinSimple, Bio-techne, Minneapolis, MN, USA), and kallikrein-like activity (Unitest, Haemochrome Diagnostica, Essen, Germany) according to the manufacturer’s instruction.Final follow-up included a structured telephone interview or study visit (if still hospitalized) 28 days after enrollment to assess adverse events (AEs) and outcome. Afterwards, serious adverse events (SAEs) were followed until resolution, stabilization, or death, whichever occurred first.The primary endpoint was disease severity on the WHO Ordinal Scale on day 7. For statistical analysis, the scores 6 and 7 were combined into one score. Secondary endpoint included time to clinical improvement within 14 days after enrollment. It was defined as improvement of two points on the WHO Ordinal Scale or live hospital discharge, whatever occurred first. Other secondary endpoints included the proportion of participants alive and not having required invasive or non-invasive ventilation at day 14 day, and the proportion of subjects with an acute lung injury. The latter was defined by the presence of PaO
PMC10641758
Safety evaluations
The overall incidence of AEs and SAEs were assessed during a 4-week follow-up and documented by the investigators according to seriousness, intensity, causal relationship with study treatment, action taken with study treatment (e.g., withdrawal), specific treatment for AE, and outcome.AE and SAEs were grouped by the organ class system (
PMC10641758
Statistical plan and analysis
SECONDARY
Full analysis set and intent-to-treat population (FAS/ITTP) was defined as all patients who were randomly allocated to a study arm. The primary efficacy analysis was based on the FAS/ITT population. The primary endpoint was analyzed by Wilcoxon test stratified by its baseline values with a two-sided α-level of 5%. The secondary endpoints were tested after a significant test of the primary endpoint (Quantitative secondary study parameters were described based on their mean, standard deviation (SD), median, interquartile range (IQR), minima, and maxima and portrayed by Kaplan–Meier plots and compared with the log rank test. Qualitative secondary study parameters were analyzed by means of absolute and relative frequencies: Chi-square tests were carried out in order to compare the active treatments to SOC. With a two-sided significance level of α = 0.05 and a power of 1 − β = 0.80, a sample size of 76 (2 × 38) was calculated for a fixed sample size design and an advantage of at least 1 point on the WHO Ordinal Scale (SD 1.5 points) (The independent clinical trial statistician of CRM Biometrics GmbH, the first author (PU), and last author (MO) analyzed the data and had access to all data. All authors had access to primary clinical trial data only related to their institution. Study participants, treating physicians, nurses, investigators, and DSMB members were not blinded.
PMC10641758
Results
PMC10641758
Patient characteristics
SD, COPD
CHRONIC OBSTRUCTIVE PULMONARY DISEASE, COPD
Between August 2020 and March 2021, 621 patients were screened and 84 were enrolled (Baseline characteristics.ACE, angiotension-converting enzyme; ARB, angiotension receptor blocker; BMI, body mass index; COPD, chronic obstructive pulmonary disease; SD, standard deviation.
PMC10641758
Endpoints
DISEASE
Disease severity on day 7, the primary endpoint, was not different in the two groups (Disease severity at day 7.Disease severity on day 7 stratified by baseline scores.Kaplan–Meier curve for the time to clinical improvement within 14 days according to the treatment group.
PMC10641758
Laboratory analyses
Analysis of C1INH concentrations revealed elevated values in both groups at baseline (Course of main laboratory parameters from baseline until day 7 according to the treatment group. Course of
PMC10641758
Safety
PMC10641758
Adverse events
Twenty-two subjects had at least one AE: 17 (30%) in the intervention arm and 5 (19%) in the control arm. Overall, 35 AEs were reported: 30 (85.7%) in the interventon arm and 5 (14.3%) in the control arm. Ten of these AEs were attributed to investigations [i.e., laboratory parameters: eight (80.0%) in the intervention arm and two (20.0%) in the control arm]. Details are listed in
PMC10641758
Serious adverse events
thoracic and mediastinal disorders
CARDIAC DISORDERS
These occurred in 15 (27%) patients in the intervention arm and 4 (15%) in the control arm. The most common system organ classes of the SAEs were “respiratory, thoracic and mediastinal disorders” [10 (17.9%) and 2 (7.4%)], “infections and infestations” [6 (10.7%) and 1 (3.7%)], and “cardiac disorders” [3 (5.4%) and 0]. Details are listed in None of the AEs or SAEs were judged as being related to the study drug by the investigators.
PMC10641758
Premature trial determination
deaths
While SAEs and deaths were judged as not related to the trial medication, their increased occurrence in the intervention arm led the DSMB to recommend an interruption of the trial after the second interim analysis. In addition, the DSMB recommended to await the outcome data of this analysis, including analyses of the activity of the plasma cascades prior to further decision-making on cessation or continuation of the trial. Subsequently, the trial was terminated prematurely in September 2021 for the following reasons. First, the intervention regimen was not associated with a significant inhibition of the CS and activation of other plasma cascades or endothelial cells. Second, considering the results in the primary outcome not favoring the intervention and the observed imbalances in the baseline characteristics, a larger sample size would have been required to show a difference if there was a true difference. Third, during the second half of the year 2021, additional treatment options such as anti-SARS-CoV-2 monoclonal antibodies and tocilizumab were introduced and recommended, making the study groups even more heterogeneous.
PMC10641758
Discussion
pneumonia, non-critically ill COVID-19 infection, SAEs, infection, viral infections, non-critically ill, sepsis
DISEASE PROGRESSION, PNEUMONIA, DISEASE, VIRAL INFECTION, COMPLICATION, INFECTION, SECONDARY, SEPSIS
This randomized trial found that C1INH treatment added to SOC was not associated with clinical improvement or faster recovery from COVID-19 in comparison with SOC alone in hospitalized, non-critically ill patients. The overall mortality in this trial (7%) was substantially lower than the one previously reported in the dexamethasone trial (23%), published by the RECOVERY collaborative group (The conduction of this trial was justified by scientific rationales and a previous pilot study (First, the administration of ConA may have been too late in the course of COVID-19. Because of the short half-life of ConA, repeated administration of ConA over 3 days was chosen. The dosage chosen was supposed to increase the C1INH concentrations by at least 50%. Pharmacokinetic analyses revealed that C1INH concentrations were already markedly elevated at baseline in both arms, which is in agreement with our previous data (Second, the dosing regimen may have been unable to inhibit the CS in COVID-19 sufficiently and for a prolonged period of time. C1INH concentrations doubled initially after the first administration of ConA but returned to almost baseline before the 4th administration. The exact concentration required to inhibit the complement and other cascades and the optimal target are unknown both in the specific context of COVID-19 and in hyperinflammation secondary to infection in general. Of note, COVID-19 is characterized by a local activation of plasma cascades that progresses to a systemic activation early in the disease (Third, in COVID-19, the potential inhibitory role of C1INH may have been overestimated when considering activation through the classical and alternative pathway (Fourth, cross-activation of the CS downstream of the lectin and classical pathway proteases may play a considerable role in COVID-19 disease progression. For example, factor XIa inhibited the regulatory complement factor H of the alternative pathway enhancing alternative pathway activity (The CS has been a target of a number of randomized controlled trials in COVID-19. However, only retrospective data from patients requiring continuous positive airway pressure support (This trial was designed early during the pandemic. As such, it was decided that instead of defining futility margins for a rather small-scale trial including a diverse patient population, a regular review of the DSMB might be more appropriate, as the included patients would potentially receive various new treatments with poorly known safety profiles as time evolved. Instead, two adaptive interim analyses after 40 and 80 patients were carried out. Although more SAEs occurred in the intervention arm, the majority of them were noted after the intervention period. In agreement with external evaluations, we attributed most SAEs to COVID-19 or a complication of it (e.g., pneumonia or sepsis). This interpretation is also supported by the observation of more severe COVID-19 at baseline and throughout the study period in the intervention arm. Of note and in contrast to C5 inhibitory strategies, C1INH treatment has not been associated with an increased risk for bacterial or viral infections or any effect on viral replication (Our study has limitations. These include the premature closure of the trial, the lack of prespecified futility margins, the small number of patients in the control arm (due to the 2:1 randomization), and the imbalances in baseline characteristics and disease severity observed between the groups at baseline (potentially due to the 2:1 randomization and stratification in the setting of a limited number of enrolled patients). Almost 50% of patients were recruited in one center, reflecting an uneven distribution between the institutions. It was an open-label trial, and as such, it may have been prone to bias. The SOC treatment allowed the use of remdesivir and dexamethasone, which may have diminished the possible effect of ConA. Last but not least, follow-up phone calls might potentially have been less accurate than in-person follow-up visits when assessing for AEs. Despite these limitations, this is the largest study to investigate a treatment strategy that interferes with the CS, KKS, and CAS in hospitalized COVID-19 patients. In addition, we provide patient-matched laboratory data regarding the inability of ConA to limit the activation of these plasma cascades in COVID-19.In conclusion, ConA did not significantly accelerate clinical improvement or reduce mortality in hospitalized patients with non-critically ill COVID-19 infection. The chosen dose and regimen of ConA used in this study are insufficient to limit complement activation in COVID-19. It remains unclear whether or not higher dosages, a longer treatment regimen, or an earlier intervention time point with ConA in COVID-19 could have prevented disease progression.
PMC10641758
Data availability statement
The raw data supporting the conclusions of this article will be made available by the authors, on reasonable request.
PMC10641758
Ethics statement
The studies involving humans were approved by the ethics committees «Ethikkommission Nordwest- und Zentralschweiz», «Ethikkommission Ostschweiz», and “Kantonale Ethikkommission Zürich» in Switzerland, “Comissâo Nacional de Ética Em Pesquisa” (CONEP) in Brazil and “Comisión Federal Para La Protección Contra Riesgos Sanitarios” (COFEPRIS) in Mexico. The studies were conducted in accordance with the local legislation and institutional requirements. The participants provided their written informed consent to participate in this study.
PMC10641758
Author contributions
PU: Conceptualization, Data curation, Formal Analysis, Investigation, Methodology, Project administration, Supervision, Visualization, Writing – original draft, Writing – review & editing. ML: Investigation, Project administration, Writing – review & editing. PC: Investigation, Project administration, Writing – review & editing. SM: Investigation, Project administration, Writing – review & editing. IH: Conceptualization, Investigation, Methodology, Writing – review & editing. MT: Investigation, Project administration, Supervision, Writing – review & editing. RT: Investigation, Project administration, Writing – review & editing. JS: Investigation, Project administration, Writing – review & editing. AC: Investigation, Project administration, Supervision, Writing – review & editing. MB: Investigation, Project administration, Supervision, Writing – review & editing. LH: Investigation, Project administration, Supervision, Writing – review & editing. MS: Investigation, Project administration, Writing – review & editing. WA: Investigation, Project administration, Supervision, Writing – review & editing. PS: Conceptualization, Formal Analysis, Investigation, Methodology, Project administration, Supervision, Validation, Writing – original draft, Writing – review & editing. MO: Conceptualization, Data curation, Formal Analysis, Funding acquisition, Investigation, Methodology, Project administration, Resources, Supervision, Validation, Visualization, Writing – original draft, Writing – review & editing.
PMC10641758
Acknowledgments
We thank the trial participants, caregivers, investigators, and research staff who contributed to the trial. We are particularly thankful to the nurses and physicians who cared for the COVID-19 patients during stressful times of the pandemic. We thank Pharming Biotechnologies B.V., Leiden, The Netherlands, for providing ConA (Ruconest®) free of charge.
PMC10641758
Conflict of interest
MT reports receiving grants from the Swiss National Science Foundation, and having research collaborations with Roche, Novartis, and Idorsia outside the submitted work. WA reports receiving fees and research grants from A. Vogel AG, Gilead, and OM Pharma and fees for attendance of advisory boards to Pfizer, MSD Vifor Pharma, GSK, Sanofi, OM Pharma, and Janssen that were paid to his institution outside the submitted work. MO reports receiving grants from the Swiss National Science Foundation, consulting fees from Pharming Biotechnologies B.V. during the conduct of the study and grants from Pharming Biotechnologies B.V. outside the submitted work. LH reports receiving consulting fees from GlaxoSmithKline and Novartis during the conduct of the study but unrelated to this trial.The remaining authors declare that the research was conducted in the absence of any commercial or financial relationships that could be construed as a potential conflict of interest.The authors declare that this study received funding from Pharming Biotechnologies B.V. The funder was involved in the design of the study at an initial stage and in the trial organization of the study in Brazil and Mexico (e.g., shipment of study drug).
PMC10641758
Publisher’s note
All claims expressed in this article are solely those of the authors and do not necessarily represent those of their affiliated organizations, or those of the publisher, the editors and the reviewers. Any product that may be evaluated in this article, or claim that may be made by its manufacturer, is not guaranteed or endorsed by the publisher.
PMC10641758
Supplementary material
The Supplementary Material for this article can be found online at: Click here for additional data file.
PMC10641758
References
PMC10641758
Abstract
DeceasedPrincipal Investigator: Kentaro YamazakiHiroya Taniguchi and Kentaro Yamazaki Contributed equally as co-first authors.
PMC10628564
Background
METASTATIC COLORECTAL CANCER
In this phase Ib study MODURATE, we optimized the dosing schedule and tested the efficacy and safety of trifluridine/tipiracil, irinotecan, and bevacizumab in patients with metastatic colorectal cancer with fluoropyrimidine and oxaliplatin treatment failure.
PMC10628564
Methods
We included a dose escalation (3 + 3 design) and an expansion cohort. Patients were administered trifluridine/tipiracil (25-35 mg/m
PMC10628564
Results
toxicities
Twenty-eight patients were enrolled. Five dose-limiting toxicities were observed. RP2D was defined as trifluridine/tipiracil 35 mg/m
PMC10628564
Conclusion
myelotoxicity
METASTATIC COLORECTAL CANCER
Biweekly trifluridine/tipiracil, irinotecan, and bevacizumab administration may have moderate antitumor activity with high risk of severe myelotoxicity in previously treated patients with metastatic colorectal cancer [UMIN Clinical Trials Registry (UMIN000019828) and Japan Registry of Clinical Trials (jRCTs041180028)].In this phase Ib study, MODURATE, efficacy and safety of trifluridine/tipiracil, irinotecan, and bevacizumab was tested in patients with metastatic colorectal cancer with fluoropyrimidine and oxaliplatin treatment failure
PMC10628564
Lessons Learned
myelotoxicity
METASTATIC COLORECTAL CANCER
The recommended dose was determined as trifluridine/tipiracil of 35 mg/mBiweekly trifluridine/tipiracil, irinotecan, and bevacizumab administration may have moderate antitumor activity with high risk of severe myelotoxicity in previous treated metastatic colorectal cancer patients.
PMC10628564
Discussion
mCRC, tumor, DLTs, myelosuppression
METASTATIC COLORECTAL CANCER, DISEASE, METASTATIC GASTRIC CANCER, TUMOR
Refractory metastatic metastatic colorectal cancer (mCRC) treatment with trifluridine/tipiracil (FTD/TPI) combined with bevacizumab (BEV) or irinotecan (IRI) showed enhanced therapeutic effects in preclinical models.In 18 patients of the dose escalation part, 5 DLTs occurred. We determined that the recommended phase II dose (RP2D) could be defined as FTD/TPI 35 mg/mIn the entire population, at a median follow-up time of 417 (range, 346-611) days, the overall response rate (ORR) was 21%; 6 patients achieved partial response in 28 patients. The disease control rate (DCR) was 79% (Waterfall plot: maximum tumor shrinkage from baseline.Kaplan-Meier plots: progression-free survival (left) and overall survival (right).Even with biweekly administration of FTD/TPI, the combination of FTD/TPI, IRI plus BEV produced a high rate of myelosuppression. The preliminary efficacy results showed comparable antitumor activity compared to the standard FOLFIRI regimen. Continued investigation of this regimen may be possible in other patient populations such as metastatic gastric cancer.
PMC10628564
Additional Details of Endpoints or Study Design
PMC10628564
Study design:
This study was conducted using an open-label, nonrandomized, 2-part phase Ib design and was carried out at 2 centers. The study population consisted of a dose escalation cohort (part 1) to establish the recommended phase II dose (RP2D) for biweekly administration of the combination of FTD/TPI, IRI, and BEV, and an expansion cohort (part 2) for further investigation of safety and provision of a preliminary assessment of the antitumor activity of the combination regimen at the RP2D in patients with mCRC in whom fluoropyrimidine and oxaliplatin treatment had failed.
PMC10628564
Eligibility criteria:
Tumors, failure of or intolerance
ONCOLOGY, TUMORS
Eligible patients were aged 20-75 years with histologically confirmed CRC, failure of or intolerance to fluoropyrimidine and oxaliplatin treatment (those who showed relapse fewer than 6 months after administration of the final dose of adjuvant chemotherapy were also eligible), and no prior therapy with FTD/TPI and IRI. Additional inclusion criteria included an Eastern Cooperative Oncology Group (ECOG) performance status of 0-1, adequate organ function (bone marrow, liver, and kidney), and at least one measurable metastatic lesion assessed according to the revised Response Evaluation Criteria In Solid Tumors (RECIST), version 1.1.
PMC10628564
Dose escalation:
toxicity
The dose escalation cohort was formulated based on a traditional 3 + 3 design in which patients in sequential dose-level cohorts received increasing doses of FTD/TPI (25, 30, or 35 m/m2/dose, twice per day for days 1-5) and IRI (150 or 180 mg/mAt least 3 evaluable patients were treated with each dose; 6 patients were treated at the RP2D. An increase in subsequent doses was allowed only after the previous dose was determined to be safe as per protocol. Intra-patient dose escalation was not permitted. The RP2D was defined as the highest dose at which 1/3 or 2/6 of the treated evaluable patients experienced dose-limiting toxicity (DLT) during cycles 1 or 2. The expansion cohort was initiated as soon as the RP2D had been established; up to 15 patients were enrolled in parallel and administered FTD/TPI and IRI with BEV at the RP2D.
PMC10628564
Evaluation
gastrointestinal symptoms, tumor, neutropenia, febrile neutropenia, toxicity, thrombocytopenia, hypertension, Cancer
ADVERSE EVENT, TUMOR, NEUTROPENIA, FEBRILE NEUTROPENIA, ADVERSE EVENT, THROMBOCYTOPENIA, HYPERTENSION, CANCER
The primary endpoint was determination of the RP2D in the dose escalation cohort and frequency of febrile neutropenia in the expansion cohort. Adverse events (AEs) were graded according to the National Cancer Institute (NCI) Common Terminology Criteria for Adverse Events version 4.03. A DLT was defined as a cycle of one or 2 AEs that met one of the following criteria: grade 4 neutropenia lasting >7 days; grade ≥3 febrile neutropenia, grade 4 thrombocytopenia, or grade 3 thrombocytopenia requiring platelet transfusion; drug-related toxicity resulting in a >14-day delay in starting cycle 2 or 3; and grade ≥3 non-hematologic toxicity except for the following AEs: (1) grade ≥3 gastrointestinal symptoms that could be controlled by supportive care; (2) electrolyte and γGTP abnormalities; and (3) grade ≥3 hypertension that could be controlled. The population assessed for treatment safety included all patients who received one or more doses of the study drug.Antitumor responses were evaluated using RECIST version 1.1; each investigator performed tumor assessments at baseline and every 8 weeks and 12 weeks after week 32. Patients who had completed one or more treatment cycles and had undergone radiological/clinical progression assessments were evaluable for efficacy determination.
PMC10628564
Statistical analyses:
Descriptive statistics were used to summarize patient characteristics and safety and efficacy of the treatment. OS and PFS were estimated using the Kaplan-Meier method. The median OS and PFS and their 95% CIs were analyzed. Log-rank tests were used to compare differences in survival rates. All tests were 2-sided with a significance level of 0.05. All data summaries and listings were produced using R version 4.0.5 (Vienna, Austria).
PMC10628564
Adverse Events
PMC10628564
Assessment, Analysis, and Discussion
PPTD, DLTs, diarrhea, toxicities, perforation, proteinurea, myelotoxicity, anorexia
EVENTS, HYPERTENSION, METASTATIC GASTRIC CANCER, ANOREXIA
This phase Ib study indicated that combining IRI and BEV with biweekly FTD/TPI is safe for mCRC treatment. In Japanese mCRC patients pretreated with fluoropyrimidine and oxaliplatin, this regimen showed modest efficacy in this pilot study. To the best of our knowledge, this is the first study to evaluate such a triple combination with biweekly administration of FTD/TPI in Asian patients.Five DLTs occurred in the dose escalation part of the study. We determined that the RP2D could be defined as FTD/TPI 35 mg/mThe triple drug combination was tolerable, and no drug-related AE was observed other than those that might be expected. Most drug-related AEs were grade 3-4 hematological events that could be managed by delay in the treatment schedule, dose reduction, and basic supportive care. Gastrointestinal toxicities such as anorexia and diarrhea were mainly grade 1 or 2 and related to FTD/TPI and IRI, which was also within our expectations. In addition, grade 3 hypertension, proteinurea, and perforation related to BEV were observed in <10% of our patients. AEs were managed using dose reduction and dose delay, with only 2 treatment-related AEs resulting in treatment discontinuation. Thus, the overall safety profile of this regimen is consistent with the expected toxicities of the individual agents, with no unanticipated safety issue.The preliminary efficacy results showed modest antitumor activity in this trial. We reported an ORR of 19% and PFS of 7.1 months in the RP2D population, which is numerically better compared to previous trials of those for other conventional chemotherapies, including FOLFIRI in combination with anti-VEGF as second-line therapy.The limitation of this study is that it was a nonrandomized prospective trial with a small sample size. In particular, because the PPTD population consisted of only 16 patients, it was difficult to accurately assess efficacy in such a heterogeneous group with various prognostic factors such as RAS status and previous treatment with biologics. Given the study design, it was also difficult to determine the most appropriate IRI dose between 150 mg/mIn conclusion, this dose escalation/expansion study indicated that treatment with a triple combination of FTD/TPI, IRI, and BEV has moderate antitumor activity with severe but manageable myelotoxicity for mCRC after failed standard first-line therapy with fluoropyrimidines and oxaliplatin. Continued investigation of this regimen may be possible in other patient populations such as metastatic gastric cancer.
PMC10628564
Acknowledgments
The authors thank all clinicians for their involvement and contribution to the study. This study was supported by the Fuji Pharma Valley Center, a nonprofit organization.
PMC10628564
Funding
This study was funded by Taiho Pharmaceutical Co., Ltd under a research contract.
PMC10628564
Conflict of Interest
Hiroya Taniguchi reported research funding from Taiho and Daiichi-Sankyo, and honoraria from Taiho, Chugai, Daiichi-Sankyo, and Yakult Honsha. Kentaro Yamazaki reported research funding from Taiho and Daiichi-Sankyo, and honoraria from Taiho, Chugai, Daiichi-Sankyo, and Yakult Honsha. Toshiki Masuishi reported research funding from Daiichi-Sankyo and honoraria from Taiho, Chugai, Daiichi-Sankyo, and Yakult Honsha. Takeshi Kawakami reported honoraria from Taiho, Daiichi-Sankyo, and Yakult Honsha. Shigenori Kadowaki reported research funding and honoraria from Taiho, Chugai, and Daiichi-Sankyo. Kei Muro reported research funding from Taiho, Chugai, and Daiichi-Sankyo, and honoraria from Taiho, Chugai, and Daiichi-Sankyo, Yakult Honsha. The other authors indicated no financial relationships.
PMC10628564
Data Availability
The data underlying this article will be shared on reasonable request to the corresponding author.
PMC10628564
References
PMC10628564
2. Materials and Methods
PMC10745664
2.1. Test Products
DECAY
The study design and test product composition have been described in detail previously [The group receiving fermented aronia extract will be referred to as FAE and the group receiving non-fermented aronia extract as AE. The aronia extracts were based on aronia berry pulp. The FAE and AE groups were supplemented with snack bars that administered approximately 893 mg or 533 mg anthocyanins, respectively, per day. Measurements on anthocyanin content were made by Elkaerholm (Egtved, Denmark) prior to the study, and since anthocyanins decay over time, the amount of provided anthocyanins might have decreased towards the end of the study. In order to minimize the decay, the supplements were stored in the dark at −18 °C. The nutritional composition is outlined in
PMC10745664
2.2. Study Design and Participants
RECRUITMENT
This study was carried out at the Department of Endocrinology and Internal Medicine, Aarhus University Hospital, Denmark, spanning the period from December 2020 to April 2022. The study adhered to the principles outlined in the Declaration of Helsinki and received approval from The Central Denmark Region Committees on Health Research Ethics (Journal no. 1-10-72-102-19). Furthermore, the study was enlisted on Advertisements in local newspapers, a dedicated recruitment website (“Pre and post each supplementation period, we assessed 24 h ambulatory blood pressure and took fasting blood samples to quantify lipids, adiponectin, and hs-CRP levels.
PMC10745664
2.3. 24 h Ambulatory Blood Pressure Monitoring
pain
The monitoring of 24 h ambulatory blood pressure was conducted using ambulatory blood pressure monitors (Spacelabs Medical, Ebeltoft, Denmark). The monitors were calibrated to measure blood pressure with a half-hour span between 7:00 AM and 11:00 PM, and with an hour span between 11:00 PM and 7:00 AM Participants recorded wake-up and bed times. Using this information, computer software (Sentinel, Ebeltoft, Denmark, version 11.5.2.13260) calculated systolic and diastolic blood pressure measurements for the entire monitoring period, as well as separately for the sleeping and waking periods. One participant who completed the trial did not complete the blood pressure monitoring due to experiencing pain during the measurements.
PMC10745664
2.4. Blood Analyses
BLOOD
Blood samples were collected following an eight-hour fasting period and promptly underwent centrifugation at 4 °C and 3989 RPM for 10 min. The resulting plasma samples were preserved at −80 °C until the end of the study, when samples from all participants were analysed together.
PMC10745664
2.4.1. Hs-CRP and Adiponectin
Hs-CRP and adiponectin concentrations were measured using non-competitive, time-resolved immunofluorometric assays. The method for the determination of hs-CRP has been described previously by Reinhard et al. [
PMC10745664
2.4.2. Lipids
The Department of Clinical Biochemistry at Aarhus University Hospital, Denmark (DS/EN ISO 15189:2013 approved [
PMC10745664
2.5. Power Calculation
Based on a power calculation which has been described previously [
PMC10745664
2.6. Statistics
Statistical analysis was performed in collaboration with a medical statistician who provided the code for the fitting of a linear mixed effects model in Rstudio (Rstudio, Package lme4). As fixed effects, we included the treatment order (six possible orders), period (first, middle, last), treatment (FAE, AE, placebo), and time (pre, post), along with the interaction between treatment and time. As random effects, we included record id and record id within period. Standard normality tests of residuals were conducted, including quantile-quantile plots and histograms, along with plots of residuals versus fitted values. We used the Rstudio package emmeans to compute estimated marginal means from the mixed model. We will simply refer to the estimated marginal means as ‘means’ throughout this article. We also compared mean differences (Δ-mean) between the three supplementations and obtained the corresponding If values were below the lower level of detection in the previously described assays, we imputed these values as half of the lower limit of detection for the respective assays. We assessed the baseline data for normality, and for normally distributed data, we will report the results as mean ± standard deviation (SD). Non-normally distributed data will be reported as the median along with the interquartile range (IQR).
PMC10745664
3. Results
PMC10745664