Only a small percentage of patients who have infections with organisms such as Campylobacter, Salmonella, Shigella, or Yersinia develop ReA [27].

Similarly, amongst millions who have developed SARS-CoV-2 infection, only a minor propor- tion develops arthritis.

Understanding this may help unearth new verities about the immune system and tolerance mechanisms.


Post COVID-19 arthritis more commonly has a rheuma- toid like phenotype affecting the wrists, ankles, and small 1642 Clinical Rheumatology (2022) 41:1641-1652 joints of hands and feet.

However, a spondyloarthritis-like presentation with axial involvement has also been reported [28].

It can also present as classical ReA with lower limb predominant oligoarthritis [29].

Isolate monoarthritis of a single metacarpophalangeal joint has also been reported [30].

Table 1 summarizes the different phenotypes, treat- ments given, and outcomes in various case reports of post- COVID-19 reactive arthritis from across the world.


The initial reports of post-COVID-19 ReA were in men past 50 years of age [31-33, 35].

This is in contrast to the clas- sical ReA that is most common between 15 and 40 years of age.

Again, at least three cases of post-COVID-19 ReA have also been reported in the paediatric age group [41, 45].

Unlike classical ReA, gender distribution appears equal between males and females.

However, the total number of reported cases is too small for conclusive comments.


Thus, the phenotype and outcomes of post-COVID-19 ReA appear to be different from those of classical ReA. These differences are summarized in Table 2.


Vaccination-induced autoimmunity is a concern since vac- cines stimulate the immune system [51].

The first published case of ReA post-COVID-19 vaccination was reported in a 23-year-old woman after the inactivated Sinovac-CoronaVac vaccine [52].

We could identify a total of seven cases of inflammatory arthritis reported post-vaccination (Table 3).


We have reviewed post-COVID-19 rheumatic diseases at an earlier stage of the pandemic [57].

Post-COVID-19 periph- eral nerve entrapment syndromes like carpal tunnel or tarsal tunnel syndromes have been hypothesized to be either due to localized demyelination, microangiopathy involving the vasa nervosum or an immune phenomenon targeting the adjacent synovial sheath [58].

An interesting group is the patients who have clinical phenotype and antibodies sug- gestive of rheumatoid arthritis developing post-COVID-19.

These patients developed anti-cyclic citrullinated peptide antibody-positive arthritis after documented COVID-19 infection [48-50].


One concern was whether vaccination would cause a flare in persons with pre-existing autoimmune diseases [51].

Cases with flares of RA temporarily related to vacci- nation have been reported [59].

However, in a cohort of 724 patients with autoimmune rheumatic disease, only 4 patients had complained of a flare in joint pain.

This was managed with NSAIDs and lasted less than a week [60].


In a cohort of 5493 RA patients from Hong Kong, a pro- pensity-score weighted multivariate analysis did not show any association with COVID-19 vaccination and flare of RA [61].


Several viruses are associated with acute polyarthritis that lasts less than 6-8 weeks [62].

In a small proportion of cases, such viral arthritis may become chronic such as in the case of HIV (Human Immunodeficiency Virus), Hepatitis B and C viruses [63, 64], parvovirus B19, and Chikungunya [65].

Some authors have argued that it may be better to label "COVID-19 associated arthritis" rather than "COVID-19 ReA" [66].

COVID-19 can also possibly precipitate arthritis in a susceptible individual.


There is a case report of a lady with psoriasis and inflammatory bowel disease who devel- oped arthritis post-COVID-19 infection [67].

Post-chikungunya or Parvovirus B-19 there can be an onset of arthritis indistinguishable from rheumatoid arthri- tis [68, 69].

A similar phenomenon has been reported post- COVID-19 too [48-50].

However, such anti-citrullinated antibody-positive RA has been reported only in 3 cases to date.


The possibility of a coincidence cannot be excluded looking at the high incidence of COVID-19 infections and the not uncommon incidence of RA, but the point in support of a "reactive" arthritis is that the arthritis is seen after the acute COVID-19 infection.

It is self-limiting.

Had it been a direct viral arthritis, the synovitis should have occurred dur- ing the seroconversion phase.

In acute COVID-19 infection, though arthralgia is common, documented arthritis has been rarely reported.


Viruses have been long implicated in the breakdown of immune tolerance and precipitation of autoimmune dis- ease [70].

SARS-CoV-2 activates CD14 + monocytes and PD-L1 + neutrophils via the Osteopontin-mediated inhibi- tion of Interleukin-10.

This pathway is involved in rheuma- toid arthritis and thus provides a common pathway for the Interferon (IFN)-related pathways have been implicated in COVID-19 [73, 74] and these have a role in the initiation of rheumatoid arthritis.

The TNF (Tumor Necrosis Factor)- induced animal models of rheumatoid arthritis are dependent on IFN and IFN response elements such as the IRF1 (inter- feron regulatory factor 1) transcription factor [75].


Also, various autoantibodies have been reported in COVID-19 [76].

Some of these might have pathological potential and if they persist after the infection, they may lead to rheumatic manifestations like arthritis.

At least 15 different autoantibodies have been described in COVID-19 and 34 human peptides have similarities with SARS-CoV-2 proteins [77].

This may have implications for molecular mimicry in COVID-19.


Classical ReA is self-limiting in two-thirds of cases, but can damage the joints even in such a short period.

Chronic ReA can have much worse sequelae.

In the case of post- COVID-19 ReA, the manifestations appear more transient and self-limiting.

This appears more similar to post-strepto- coccal ReA rather than classical ReA [17].

Also, some cases of post-COVID-19 ReA have different antibodies.

There is a possibility that these may evolve into classifiable rheumatic diseases such as rheumatoid arthritis or lupus [57].


It is not necessary that all arthritis occurring post- COVID-19 should be reactive arthritis.

The alternative is that it may be late-onset viral arthritis with actual invasion of the synovial space with the virus [78].

We could identify one study that reported the detection of SARS-CoV-2 RNA in a patient with wrist arthritis that had appeared 15 days after diarrhoea and upper respiratory tract symptoms [79].

However, other cases have not found such evidence [80].

Moreover, a post-mortem study also failed to find any viral RNA in synovial fluid or bone tissue in five patients who had died of COVID-19 [81].


One limitation of this review is that the search strategy could miss cases of SARS-CoV-2 associated arthritis if the words "reactive" or "post-infectious" were not used.

However, the main focus of the review was to assess how clinicians per- ceive and use the concept of reactive arthritis rather than only assessing SARS-CoV-2 associated arthritis.


The definitions of ReA have been evolving gradually over the last half-century.

Nevertheless, an ideal working defi- nition still eludes us.

Since this entity is not very com- mon in high-income countries, there are possibly limited guidelines for this entity.

The evidence base for treatment is also weak.

The first and foremost requirement to fill in these deficiencies is a strong and universal definition of ReA. The advent of ultrasound in the detection of enthesitis can ena- ble a more objective definition [82].

Also, radiographic features such as new bone formation at the site of enthesitis can be a possi- ble marker [83].

Radiographic changes are late but ultrasound diag- nosis can be early with validated OMERACT (Outcome Measures in Rheumatology Clinical Trials) definitions available [84].


The emergence of post-COVID-19 ReA and possibly post- vaccination ReA is forcing a paradigm shift in how we per- ceive this entity.

Post-vaccination autoimmune diseases are being reported [85].

This leads to the question of whether individuals with genetic predisposition such as HLA-B27 positivity need to be segregated for different vaccines [52].


As the SARS-CoV-2 pandemic is transformed into an endemic due to wide-spread vaccination and emergence of less virulent strains, it will be interesting to study how this affects emergence of COVID-19 associated autoimmune conditions including ReA.


Finally, post-infectious arthritis may hold the key to understanding how the chronicity of arthritis develops.

This may help in future preventive strategies.

The first step has to be a coordinated effort across nations and various rheumatology societies to set up working definitions and enumerate thrust areas of research for ReA.


All co-authors contributed substantially to the concept formulation, searches of relevant articles, and revisions.

They approve the final version of the manuscript and take full responsibility for all aspects of the work.


SA has received honorarium as speaker from Pfiz- er, DrReddy's, Cipla, and Novartis (outside of the current work).

All other authors declare no competing interests.


Dear Editor,


We read with interest the published manuscript by Bekaryssova et al. [ 1] summarizing cases of post-COVID-19 reactive arthritis (ReA).

In their manuscript, the authors started their review by discussing the definition of ReA and its progression over time.

Then, they summarized cases of COVID-19 ReA and those of COVID-19 vaccination-induced arthritis.

They described clinical features, therapeutic management of ReA, and outcomes of these patients.


Twenty-two cases of COVID-19 ReA were summarized [1].

Several studies showed that COVID-19 infection is not only responsible for ReA but also viral arthritis.

Thus, it is necessary to specify whether articular manifestations are due to ReA or viral arthritis.


Viral arthritis is characterized by an early onset and is commonly associated with symptoms of disseminated viral infection.

This diagnosis remains possible in cases of early onset of articular symptoms.

In this review, two cases of early arthritis associated with signs of disseminated viral infection were considered ReA [2, 3].

Indeed, Houshmand et al. described the case of a 10-year-old boy who presented with a concomitant fever, urticaria, and arthritis.

Urticarial lesions tended to appear simultaneously with systemic viral symptoms.

They have been reported in 11 to 19% of patients with COVID-19 infections [4].


These findings support the diagnosis of viral arthritis rather than post-COVID-19 ReA in this patient.

The post-COVID-19 ReA diagnosis can be established based on the occurrence of rheumatological manifestations with a delay between the onset of these manifestations and the confirmed diagnosis of COVID-19 and nasopharyngeal real-time polymerase chain reaction (RT-PCR) negativation at the time of articular signs onset [5].

It is important to emphasize that RT-PCR positivity can persist in patients who have already been in remission [6].


In this review, the authors did not specify the delay between the COVID-19 infection diagnosis and articular manifestations onset [1].


Besides, the authors did not describe the treatments received during the COVID-19 infection [1].

Indeed, articular manifestations can be triggered by several drugs prescribed during COVID-19 infection.

Favipiravir may induce hyperuricemia and even acute gouty arthritis [7].

Likewise, interferon β1 treatment may be responsible for inflammatory rheumatic disease occurrence [8, 9].


There is no agreement on the ReA criteria.

Therefore, we believe that ruling out differential diagnoses such as viral arthritis related to COVID-19, drug-induced arthritis, crystal-induced flares, or a recent onset of another inflammatory rheumatic disease is necessary before making the ReA diagnosis [10].


The authors included seven cases of ReA after COVID-19 vaccination with corona VAC, Sinovac, and SPUTNIK-V.


While some authors consider joint manifestations induced by anti-COVID vaccination a form of ReA, others consider it an autoimmune or inflammatory syndrome induced by adjuvants.

Adjuvants are components added to subunit and inactivated vaccines to stimulate innate and adaptive immune responses.

This stimulation increases the effectiveness of subunit and inactivated vaccines, but it can be responsible for autoimmune/inflammatory syndrome induced by adjuvant (ASIA) [11].

Diagnosis criteria have been suggested for ASIA.

The first major criterion is exposure to external stimuli such as a vaccine, and the second is the appearance of typical clinical manifestations such as arthritis [11].

These manifestations typically occur 2 to 5 days after COVID-19 vaccination [12].

The detection of autoantibodies or anti-adjuvant antibodies is possible and considered a minor diagnosis criterion [12].

It is not clear whether articular manifestations occurring after COVID-19 vaccination correspond to ReA or ASIA [11].


ReA post-COVID-19 infection or post-COVID-19-vaccination is a matter of concern that must support increased research into the pathophysiology of ReA.


We are grateful to Slouma and associates for mirroring our thought processes in the letter [1] in response to our review on reactive arthritis (ReA) before and after COVID-19 [2]. They have reiterated the need to differentiate infective viral arthritis from post-viral reactive arthritis.

The initial concept of ReA was that it was a para-infectious arthritis due to an autoimmune phenomenon without direct invasion of the infectious agents into the synovium.

However, the demonstration of Chlamydial elementary bodies [3] or bacterial DNA [4] in joints of “ReA” has blurred this distinction.

The time period between the infection and the onset of arthritis may be important, but in post-streptococcal reactive arthritis, this gap is very small [5].

Even in the case of COVID-19, this time gap is not known and our review included all cases labelled as the authors by post-COVID ReA to demonstrate how variable the interpretation could be.

Ultimately, the immunopathogenesis of post-COVID ReA must be understood to be able to differentiate it from acute viral arthritis [6].


Slouma and associates are correct that certain drugs may precipitate or unmask rheumatic symptoms.

However, if they check Table 1 in the review, they will see that most patients have received only non-steroidal anti-inflammatory drugs, and oral, parenteral or intra-articular steroids [2].

Also, in most of the case reports, the respective authors have specified how they have excluded other diagnoses before making a diagnosis of post-COVID ReA.


Autoimmune/inflammatory syndrome induced by adjuvant (ASIA) can be considered a differential diagnosis for post-vaccination ReA. Most of the post-vaccination autoimmune phenomena will meet the criteria for ASIA [11].

However, there are some controversies raised about this entity [12] and the mere swapping of names will not leave anyone the wiser.


This letter has helped bring out the message from our review.

The various controversies related to ReA diagnosis are summarized in Table 1.

Whether the concept of post-COVID ReA should be treated as a separate entity needs to be explored.

Large online surveys of treating physicians and multi-national cohort studies of reactive arthritis are required to analyse the concept of viral arthritis and post-COVID-19 joint involvement during the pandemic.

This should be a clarion call to clinicians and rheumatology societies worldwide to get together to update and craft better classification criteria enabling better understanding of this enigmatic entity.


The annual incidence of venous thromboembolism (VTE) in the United States is approximately 1 per 1,000 adults.

Among nonfatal VTEs, approximately 60% are cases of deep vein thrombosis (DVT) and 40% are cases of nonfatal pul- monary embolism (PE) (1).

Arterial thrombosis and venous thrombosis share multiple risk factors, the strongest of which are age, obesity, cigarette smoking, and hypertension (2-4).

However, little is known about the relation between diet and VTE.


A relation between diet and VTE was suggested as early as World War II (5).

However, to our knowledge, there have only been 2 prospective epidemiologic studies-the Athero- sclerosis Risk in Communities (ARIC) Study and the Iowa Women's Health Study (IWHS)-in which investigators have systematically examined the role of dietary patterns in the development of VTE (6, 7), and the results of those studies conflicted.

There have been 8 studies in which investigators have explored the relation between alcohol and VTE; in 4 of those studies, an inverse association was reported (7-10), whereas no relation was found in the other 4 (11-14).

The relation between specific nutrients and coagulation factor levels has been evaluated more broadly (6, 7, 15-17).

Vitamins B 6 and B 12 have been shown to reduce elevated homocysteine 114 Am J Epidemiol.

2012;175(2):114-126 levels, which are associated with an increased VTE risk; omega-3 fatty acids decrease platelet aggregation and factor VII and fibrinogen levels (18); and vitamin E might inhibit the biologic activity of vitamin K and vitamin K-dependent clotting factors (19).

However, little is known about the potential role of these nutrients in the development of VTE.


The aim of the present study was to better define the association between dietary intake and the risk of VTE by analyzing cohort data from approximately 130,000 US women and men.


The Nurses' Health Study (NHS) began in 1976, when 121,701 female nurses who were 30-55 years old and living in 11 US states (California, Connecticut, Florida, Maryland, Massachusetts, Michigan, New Jersey, New York, Ohio, Pennsylvania, and Texas) responded to a mailed health questionnaire (20).

The Health Professionals Follow-up Study (HPFS) began in 1986, when 51,529 male US health professionals who were 40-75 years old responded to a de- tailed mailed questionnaire that included a diet survey and questions about lifestyle practices and medical history.

In both cohorts, follow-up questionnaires were sent every 2 years thereafter to acquire updated information on lifestyle factors and to query participants about newly diagnosed medical conditions.

Women in the NHS also completed a 126-item food frequency questionnaire (FFQ) in 1984, and men in the HPFS completed a 131-item FFQ at baseline (i.e., in 1986).

Similar FFQs were sent every 2-4 years thereafter.

The Partners Institutional Review Board (Partners HealthCare, Boston, Massachusetts) ap- proved the NHS and the HPFS protocols.

The studies are being conducted according to the ethical guidelines of Part- ners HealthCare.


We excluded participants who did not complete an FFQ at baseline from the analysis.

Likewise, we excluded partici- pants with extremely high energy intakes (>3,500 kcal/day for women and >4,200 kcal/day for men) or extremely low energy intakes (<500 kcal/day for women and <800 kcal/day for men), as well as those who left more than 70 questions blank.

Subjects who reported a history of VTE at baseline also were excluded from the present analysis.

The final baseline population (in 1984 for women from the NHS and in 1986 for men from the HPFS) included 80,192 women and 49,238 men.

In the NHS, the active follow-up rate (the number of person-years in the cohort when participants are censored after their last questionnaire response) from 1984 to 2008 was 92.2%, and in the HPFS, the follow-up rate from 1986 to 2008 was 88.0%.


Dietary intake information was collected using an FFQ designed to assess average food intake over the previous 12 months.

Standard portion sizes were listed with each food.

For each food item, participants indicated their average fre- quency of consumption over the past year in terms of the specified serving size by checking 1 of 9 frequency categories that ranged from ''almost never'' to ''6 times/day.''


To prepare for factor analysis, food items were grouped into 38 predefined food groups as previously described (21).

Using principal component analysis, dietary patterns were identified from FFQs administrated in 1984, 1986, 1990, 1994, 1998, and 2002 in the NHS and 1986, 1990, 1994, 1998, and 2002 in the HPFS.

We rotated the factors using an orthogonal transformation to achieve structure with greater interpretability and determined the number of factors to be retained using the diagram of eigenvalues.

Foods with a cor- relation of at least 0.30 were considered to be making a con- tribution to the factor.


On the basis of prior published reports and biologic plausi- bility, we selected some specific food groups (fruits, vegetables, fish, red and processed meats, and alcohol) and nutrients (omega-3 fatty acids, trans fatty acids, total fiber, vitamin K 1 , vitamin B 6 , vitamin B 12 , and vitamin E) to assess their association with the risk of VTE.

We assessed both dietary and total (diet plus supplements) intakes.

Nutrient intakes were computed by multiplying the frequency response by the nutrient content of the specified portion sizes.

Food com- position values were obtained from the Harvard University Food Composition Database (Boston, Massachusetts), which was derived from US Department of Agriculture sources and supplemented with information from manufacturers.

All di- etary factors were adjusted for total energy using the residual method (22).


To reduce measurement error and represent long-term dietary intake, the cumulative averages of pattern scores, foods, and nutrients were calculated and then divided into quintiles.

We also examined the consistency of the association between dietary patterns and VTE by using the most recent dietary intakes as predictors of VTE risk.


Participants who reported a physician-diagnosed PE on a biennial questionnaire but did not have a prior history of malignancy received a follow-up letter requesting medical records from the facility in which they were diagnosed with a PE.

A detailed review of these records was undertaken, and cases were coded.

Incident cases for which the medical record included imaging that was diagnostic of a PE were considered confirmed.

Imaging was considered diagnostic if the radiologist reading the study noted a ventilation/perfusion lung scan that indicated a high probability of a PE, a filling defect on a contrast-enhanced computed tomographic scan of the pulmonary vasculature, or a filling defect on a catheter- based pulmonary angiograph.


Over the follow-up period, we identified 956 women and 353 men with an incident PE.

Participants also reported physician-diagnosed DVT on the biennial questionnaire.

Men were considered to have incident DVT if they reported a physician-diagnosed DVT between 2 consecutive questionnaires, and women were if they reported ''phlebitis and thrombophlebitis'' as another major illness (code 451 according to the International Classification of Diseases, Eighth Revision).

A total of 584 women and 999 men were classified as having DVT under these definitions.


Overall, 1,540 women and 1,352 men reported VTE.


When possible, data on covariates were obtained from the baseline questionnaire (1984 in NHS and 1986 in HPFS) and updated every 2 years.

Variables included age, physical activity level, physical inactivity level, body mass index (BMI, mea- sured as weight (kg)/height (m) 2 ), total caloric intake, smoking status, pack-years of smoking, race/ethnicity, spouse's high- est educational attainment (only in the NHS), parity (only in the NHS), menopausal status (only in the NHS), nonaspirin nonsteroidal antiinflammatory drug use, warfarin use, mul- tivitamin use, hypertension, coronary heart disease, and rheumatologic disease.


Physical activity, including a variety of activities such as walking, bicycling, swimming, or playing tennis, was mea- sured in metabolic equivalents per week and categorized in quintiles.

Physical inactivity was defined as the number of hours spent sitting at home per day and was categorized in 6 categories (from the lowest amount of time to the highest).

BMI was updated biennially and categorized in 4 categories: less than 25.0, 25.0-29.9, 30.0-34.9, and 35 or higher.

Total caloric intake was estimated through the FFQ, expressed in


Our strategy for analysis was to study the association between dietary intake and the risk of VTE (DVT and PE) in both men and women.

Each dietary variable was analyzed using the Cox proportional hazards model.

A test for trend across the quintiles of each dietary variable was calculated by treating the categories as ordinal variables in a propor- tional hazards model.

After calculating sex-specific relative risks, we combined the ln relative risks weighted by the inverse of their variances using a random-effects model (23).

We tested for between-study heterogeneity using the Q To assess whether age-related physiologic differences might modify the association between diet and VTE (9), we further stratified our analysis according to the median age at baseline (50 years in women and 53 years in men).

We also stratified analyses according to obesity (BMI 30) and level of physical activity (median).

In addition, we performed sensitivity analyses by excluding participants with prior co- morbid conditions (cancer or cardiovascular diseases).

All analyses were conducted using SAS, version 9.1 (SAS Institute, Inc., Cary, North Carolina).


Through the use of principal component analysis, we iden- tified 2 distinct major dietary patterns among both women and men.

The first pattern was defined by high intakes of fruit, vegetables, fish, poultry, whole-grain products, and low- fat dairy products.

The second pattern was defined by high intakes of refined grains, cured and red meats, desserts, sweets, French fries, and high-fat dairy products.

In accordance with what was done in previous studies of dietary patterns in this population, we labeled the first pattern the ''prudent pat- tern'' and the second pattern the ''Western pattern.'' Tables 1 and 2 show baseline characteristics of the participants, which were adjusted for age and stratified according to each dietary pattern among women and men.

Compared with participants with the lowest intake of foods from the prudent diet (the lowest quintile), participants with the highest intake of foods from the prudent diet (the highest quintile) were older, more physically active, less likely to be current smokers, and more frequent users of multivitamin supplements.

Compared with participants with the lowest intake of foods from the Western diet, participants with the highest intake of foods from the Western diet had a higher BMI, were less physically active, were more likely to smoke, and took fewer multivitamin supplements.

When the population was restricted to participants without prior cancer or cardiovascular disease (n ¼ 112,658 women and men), the results did not differ materially (for the highest quintile of Western diet vs. the lowest, multivari- able pooled RR ¼ 1.24, 95% CI: 0.91, 1.80; P for trend < 0.001; P for between-study heterogeneity ¼ 0.06).


We performed several subanalyses of the association between dietary patterns and VTE.

First, we stratified our analyses according to the median age at baseline (Figures 1 and 2).

Among both the youngest participants (women aged 38-49 years at baseline and men aged 40-52 years at base- line) and the oldest participants (women aged 50-63 years at baseline and men aged 53-75 years at baseline), no Regarding food groups (Table 4) and nutrients (Table 5), there was a consistent inverse association between vitamin E intake and the risk of VTE in women (P for trend ¼ 0.02), in men (P for trend ¼ 0.07), and in the pooled analysis (P for trend ¼ 0.004).

For fiber and vitamin B 6 intakes, there was a significant inverse association with the risk of VTE in the pooled analysis, with no significant heterogeneity between men and women, although the associations were significant only in men (Table 5).

For intakes of red and processed meat and of trans fatty acids, no association with VTE was found in women, whereas a significant positive association was found in men (the percentages of total variance between studies were 88% and 84% for red and processed meat and trans fatty acids, respectively).

The association in the pooled analysis was not significant for trans fatty acid intake (for the Dietary Patterns, Foods, Nutrients, and VTE 121 Am J Epidemiol.

2012;175(2):114-126 highest quintile of trans fatty acid intake vs. the lowest, mul- tivariable RR ¼ 1.14, 95% CI: 0.84, 1.53; P for trend ¼ 0.33; P for between-study heterogeneity ¼ 0.01) and was border- line significant for red and processed meat intake (for the highest quintile of red and processed meat intake vs. the lowest, multivariable RR ¼ 1.38, 95% CI: 0.92, 2.06; P for trend ¼ 0.07; P for between-study heterogeneity ¼ 0.004).

Analyses in which we used the most recent dietary intakes or nutrient intakes derived from foods only (not supplements) had similar results (data not shown).

No associations were found between the risk of VTE and the intakes of fruit, vegetables, fish, alcohol, omega-3 fatty acids, vitamin K 1 , and vitamin B 12 (Tables 4 and 5).


In a pooled analysis of men and women, we found a weak association between diet and risk of VTE.

No relation was found between the prudent diet pattern and the risk of VTE; however, we did find a weak positive association between the Western diet pattern and the risk of VTE.

Stratification according to age, BMI, and physical activity level led to similar results.

Regarding specific foods or nutrients, no associations were found between the risk of VTE and the intakes of fruits, vegetables, fish, alcohol, omega-3 fatty acids, vitamin K 1 , and vitamin B 12 .

Vitamin E had a protective association, as did fiber and vitamin B 6 , particularly in men.

Similarly, we found that increased intakes of red and pro- cessed meat and trans fatty acids might be associated with VTE in men.

These sex differences should be considered with caution, as issues of sample size and multiple testing could have influenced the results.


Our use of data from 2 large prospective cohorts of health professionals who were 38-73 years of age at baseline and followed for more than 20 years enabled us to establish a temporally correct relation between dietary intake and VTE and to control for many potential confounders in our analyses.


Data relating food groups/nutrients to VTE are scant, and in the few published epidemiologic studies of this relation, investigators reported conflicting results (6, 7, 11).

Our find- ings regarding vitamin B 6 and red and processed meat intakes are consistent with those from the ARIC Study (6); of the 6 food groups and 5 nutrients investigated, only intakes of vitamin B 6 and fruits and vegetables were significantly as- sociated with a decreased risk of VTE, and only red and processed meat intake was associated with an increased risk of VTE (6).

A borderline-significant negative association was reported for folate intake (6).

However, in 2 large randomized trials, supplementation with vitamins B 6 and B 12 and folic acid did not reduce VTE incidence (16) or recurrence (15).

In the IWHS, of the 11 food groups and 6 nutrients investi- gated, only alcohol intake was associated with a reduced risk of VTE (7).

Recently, in a case-control study of 292 Asian men and women, 6 food groups were investigated, and only a high vegetable intake was negatively associated with VTE (11).

Our finding regarding vitamin E is consistent with a previous long-term trial in the Women's Health Study, in which intake of 600 IU of natural-source vitamin E on al- ternate days was associated with a significant 21% reduction in the hazard of VTE (17).


There are several possible explanations for the different findings in the ARIC Study, the IWHS, and our study.

To explain the contrary findings between the ARIC Study and the IWHS, Lutsey et al. ( 7) hypothesized that diet may play a bigger etiologic role in the development of VTE in younger people than in older people.

In the present study, we found similar results in strata of younger and older participants, although this limited the power of our study.

Another pos- sible explanation is race/ethnicity; approximately 25% of participants in the ARIC Study were black, whereas most ).

Tang et al. ( 26) recently reported that, compared with whites, blacks experienced 3 times more frequent fatal out-of-hospital PE in the New York City area and died at an age that was 10 years younger in the case of fatal PE, but they did not carry factor V Leiden and the prothrombin G20210A mutation (27).

However, the impact of these black/white differences on the diet-PE association is not clear.


Another possible explanation for the discrepant findings is that the primary outcome differed across studies.

In the ARIC Study, the main outcome was non-cancer-related VTE In conclusion, we found a weak association between diet and the risk of VTE in US women and men.

Nutritional factors of possible etiologic relevance include the Western dietary pattern and intakes of vitamins E and B 6 , fiber, red and processed meat, and trans fatty acids.

Other nutritional fac- tors were not associated with VTE in our 2 large cohorts.

The unique characteristics of our cohorts might limit generaliz- ability of the results to individuals of nonwhite race/ethnicity or lower socioeconomic status or persons with limited access to medical care.

Further studies are warranted in these vulnerable populations.


Recently, there has been interest in determining whether diet is associated with the risk of venous thromboembolism.

The article by Varraso et al. ( Am J Epidemiol.

2012;175(2):114–126) published in this issue of the Journal is an important contribution to this literature.

In this commentary, the author discusses the findings of Varraso et al. within the context of the existing literature and posits epidemiologic explanations for why investigators might have failed to identify strong associations between diet and venous thromboembolism.


In this issue of the Journal, Varraso et al. [ 1] report the results of a comprehensive assessment of the associations between diet and incident venous thromboembolism (VTE) in a sample of 129,430 male and female health professionals.

Dietary intake was represented by dietary patterns (prudent diet vs. Western diet) and intakes of various food groups and nutrients.

Despite the large number of VTEs reported (n = 2,892) and the use of analytic methods that attempted to reduce dietary measurement error by taking advantage of multiple dietary assessments, overall there was little suggestion of a relation between diet and VTE.

Of the 14 dietary patterns, food groups, and nutrients evaluated, only vitamin E, vitamin B6, and fiber were associated with a lower risk of VTE in the gender-pooled analysis.

Higher Western dietary pattern scores and greater consumption of red and processed meats and trans fatty acids were associated with a greater risk of VTE in men but not in women.

In the present commentary, prior studies that explored the relation between diet and VTE are summarized, and potential reasons why strong associations between diet and VTE have not been consistently observed are outlined.


Etiologic data from Norway gathered during World War II (1940–1944) provided the first suggestion of a relation between diet and VTE [2, 3].

In recent years, possible relations have been examined in several epidemiologic studies [1, 4–19].

As shown in Table 1, some studies, but not all, showed that VTE risk was inversely associated with intakes of fruits and vegetables, alcohol, vitamin E, vitamin B6, and fiber but positively associated with adherence to a Western dietary pattern and intakes of red and processed meat and trans fatty acids.

Overall, the results of Varraso et al. [ 1] are consistent with those of previous investigators, who have generally failed to report strong associations between diet and VTE.

Given the lack of consistent and strong associations between diet and VTE, it is important to evaluate 1) the mechanisms underlying the hypothesized associations and 2) the methodological factors that might be impairing our ability to detect relations between diet and VTE if they are present.


Physiologically, diet might affect VTE risk by altering levels of hemostatic and fibrinolytic factors and/or by influencing an individual’s propensity for obesity.

Epidemiologic associations between VTE and specific dietary components are inconsistent, but many of the food groups and nutrients with the strongest evidence for an association with VTE—including vitamin E, the B vitamins, fruits and vegetables, red and processed meat, and alcohol—act on the hemostatic system.

For example, red and processed meats are high in saturated fatty acids, which have been shown to increase platelet aggregation [20].

Moderate alcohol consumption might have antithrombotic effects [21–23], although it is unclear whether these effects are due to ethanol or other compounds [24] such as resveratrol, which is present in red wine [25], or hops, which are found in beer [26].

However, effects of diet on hemostatic pathways have not always translated into risk of VTE in controlled trials.

B vitamin supplementation did not reduce the risk of incident VTE [5] or recurrent VTE [6], despite the apparent inverse relation with homocysteine levels [27].

However, supplementation with vitamin E, which has been shown to have anticoagulant effects in humans [28, 29] and animals [30, 31], was associated with a 21% lower risk of incident VTE in the Women’s Health Study clinical trial [4].

Although numerous statistically significant associations have been observed between dietary intake and hemostatic factor levels, it must be acknowledged that the magnitudes of these associations were generally very modest.

Furthermore, associations between hemostatic factors and VTE incidence are also often of modest magnitude.

Given this compilation of modest physiologic associations, it is unlikely that acting through hemostatic factors, diet would have a strong impact on the absolute risk of VTE.


Diet may also influence VTE risk through its relation to obesity, which is a well-established strong risk factor for VTE [32].

Obesity is associated with venous stasis and also with venous damage and varicosity [11].

Further, obesity may promote thrombosis through increased activity of the coagulation cascade and decreased activity of the fibrinolytic cascade [33].

Particularly when thinking about the positive associations among Western dietary patterns, red and processed meat, and VTE, it is important to be cognizant of the possibility of residual confounding by total caloric intake and obesity.

Caloric intake is poorly estimated by food frequency questionnaires, and estimates are known to be differential by overweight status [34].


In addition to the potential issue of small effects between diet and hemostatic factor levels, dietary measurement error may make it difficult to detect associations between diet and VTE.

In many of the publications presented in Table 1, diet was assessed only once, and follow-up was often long.

Given the imprecision of dietary assessment and the possibility of an individual’s diet changing over time, dietary measurement error might have muddied the results.

To reduce dietary measurement error, Varraso et al. [ 1] utilized data from a biennial food frequency questionnaire in a cumulative average diet analytic approach.

Further, to address the issue of change in dietary intake over time, they conducted sensitivity analyses in which they used the most recent dietary intake as the predictor of VTE risk.

Given their careful analytic approach, dietary measurement should be less of a concern in the article by Varraso et al. [ 1] than in others in which the relation between diet and VTE was explored.


Another issue to keep in mind when reviewing this (and any) literature is the possibility of publication bias.

Given that many of the published studies have yielded null results, one has to question whether publication bias may also be present.

It is possible that some authors have chosen not to publish papers with null results.


In summary, the evidence suggesting a relation between dietary intake and the risk of VTE is relatively weak overall.

The article by Varraso et al. [ 1] is an important contribution to this body of literature, given the large number of cases and the analytic approach, which was intended to reduce dietary measurement error.

Questions still remain regarding whether diet has an important impact on VTE risk.

However, given the small magnitude of the associations between diet and hemostatic factor levels, combined with the relatively weak epidemiologic findings between diet and VTE, current data do not support a major role for diet in the development of VTE.


Although exploring the relations between diet and VTE is etiologically interesting, it is also important to ask: What are the potential public health and clinical implications of this work? Given that VTE is a relatively rare condition with an incidence rate of approximately 1 per 1,000 person-years [35–37], it is unlikely that public health messages will promote adherence to a healthy diet for VTE prevention, especially as the foods hypothesized to be beneficial are also advantageous for more common conditions, such as coronary heart disease and cancer.

Recurrence of VTE is common, however, with approximately 8% of individuals experiencing a recurrent event within 1 year of their initial diagnosis [35] and one-third experiencing a recurrent event in the decade after their incident event [37–39].

Therefore, identifying dietary factors that are effective at preventing VTE recurrence may have clinical value.


We appreciate the thoughtful comments by Dr. Lutsey [1] about our analysis [2] of data from the Nurses’ Health Study and the Health Professional Follow-up Study.

We agree with her conclusion that the association between diet and the risk of venous thromboembolism (VTE) is likely weak.

In the invited commentary [1], Dr. Lutsey discussed the potential for dietary measurement error.

We agree that measurement of dietary intakes is difficult, especially because they change over time.

However, in addition to considering errors in the measurement of the dietary exposures, one might also examine the heterogeneity of the outcome (in this case, VTE).

In most of the studies cited in Table 1 of the invited commentary [1], the authors investigated all VTEs (i.e., all cases of pulmonary embolism (PE) or deep vein thrombosis) without differentiating between idiopathic and provoked VTE.

If one studies all types of VTE, he or she also studies the risk factors for VTE (e.g., cancer).

Thus, if one wants to study novel risk factors for VTE, one might preferentially study cases of idiopathic VTE (i.e., cases that were unrelated to classic risk factors for malignancy, recent surgery, and trauma).

Although our data did not permit us to distinguish between idiopathic and provoked VTE, we could specifically analyze idiopathic PEs.


Over the follow-up period, we identified 308 women and 109 men who had an incident idiopathic PE.

After adjusting for 17 potential confounders (age, total physical activity level, physical inactivity level, body mass index (weight (kg)/height (m)2), total caloric intake, smoking, pack-years of smoking, race/ethnicity, spouse’s educational attainment (in women only), parity (in women only), menopausal status (in women only), nonaspirin nonsteroidal antiinflammatory drug use, warfarin use, multivitamin supplement use, hypertension, coronary heart disease, and rheumatologic disease), we found no association among dietary patterns, foods, or nutrients and the risk of idiopathic PE in either women or men.

The pooled relative risk of PE for persons in the highest quintile of prudent diet intake compared with persons in the lowest was 0.85 (95% confidence interval (CI): 0.42, 1.72; P for trend = 0.78); for Western diet intake, the corresponding relative risk was 1.14 (95% CI: 0.53, 2.45; P for trend = 0.94).

These results provide further evidence that there is little (if any) association between diet and VTE.


In our study [2], we investigated several foods and nutrients in relation to VTE, but we did not study coffee intake.

A recent study in which it was reported that moderate coffee consumption might be associated with a reduced risk of VTE [3] led us to conduct further analyses regarding the potential role of coffee intake in the development of VTE.

However, we found no association between coffee intake and the risk of VTE (for the highest quintile of coffee intake compared with the lowest, relative risk (RR) = 1.02, 95% CI: 0.87, 1.22) or idiopathic PE (RR = 0.94, 95% CI: 0.44, 1.18).

As mentioned by Dr. Lutsey, diet may also influence VTE risk through its relation to obesity, which is a strong risk factor for VTE.

We previously showed that increasing body mass index had a strong linear association with the risk of idiopathic PE in the Nurses’ Health Study [4].

This association remained statistically significant after further adjustment for dietary patterns (for each 1-unit increase in body mass index, RR = 1.09, 95% CI: 1.07, 1.10; P < 0.001).

In addition to obesity, physical activity or inactivity might also modulate the association of diet, obesity, and VTE.

Recently, we reported that in the Nurses’ Health Study, the risk of idiopathic PE was more than 2-fold higher in women who spent the most time sitting than in women who spent the least time sitting, independent of obesity, diet, and other factors [5].

The interrelations between nutritional factors and lifestyle factors (diet, obesity, physical activity, and physical inactivity) provide important challenges for epidemiologic researchers.

Accordingly, there is a need for further research to disentangle the independent effect of each nutritional factor on VTE risk by using, for example, causal models [6].

This analytic approach allows for testing of different models of causality in the epidemiology of disease arising out of environmental factors and analysis of the interplay between these factors.

Such an approach might help us find a stronger scientific basis to support nutritional recommendations that lower the risk of VTE.


Atmospheric ionization events break N 2 chemical bonds, enabling nitrogen oxides [NO(y)] formation, normally at low atmospheric abundance [e.g. Thomas et al., 2005].

There has been controversy whether NO(y) deposition in ice cores, primarily as nitrate (NO 3 ), can be used as a proxy for very large solar proton events (SPEs).

Based on the impulsive nitrate events identified in polar ice by Dreschhoff and Zeller [1990, 1994, 1998] McCracken et al. [ 2001a] established a calibration between impulsive nitrate deposition in the 415-year GISP2-H ice core obtained from the top of the ice sheet divide at Summit, Greenland, in 1991 by Dreschhoff and Zeller [1994, 1998] and extremely large SPEs between 1956 and 1989.


These authors identified 70 impulsive nitrate events in the GISP2-H core and concluded that they could be used as proxies to identify past extremely large SPEs.

One of the largest impulsive nitrate events was dated as late 1859 and associated with the well-documented but poorly quantified September 1859 Carrington event [Clauer and Siscoe, 2006].


Wolff et al. [ 2012] analyzed several central Greenland ice cores, including their D4 [McConnell et al., 2007] and Zoe [Wolff et al., 2012] cores for a 40-year time period (1840-1880) and suggested that the impulsive nitrate event identified by McCracken et al. [ 2001a] as the 1859 Carrington event most likely resulted from biomass burning in 1863.


It is the hard spectra solar cosmic ray ground-level events that have sufficient >300 MeV fluence to penetrate to and through the ozone layer (30 to 17 km altitude).

The large fluence of these particles produces the ionization that provides the energy to ionize N 2 in the lower stratosphere or even the troposphere [Atri et al., 2010; Usoskin et al., 2011].

When NO(y) is generated at these lower altitudes, there is the possibility of moving quickly into the troposphere, either by downward advection or by incorporation into polar stratospheric clouds and gravitational settling, where it will be deposited as NO(y) in snow events.

The softer spectra events will deposit the ionization energy at higher altitudes, and the resulting NO(y) must be transported downward by mechanisms such as the upper branch of the Brewer-Dobson circulation.

These well-established transport mechanisms acting over longer time periods should significantly broaden the deposition timescale as the material diffuses down into the troposphere making any nitrate signal in the ice much harder to identify.


The problem with using the Carrington event to dispute all SPE effects in polar ice nitrate profiles as done by Wolff et al. [ 2012] is that while this was clearly a major solar event (white light central meridian solar flare) with subsequent associated extreme geomagnetic storm and low-latitude aurora, it is only a single example and little quantitative information exists with respect to a SPE.

Hence, it may not represent the type of high-energy SPE needed to produce an impulsive nitrate event and is not the ideal test case.

A careful inspection of Figure 1 in McCracken et al. [ 2001a] shows a complex structure of several events occurring in the 1859 dated GISP2-H core, which is not seen in the 1863 Zoe and D4 data.

It is simply not possible at this time to state conclusively whether the large nitrate spike dated to 1859 or 1860 in the GISP2-H core and to or 1863 in other Greenland cores resulted from the Carrington event or if a smaller, or no, impulsive nitrate enhancement should be expected.


In an effort to understand the different interpretations between McCracken et al. [ 2001a] and Wolff et al. [ 2012], we concluded that a correlation test between impulsive nitrate spikes in polar ice and SPEs could be conducted by examining ice core nitrate deposition during the only years when both well-documented extremely large hard spectrum relativistic solar cosmic ray events occurred and ultrafine-resolution nitrate measurements in consolidated firn exist, namely the 14- year interval 1937 to 1951.

We use this time period to ascertain if the ice core data available for analysis contain evidence of short-duration impulsive nitrate enhancements that could be time associated with these large relativistic solar cosmic ray events.

Using spectral analysis we also determine the resolutions of sampling schemes using these nitrate enhancements.

In this study we will show that finer than 0.08 year (sub-monthly) resolution is necessary for impulsive nitrate event detection in ice cores and conclude that the data used by Wolff et al. [ 2012] were inadequate to differentiate short-duration nitrate enhancements that might be indicative of an extremely large solar proton event.


We note that Schrijver et al. [ 2012] also discuss reasons to question the validity of nitrate spikes.

We comment briefly on those here.

( 1) The conventional nitrate transport processes from the middle stratosphere and above is very slow, so it is hard to make spikes in the ice.

The problem with this is an assumption that substantial deposition cannot occur at lower altitudes.

This can be shown to be incorrect by examining tables in Atri et al. [ 2010] or balloon data in Nicoll and Harrison [2014].


(2) Nitrate interference from biomass burning is a serious concern but can be filtered out by examining other species (e.g., black carbon, ammonium and vanillic acid), at comparable resolution.

Similarly, post-depositional variations could be detectable by examining the concentration of other species.

Ionization events should only involve impulsive nitrate increases although conductivity may increase also as nitrate is highly ionic in water and is the second largest contributor to Greenland ice conductivity after sulfate.


There appears to be disagreement as to what constitutes an "impulsive nitrate event" in the ice core data.

In fact, for years, these features either were not observed due to insufficient time resolution or were attributed to contamination [e.g., Herron, 1982; Delmas et al., 1982; Dreschhoff et al., 1983; Legrand and Delmas, 1986].

The amount of nitrate found in polar ice and snow from generally accepted background sources (biogenic decay, biomass burning, lightning, anthropogenic emissions, and stratosphere-troposphere exchange) [e.g., Ehhalt and Drummond, 1982; Chameides et al., 1977; Neftel et al., 1985; Hameed et al., 1981; Hastings et al., 2004] and from proposed extreme SPEs is dependent on many factors that tend to vary in an annual cycle (e.g., source strength, atmospheric processes, and transport mechanisms to the ice).


The impulsive nitrate enhancement definition used by McCracken et al. [ 2001a,b] was an extremely short duration nitrate impulse that was at least three standard deviations above and superimposed on the temporal, highly variable nitrate background.

The smoothed temporal profile was subtracted from the short-duration impulse event amplitude to obtain the additional accumulated NO(y) contained in the impulsive nitrate event.


An illustrative example is the impulsive nitrate event contained in samples 1133-1136 of the GISP2-H data shown in Figure 1 that is time associated with the 23 February 1956 solar cosmic ray ground-level event [Meyer et al., 1956; Pfotzer, 1958; Shea and Smart, 2012].

This is the largest relativistic solar cosmic ray event observed in the history of cosmic ray measurements with relativistic solar particles impacting the Earth's polar regions for more than 24 hours (Švestka and Simon, 1975).

The duration of this impulsive nitrate deposition event in the ice was about 2 cm water equivalent at Summit, or 1 month.


The data used in this analysis are from four ice cores identified by the following names: Zoe, D4, GISP2-H, and BU.

The Zoe, GISP2-H and BU cores were obtained at Summit (72.6°N, 38.3°W, 3216 m elevation, 24.6 cm average annual water equivalent accumulation [Meese et al., 1994; Albert and Schultz, 2002]), and the D4 core was drilled 237 km away in central Greenland (71.4°N, 44.0°W, 2713 m elevation, 41.4 cm average annual water equivalent accumulation [Banta and McConnell, 2007]).

E. W. Wolff and J. R. McConnell (personal communication, 2012) have generously provided their Zoe and D4 ice core data.

GISP2-H [Dreschhoff and Zeller, 1994; 1998] and BU [Kepko et al., 2009] data were provided by G. A. M. Dreschhoff (personal communication, 2000) and L. Kepko (personal communication, 2009) respectively.


Figure 2 presents the 14 year time series of nitrate concentrations from 1937 to 1951 for all four cores.

The nitrate profiles look very similar when plotted in terms of water equivalent depth and are not shown here.


The Zoe and D4 curves obtained from continuous flow analysis (CFA) of multiple species actually show coarser effective resolution compared to GISP2-H and BU, despite the finer resolutions listed in Table 1 of Wolff et al. [ 2012].


Discretely sampled and co-located nitrate and conductivity values were identified each 1.5 cm of firn or ice along the entire GISP2-H core yielding approximately 20 discrete samples per year (~1.25 cm water equivalent per sample).

For the BU core, Kepko et al. [ 2009] developed a simplified CFA procedure that concentrated on obtaining only co-located nitrate and conductivity measurements through a single flow line, resulting in an approximately 0.063 cm water equivalent sampling interval, thus reducing dispersion effects and achieving a sampling frequency in excess of 284 (cycles) year -1 (per year) for 1937 to 1951.


To ensure the accuracy and repeatability of the data acquired, Kepko et al. also divided the initial core into four parallel sections and analyzed each section independently before averaging.

This resulted in an ultrafine- resolution nitrate and conductivity data set that could be dated using the Hekla eruption volcanic tie point, annual layer counting, and the consensus Summit depth/time profile [Meese et al., 1994].


In contrast, the multi-species CFA conducted on the Zoe and D4 cores used sampling intervals ranging from 0.4 to 0.9 cm water equivalent.

While this CFA design enabled many geochemical species in the ice cores to be characterized in parallel, this approach, coupled with dispersion effects, inherently sacrificed effective depth resolution [Breton et al., 2012] and reduced the time resolution of the Zoe and D4 data compared to those of GISP2-H and BU as shown in Figure 2.


Nearly any mathematical function can be represented as the sum of a series of sinusoids; examining the nature of these has become a standard method in many fields, in this case time and depth series.

For an introduction, see Muller and MacDonald [2002] and Melott and Bambach [2011].

The power spectrum is a way of showing the strength of fluctuations at various frequencies.

In order to represent a sudden change over time T, frequencies up to 1/(2T), the Nyquist frequency, must be included.

When considering a depth interval D, an analogous Nyquist frequency 1/(2D) is obtained.

Smoothing data, which involves averaging over neighboring points, may happen by mixing the data at different times or depths.

It is equivalent to removing high frequencies from the data, which can be seen in the power spectrum.


The Lomb-Scargle Method [Scargle, 1982] was developed to analyze irregularly spaced data directly without interpolation.

It is equivalent to doing a least-squares fit to sine waves of various wavelengths [Cornette, 2007].


In Figure 3 we show the results of a Lomb-Scargle analysis of the four nitrate data sets in terms of time.

A spectral analysis of all four data sets was also obtained in terms of water equivalent depth.

The depth power spectra gave similar results and are not shown, but the resulting depth resolutions are reported here.

Significance levels are assigned assuming a "red noise" AR(1) background.

All the data in Figure 3 show a peak near 1, corresponding to the annual nitrate cycle in polar ice that is well preserved at Summit.


The discretely sampled GISP2-H data show significant power right up to the largest sampled frequency.

In contrast, the CFA-sampled Zoe, D4, and BU data show a distinct drop of significance at the higher frequencies, far below the putative Nyquist frequency.

We recognize that there may be some mild nonlinearities in the correspondence between time and depth scales, but these will average out over the 14-year interval with the result that there is some mixing of power for adjacent frequencies.

In any case, shorter depth intervals will correspond on average to shorter times and higher frequencies.


The narrowness of the peak at 1 year -1 sets a limit of a few percent in the variation in annual snowfall rate.


The Zoe and D4 nitrate data show that even at the 50% confidence level, there is no significant power at frequencies greater than about 3 year -1 .

The depth analysis of the observed nitrate pattern in the Summit Zoe data corresponds to a depth resolution that is closer to 8 cm water equivalent rather than 1 cm water equivalent, suggesting that these are at best seasonal features (i.e., the annual nitrate cycles) that are being resolved.

The actual depth resolution in the D4 ice core nitrate data from 1937 to 1951 with power exceeding the 95% confidence interval is no better than 9.4 cm water equivalent at Summit.

In contrast, the GISP2-H nitrate data show significant power at the 99.9% confidence level up to about 12 year -1 (1 month period) and have a 1.9 cm water equivalent depth resolution, and the more finely depth sampled BU core nitrate data show significant power at the 99.9% confidence level up to about 36 year -1 (~10 days period or ~0.67 cm water equivalent depth resolution).

This suggests strongly but does not prove that there is a meaningful signal in the Summit ice at about a 10-day resolution that has not been consistently compromised by post-depositional processes.

This resolution limit is most probably determined by the high frequency of episodic snowfall events ~88 year -1 (~7.3 per month or roughly one snowfall event every 4 days, corresponding to ~0.28 cm water equivalent per event [Dibb and Fahnestock, 2004]) in combination with winds and subsequent migration of nitrate in the firn and applies to other species as well.

The question we are left with then is, "What is the effective sub-annual resolution of nitrates in ice cores at Summit; i.e., how fine a resolution in the ice cores at Summit will yield useful information from multi-parameter (as well as possibly SPE/nitrate deposition) studies?"


It is not sufficient to show the presence of high frequencies, as in the GISP2-H and BU core power spectra (Figure 3).

Noise in the data could introduce high-frequency power.

In order to demonstrate that they show fine-resolution sampling, power must be correlated in such a way as to generate high peaks on a corresponding fine depth or time scale.


In Figure 4 we show the five highest nitrate peaks for the interval 1937-1951 in each of these data sets.

The full width at half- maximum (FWHM) was calculated by plotting each peak out to its first local minimum on either side.

Peak heights and half maximum widths were plotted and calculated relative to the average nitrate concentration of each pair of local minima as the zero point.

An average FWHM (FWHM av ) was then calculated from all five peaks for each core.


The FWHM av of each core corresponds closely to the resolution limits given by the power spectra in Figure 3, but we note that the D4 core FWHM av of 3.5 year -1 (3.4 months) is slightly better than the 2.7 year -1 (4.5 months) resolution indicated by the power spectrum analysis.

We therefore have good overall agreement and an independent confirmation of the resolution in the nitrate data sets.


Summit is an optimal location for preserving the seasonal geochemical depositional record including nitrates because the relatively high snow accumulation of 0.65 m year -1 at the surface (0.246 m year -1 water equivalent) [Meese et al., 1994; Albert and Schultz, 2002] is not dominated by wind erosion drifting features or sastrugi, and post-depositional processing effects are minimal [Hastings et al., 2004].

Summit is also not subject to katabatic winds that re-arrange the snow at down-slope locations.

Furthermore, and most importantly, any mixing of episodic snowfall events by winds will on average have the effect of reducing nitrate spike amplitudes relative to the background.


In a major study of nine soluble ions involving multiple snow pit and daily surface samples covering three years, Dibb et al. [ 2007] concluded that at least on a seasonal basis "...post- depositional changes do not greatly impact the glaciochemical records preserved at Summit." Dibb et al. [ 2007] went on to say that nitrate loss due to volatility "...is a minor (≤ 5% up to perhaps 25%) fraction of the total that is deposited..." Their findings are consistent with a previous surface and snow pit study focused on nitrates by Burkhart et al. [ 2004], who also observed impulsive nitrate features within one year of deposition at the depth and time scales discussed here and concluded that, "Over 90% of the measured nitrate in the surface snow is preserved in the pits indicating that photochemistry and temperature-dependent uptake and release from the snow do not play as important a role with preservation at Summit…" While the Burkhart et al. study did not observe a clear annual cycle and a consistent preservation of impulsive nitrate events, their nitrate study was limited to one year, and their results must be interpreted accordingly.

These findings do not, of course, prove that impulsive nitrate features at the fine resolution indicated in the current study will be preserved at depth.

However, the presence of both highly significant nitrate power spectra and consistent behavior in FWHM nitrate spikes in the BU core down to approximately 0.67 cm water equivalent depth (10 day) intervals from our results strongly support limited interference by post-depositional processes and are a validation of this analytical approach.


Mixing/dispersion effects during CFA result in coarser resolution after sampling [Breton et al., 2012].

These effects are minimized in the BU core analysis and completely absent from the discretely sampled GISP2-H data as shown in Figure 2.

The effects of dispersion and resolution loss on the Zoe and D4 cores can be demonstrated by (1) applying a Gaussian filter to the fine- resolution BU data of the form exp(-28.3t 2 ) and (2) decimating the filtered BU data by a factor of 16 (21 days) to match the sampling rate of the Zoe data from 1937 to 1951.

The coefficient corresponds to a low-pass frequency filter for f c = 3 year -1 (4 months), the point at which the contribution from adjacent samples falls off from 1 at t = 0 to exp(-π).

The filtered/decimated BU data and their power spectrum are presented in Figures 5a and 5b, respectively.

Filtering the BU data to the Zoe resolution simulates how mixing in the CFA fluid stream smoothes and removes the high-frequency peaks as shown in Figure 5a.

The resulting power spectrum of the filtered BU data in Figure 5b strongly resembles that of Zoe shown in Figure 3a.


The first observed SPEs were the relativistic high-energy (>4 GeV) events detected by cosmic ray ionization chambers in 1942, 1946, and 1949 [Forbush, 1946; 1950].

Figure 6 shows all of the high-energy solar cosmic ray ground-level events observed by ionization chambers and/or muon telescopes since the beginning of the continuous cosmic ray measurement era (1936 to present).

Such events are expected to ionize the atmosphere down to low altitudes [Atri et al., 2010; Usoskin et al., 2011].

As can be seen in Figure 6, the events in the 1940s were extremely large over a short time period compared to events during the contemporary spacecraft era (1965 to present).


In an examination of the BU core in Figure 2d, the large-amplitude impulsive nitrate increases (more than 10 standard deviations above the pre-event background) in the core are time associated with the first known very high-energy solar cosmic ray events (28 February and 7 March 1942 (combined); 25 July 1946, 19 November 1949).

This ultrafine-resolution CFA method resulted in a FWHM of 9 days (0.6 cm water equivalent) for the impulsive nitrate increases coincident with these high-energy relativistic solar cosmic ray events.

The probability that during a 14-year period (i.e. 168 months) you would purely by chance select three events that would correspond this closely to the month of known high-energy solar cosmic ray events (February/March, 1942, July 1946, and November 1949) is very small ~(3/168) 3 , or about 1 in 175,000.


Nitrate increases are also observable in the GISP2-H core but not as distinctly as in the higher-resolution BU core.

None of these events is uniquely discernible in the Zoe or D4 cores shown in Figure 2.

Figure 7 presents the BU (nitrate and conductivity) and the Zoe (multi-species) data on the same time scale.

This is an interval when the annual cycles for these two cores (BU and Zoe) are in good synchronization, based on the surface and 1947 Hekla eruption tie points, the Meese et al. [ 1994] depth-age scale, and interpolation using species that display annual cycles; the data are plotted directly as acquired without any adjustments.

Despite differences in resolution, note that these impulsive nitrate increases found in both the BU and GISP2-H cores do not correspond in time to indicators of biomass burning such as anomalous increases in ammonium or black carbon in the Zoe and D4 multi-species data such as shown in Figure 7.


In the BU core analysis, Kepko et al. [ 2009] also identified small nitrate increases that correspond to the time of strong polar cap blackouts recorded by vertical ionospheric soundings that were identified as probable solar proton events by Švestka [1966].

Solar proton events undoubtedly occurred during the solar maximum years of the 17th and 18th solar cycles; however, the only known high-energy solar cosmic ray events are those recorded by the Forbush ionization chambers.

The only short-duration impulsive nitrate events that are time associated to high-energy solar cosmic ray events are the increases in 1942, 1946, and 1949.

This is why we have concentrated on these well-documented relativistic solar cosmic ray events to show that the lack of temporal resolution in the D4 and Zoe cores do not permit the identification of these short-lived impulsive nitrate events.


Wolff et al. [ 2012] did not find a nitrate increase in the ice cores they examined corresponding to the 1859 Carrington event.

Subsequently, their analysis of this single, incompletely characterized event has been used to discredit impulsive nitrate events as possibly indicative of large fluence SPEs [e.g., Schrijver et al., 2012; Cliver et al., 2014].


After examining the data provided by Wolff et al. that overlap the GISP2-H and BU data for the well-documented, large, high-energy relativistic solar cosmic ray events in the 1940s, we conclude that their data resolution was inadequate to differentiate any of the impulsive nitrate events in the test period of 1937-1951.

The limitations on significant data resolution mean that the Zoe and D4 data sets cannot confidently detect or represent changes at frequencies greater than ~3 year -1 , or on time scales of less than approximately 3-5 months.

The 36 year -1 (~10 day) average resolution that is obtainable, as indicated by the BU core, corresponds to a depth resolution < 1 cm water equivalent at Summit.

These findings also imply that ice core analysis of nitrate at a resolution such as Zoe and D4 probably could not discern the Carrington event as well.


We note that the GISP2-H core power spectrum up to its sampling interval frequency appears to be similar to the BU core power spectrum as shown in Figures 3c and 3d.

The fact that the BU data resolution makes it possible to discern impulsive nitrate events means that there is valuable information down to time scales of order 10 days in Summit ice core data that is currently not being exploited.


These results have relevance and impact beyond the issue of SPE resolvability in the polar ice core nitrate record.

This study shows that the ice sheet at Summit contains sub-seasonal information in at least some species at the approximate time scale of snowfall events that can be extracted relatively easily for comparison with current and historical climatological records and applied to studying interactions between different species.

This will allow glaciologists and atmospheric scientists to better understand sources in the atmosphere and the transport mechanisms of impurities to the ice sheet, as well as post-depositional processes.


We suggest additional fine-resolution, multiple species analysis that include nitrate and potentially interfering and "fixing" impurities (i.e., ammonium, black carbon, vanillic acid, dust, and sea salt) with replicate sampling at times of other potentially large-amplitude solar events in the last two millennia (e.g., 14 C and 10 Be events) such as events documented circa 774-775 A.D. and 993-994 A.D. [Miyake et al., 2013; Melott and Thomas, 2012; Usoskin et al., 2013].

A similar recommendation was made by Wolff et al. [ 2008].


We stress that astrophysical ionization events are not expected to produce any of the chemical species attributable to volcanoes or wildfires, other than nitrate.


This is important, as there are indications of much more energetic events on stars similar to the Sun [Nogami et al., 2014] which are potentially very dangerous if they occur on the Sun as well.


The medieval events were very high in fluence or had extreme spectral hardness since 14 C is dependent on high-energy proton fluence [Thomas et al., 2013], and ice core nitrate studies may be important in our understanding of these events by effectively giving information on the total energy deposition in the atmosphere, and thus a crude approximation to the spectrum and total energy deposition.


Soft solar events with enough fluence to account for the observed 14 C in 774-775 A.D. and 993-994 A.D. can severely deplete the ozone layer and are potentially catastrophic [Thomas et al., 2013].


Smart et al. ( 2014) suggested that the detection of nitrate spikes in polar ice cores from solar energetic particle (SEP) events could be achieved if an analytical system with sufficiently high resolution was used.

Here we show that the spikes they associate with SEP events are not reliably recorded in cores from the same location, even when the resolution is clearly adequate.

We explain the processes that limit the effective resolution of ice cores.

Liquid conductivity data suggest that the observed spikes are associated with sodium or another nonacidic cation, making it likely that they result from deposition of sea salt or similar aerosol that has scavenged nitrate, rather than from a primary input of nitrate in the troposphere.

We consider that there is no evidence at present to support the identification of any spikes in nitrate as representing SEP events.

Although such events undoubtedly create nitrate in the atmosphere, we see no plausible route to using nitrate spikes to document the statistics of such events.


Large solar energetic particle (SEP) events have the potential to severely disrupt satellite, communications, and electronic systems.

There is therefore strong motivation to establish a proxy that could document the statistics of occurrence of SEP events of different magnitudes and in particular the recurrence frequency of the largest events.

There has long been a controversy as to whether spikes in the concentration of nitrate in polar ice cores can be used as such a proxy [1][2][3][4][5].

The perspective of the proponents, coming from the space physics community, has been that SEP events will produce NOx in the atmosphere, some of which will be deposited in ice.

They have then attempted to align measured spikes with known SEP event dates to establish a link.

The perspective of the opponents, coming from the atmospheric chemistry and ice core community, has been that any signal would be too small and broad to be detected as a spike, and that there are other causes of such spikes, unrelated to SEPs.


In an attempt to answer the questions posed by the controversy, and to reach both scientific communities, we presented a study [6] in which numerous high-resolution ice core profiles of nitrate from Greenland and Antarctic ice cores were compiled and compared for a 40 year period surrounding the well-known Carrington space weather event of 1859.

We showed that a peak corresponding to that event was not present in most cores and that most nitrate peaks in Greenland during the 40 year period were due to the transit of biomass burning plumes over the ice core site (simultaneously depositing ammonium, formate, and to a lesser extent nitrate [7], along with specific fire tracers).

Subsequently, a new paper [8] has been published, essentially as a critique of our paper [6].

This has three main conclusions: 1. The Carrington Event was a poor choice of test case because it is not clear whether it had the characteristics that the authors would expect to lead to a significant and sharp nitrate enhancement.

The resolution typically used to discern nitrate spikes in ice cores is insufficient to discover the kind of events the authors have in mind.

3. Analysis at higher resolution and measuring multiple chemical species may allow nitrate spikes caused by SEPs to be isolated, reinstating the possibility to assess their occurrence using the ice core record.


In this comment we would like to discuss each of these points in turn.

Before doing so, we think it would be helpful to summarize two issues on which we think that the authors of the commented paper [8] and ourselves can now agree, which may not have been so obvious in earlier discussions.

SEPs deposit most of their energy and therefore produce most NOx in the middle stratosphere or above.

A source of NOx at these altitudes would take months to years to reach ground level, would be broad and diffuse over time, and would be diluted by other sources.

The signature of such a source could never be a sharp spike deposited almost immediately after the event.

It seems therefore to now be a common ground that only hard spectrum events that can deposit energy into the troposphere could possibly produce the kind of spikes being described, and only nitrate produced at low altitudes should be seen as spikes.

It also is agreed that there are other causes of sharp nitrate spikes in polar ice, and in particular that some nitrate spikes, previously attributed to SEPs, are in fact caused by biomass burning plumes.

This is critical because it instantly establishes that inventories of nitrate spikes without additional chemical information cannot be used to establish the statistics of SEP events, and this was actually the main message intended in our earlier paper [6].

We now discuss the three main issues we have identified from the paper on which we are commenting [8].


The Role of the Carrington Event We acknowledge that this event may not have deposited energy at low altitudes and that a nitrate spike of the kind the authors now propose would therefore not be expected.

We emphasize that our earlier paper [6] used the 40 years around the Carrington Event as an example period, in which we demonstrated that most peaks previously claimed to be SEP-related actually have a different origin.

Our conclusion about the use of nitrate to identify SEP events did not rely on the Event itself or alone.

However, the apparent coincidence of timing of the largest integrated nitrate peak in a 400 year period, and the Carrington Event, had previously been used as a major statistical underpinning of the hypothesis that nitrate spikes were indeed caused by SEPs [9].

Once that coincidence is removed (because the spike has the signature of a biomass burning event), so that there is no evidence for any spike associated with the Carrington Event, the idea that any nitrate spikes above background are due to SEPs reverts to being speculation.

We agree that it is worthwhile to assess whether other events, known to have a hard spectrum, might show a signature, but the idea cannot be considered to have any prior support.

In the reply to this comment [10], it is claimed that there is a nitrate peak in the GISP2-H core associated with the February 1956 SEP event.

However, given the rapidly changing snow accumulation rate deduced in this part of the core [8, Figure 1] (14 samples in 1955 but 35 in 1956), the dating of the nitrate peak must be considered uncertain within several months, and the evidence that the nitrate peak is related to the SEP is very weak.

As an additional point, our earlier work does establish that events such as the Carrington, which was associated with a huge geomagnetic storm, cannot be logged through nitrate.


Ice Core Resolution Smart et al. [ 8] carried out power spectral analysis to assess the resolution of different ice core records, and on this basis they suggest that many of them were inadequate to detect the kind of signals that SEPs might cause.

First, we comment that the resolution of most of the analytical systems in use has been characterized directly by applying a rapid change in concentration at the melter and observing the character of the signal at the detector.

This is an empirical and direct way to discover what kind of smoothing is caused by mixing of water on the melt head, in the tubes leading to the detector, and in the detector itself.

It therefore includes all the sources of dispersion that would occur for a real sample.

The resolutions quoted in Table 1 of our earlier paper [6] were generally derived in this way.

It is certainly likely that the system used on the Boston University (BU) core, analyzing only one component, has a higher resolution than the multi-component systems used at Zoe and D4.

However, this analysis ignores many issues concerning the way in which signals are recorded in ice cores, which inherently limit the resolution that is useful and reliable.

Chemicals can be deposited either by wet or dry deposition.

If they are dry deposited, they may give a very thin layer between snowfalls.

If they are deposited by wet deposition, then they may give a signal that is initially the width of a snowfall (typically millimeters to centimeters).

While there are numerous snowfall events each year at Summit (84 events were recorded in 2001), they are far from uniformly distributed through the year [11].

This has two consequences: first, it is impossible to accurately attach a calendar date to a layer in an ice core, because the snowfall quantity varies strongly from month to month.

Based on [11], linear interpolation of the quantity of new snow with time within a year would lead to an error of up to about 2 months at some parts of the year.

Second, there are months when there are only one or two snowfall events, so that the effective resolution, even in the deposited fresh snow, is 1–2/month.

With no a priori way of knowing which months this applies to, the reliable resolution (if one is going to assess event frequencies) in the deposited snow in central Greenland is of order 1 month.

However, after snowfall, snow is redistributed through wind, leading to mixing of different snowfall layers, and to inhomogeneous deposition across sastrugi, where some parts of the surface may contain a thick layer, and the layer may be completely lost from other parts of the surface.

Recent model studies suggest that drifting snow occurs on 50 or more days per year in central Greenland [12].

Finally, nitrate that is deposited as nitric acid is known to be mobile in the snow pack, so that even sharp peaks become smoothed through vapor redistribution.

Nitrate that is deposited as aerosol will not be subject to this process but suffers from the issue that the deposition rate may be controlled by atmospheric concentrations of the countercation [5][13] rather than by concentrations of nitrate itself.

For example, an influx of marine air containing high concentrations of sea salt will scavenge acidic nitrate from the atmosphere, leading to deposition of a nitrate spike even in the absence of any primary input of nitrate.

Of course, despite these issues, an event lasting only a few days can be detected if it is large enough.

Indeed, the numerous biomass burning events that have been detected on the basis of markers such as ammonium, formate [14][15], and vanillic acid clearly derive from events that would only have passed over the ice core site for days, but many give clear nitrate signals [6].

However, a method that would rely on very narrow signals being reliably present in an ice core at such high resolution cannot be successful.

This is illustrated in Smart et al. ’s [8] own paper.

The BU core shows perhaps five peaks that could be identified as sharp nitrate spikes in the period 1937–1951.

These spikes appear to be 1–2 cm across and therefore should clearly show up in the GISP2-H core (which has a resolution of 1.5 cm from discretely cut samples, which equates to about 0.03 years at this age).

We have (Figure 1) binned the data from the BU core into 0.03 year sections to mimic what the H core should show if the same peaks were recorded.

We bin rather than smooth [10], because discrete samples are indeed bins of the ice section.

Some years have more than 30 samples in the H core; however, changing our bins to 0.04 or even 0.05 years does not affect the result.

Assuming the dating of both cores is correct, it is immediately obvious that the largest peak in BU (in late 1946), which should show a peak of 250–340 ppb after binning (depending on the position of the bin boundaries), is not seen in the H core.

Other significant sharp spikes in BU are also not seen at the expected depth in the H core; although one can find peaks in the H core at ages near to those in BU in some cases (e.g., at the end of 1949), they actually occur in the wrong part of the seasonal nitrate curve.

The attempts to find plausible peak matches [10, section 3.3] require such a flexible attitude to dating, seasonality and peak size and shape that it is hard to imagine a situation in which an apparent match would not be found.

In fact, the GISP2-H core also shows one very clear spike, but it is in a year when BU shows no spike.

Even if these spikes could be attributed to SEPs, they are not reliably recorded in adjacent cores.

We note that the very high resolution Law Dome (Antarctica) ice core was sampled discretely at about 12–20 samples/year (decreasing with depth) and also showed no significant nitrate enhancement, let alone a sharp spike, after individual SEP events [4], although a small, broad, enhancement of nitrate concentrations was found between 3 and 15 months after the SEP date, when averaged over the event population.

We note also that we see no clear nitrate signal in the Law Dome DSS core around the 10Be peak associated with an event in 775 A.D. [16], recently identified as most likely a hard spectrum event 25–50 times as strong as the February 1956 event [17].


A Signature of SEP Events It has been suggested that replicate sampling of several cores, with multiple chemical species, and at very high resolution, will allow SEP signals to be isolated [8].

In principle, deposition of acidic nitrate might, at least in the preindustrial era, be indicative of SEP or other events of atmospheric origin, distinguishable from biomass burning events (with associated ammonium) or deposition of nitrate as a consequence of scavenging by sea salt or dust.

This criterion (of nitrate peaks with no measured countercation) was used to isolate candidate peaks in surface snow in a recent paper [13].

However, if an additional requirement is that the peak preserved in ice at depth must be very narrow, such as those discussed [8], then we would predict that they must have been deposited as aerosol and will therefore not have an acidic signature that might be a fingerprint of an SEP event.

No cation information exists for the BU or GISP2-H core data.

However, we can infer the nature of the cation from the liquid conductivity, which was also presented [18][8].

The largest nitrate peak in the BU core, in 1946, rises about 400 ppb (6.5 μeq L⁻¹) above the background.

Using well-documented ionic conductances, we would expect such a peak to be accompanied by a liquid conductivity increase of almost 3 μS cm⁻¹, exactly what would be expected in the case where Na+ is the countercation (and similar for ammonium or calcium).

A similar calculation confirms that none of the sharp peaks shown in the BU core between 1937 and 1951 are acidic.

Finally, we need to consider whether it is plausible that the events discussed [8] could arise from a hard SEP event acting in the lower atmosphere.

Modeling studies are needed to assess this.

Newly accepted work [19] using the Whole Atmosphere Community Climate Model found that very large hypothetical SEP events, 2–3 orders of magnitude larger than those observed in recent decades, produced, as expected, NOy enhancements above the troposphere but insufficient NOx in the lowest 15 km of the atmosphere to produce spikes in Greenland ice cores.

Earlier work [20] would also not support the kind of enhancements in nitrate deposition flux that would be needed to observe spikes for events such as those in the 1940s and 1950s.

We understand that other modeling studies are in progress, and we await their results with interest, emphasizing that to be relevant to the production of very sharp spikes, such models will need to focus on production in the troposphere or lowest stratosphere.


Conclusion Smart et al. [ 8] showed that very sharp nitrate peaks may be detected in a system with very high resolution.

However, there is no evidence that these arise from SEPs.

Liquid conductivity data confirm that many sharp peaks are not acidic, making it likely that they are a by-product of influx of sea salt, biomass burning, or dust aerosol, rather than a consequence of a significant influx of nitrate.

There seems no a priori way to distinguish SEP signals from other causes of nitrate enhancement, and we again emphasize that the evidence that was used previously, regarding the coincidence in date of SEP events and nitrate spikes, is no longer valid.

In any case, we have shown clearly that such spikes are not reliably deposited in adjacent cores, for reasons we have discussed, which makes the use of such sharp features to log the power and frequency of SEP events impractical.

We do not doubt that the largest SEPs will cause an enhancement of nitrate in the middle atmosphere and in extreme cases the troposphere.

As ice core scientists, we would very much like to be able to use a proxy such as that envisaged, but we cannot see a plausible route for identifying and using nitrate deposition in snow to diagnose past SEPs.

The use of 10Be [17], although at much lower time resolution, seems a much more promising path.


Wolff et al. [ 2016] comment on Smart et al. [ 2014] and in doing so concentrate on issues other than the main point.

They do not dispute our central assertion, the inadequate resolution of nearly all extant ice cores for detection of impulsive nitrate events (spikes) from any source, including past solar proton events (SPEs).


We explain why comparing two short-length cores from other researchers and analyzed by different methods is insufficient for disputing subannual reproducibility, and call for a multiple, fine-resolution, replicate core study to resolve this issue.

While acknowledging the creation of nitrate by SPEs and the existence of ice core nitrate spikes detected by others, they present several weak arguments, such as alleged scavenging of nitrate by some unnamed and unmeasured aerosol, and why no enhanced nitrate signal for documenting SPE statistics should be distinguishable in the ice.


These are not derived from the main points in our Smart et al. [ 2014] paper.

We address these briefly and show that ionization from the February 1956 SPE was sufficient to produce a winter, likely acidic, nitrate spike at Summit, Greenland.


While noting some convergence of interpretation, we show why their claim that nitrate spikes cannot be used for deriving SPE statistics is unproven and why rejection of fine resolution core studies as unreliable is premature.


To understand the complexities regarding the Comment by Wolff et al. [ 2016] and this Reply, some background material is necessary.

Table 1 in the McCracken et al. [ 2001] paper is a tabulation of 72 short duration, “impulsive nitrate events” or spikes that those authors proposed as representing very large fluence solar proton events (SPEs) with the solar particles ionizing the atmosphere and forming oxides of nitrogen, leading to enhanced nitrate deposition in polar ice.

Wolff et al. [ 2012] chose to concentrate on one event associated with the white light solar flare observed on 1 September 1859 [Carrington, 1860] and noted that they were unable to find a corresponding nitrate increase in several “properly dated” ice cores.

Based on the analysis of this one event and their assertion that “all large spikes” in their data were “due to biomass burning plumes,” they concluded that nitrates in ice cores cannot be used to derive SPE statistics.


Smart et al. [ 2014] noted in the data supplied by Wolff and coworkers that no nitrate spikes corresponding to known high-energy ground level solar cosmic ray events observed by cosmic ray muon detectors could be found.

Smart et al. [ 2014] attributed this to insufficient resolution of ice core data primarily acquired to study long-term climatological phenomena.

Using standard statistical analysis software, Smart et al. [ 2014] noted a substantial difference between the resolutions reported in Table 1 of Wolff et al. [ 2012] and the statistically significant data resolutions in their Zoe and D4 ice cores (closest in location to the GISP2-H ice core), contradicting their claims of “comparable resolution” to the GISP2-H data, which contained significant nitrate spikes.

Smart et al. [ 2014] concluded that only ice cores with statistically significant, fine resolution of less than 2 months are capable of resolving short duration nitrate spikes regardless of their source.


This resolution issue has implications regarding inferences drawn previously about a host of short-term phenomena in coarsely resolved ice cores, including the claimed associations between biomass burning, sea salt, and nitrate spikes that cannot be proven with analyses that only delineate broad summer/winter variations.

It needs to be addressed.


We are now in the “comment stage.” Wolff et al. [ 2016] maintain that the entire nitrate spike concept for deriving SPE statistics is inconsistent with well-regarded standard models for transport through the atmosphere and preservation in ice.

These are the key points in the argument Wolff et al. [ 2016] present, but they are not in response to the key point in Smart et al. [ 2014].


The basic thesis of our paper [Smart et al., 2014] that the data in Wolff et al. [ 2012] lack the resolution to identify 0.5–2 month duration impulsive nitrate events has not been challenged in a substantive way.

Nevertheless, Wolff et al. [ 2016] continue to maintain that their ice core data are “high resolution” and “The resolution typically used to discern nitrate spikes.

” We strongly dispute these assertions.

In their Comment, Wolff et al. [ 2016] focus primarily on side issues to dispute our paper and to repeat previous arguments [e.g., Legrand and Delmas, 1986; Wolff et al., 2012; Duderstadt et al., 2014] against the feasibility of observing very large, hard spectrum SPEs as spikes in the polar nitrate record.


For example, they list our side point that the Carrington SPE was not well documented and is not a good test as our first main conclusion.

Our conclusion was not an attempt at “reinstating” SPE-produced nitrate spikes because the concept has never been disproved, despite Wolff et al. ’s [2016] continuing efforts.

Although it appears that the two sides in this debate have drawn incrementally closer, as our understanding of the physical and chemical processes involved has improved, there is still considerable disagreement, and we welcome this opportunity to respond to these additional arguments to clarify the issues.


Wolff et al. ’s [2016] assumption, coming from the atmospheric chemistry and ice core community, that both sides agree SPEs deliver most of their energy to the middle stratosphere and above, is only partly correct.

Coming from the space physics, cosmic ray, and atmospheric physics communities and with expertise in polar glaciology, we emphatically disagree that this is the only locale for energy deposition to generate nitrate spikes and that this generalization applies to all SPEs.

Standard energy deposition models have routinely omitted primary particles with energies above 300 MeV and have neglected air shower cascades that deposit additional energy in the lower stratosphere (from which rapid deposition can occur and which Wolff et al. [ 2016] continue to ignore), as well as the troposphere.

We contend it is the high-fluence, high-energy events that can produce an impulsive nitrate enhancement in ice cores.

We discuss this issue below.


Wolff et al. [ 2016] now assert that “many” nitrate spikes in Greenland cores are “likely” caused from scavenging by “sea salt, biomass burning, or dust aerosol,” but this is very different from their previous claims [i.e., Wolff et al., 2012] and has not been proven.

First, we find it remarkable that they assert that most nitrate spikes must have this association using ice core analyses that have not resolved a single impulsive nitrate spike.

Given their limited 3–5 month resolution, the Wolff et al. [ 2012] data essentially only reflect the annual cycle where nitrates, biomass burning, and a number of additional indicators vary in phase and tend to peak in summer.

This summer maximum does not apply to impulsive nitrate enhancements, which are of shorter duration and can occur at any time of year, including in winter when biomass burning interference is minimal.

For example, Figure 1 in Smart et al. [ 2014] shows the winter nitrate spike in Greenland associated with the 23 February 1956 SPE.

Second, Wolff et al. [ 2008] conducted a coastal study at Halley, Antarctica, which reflects a marine environment with associated high sea-salt and nitrate concentrations in surface snow samples, not ice cores.

They specifically state that in central Greenland, which is remote from the oceans, sea salt “…will rarely be at the concentrations that could cause the effects described…” Third, there are exceptions even with the coarse-resolution data.


The strong statement in Wolff et al. ’s [2012] abstract that “in the 40 years surrounding 1859…where other chemistry was measured, all large spikes have the unequivocal signal…of biomass burning plumes” is simply wrong.

Their supporting Figure 4 selectively covers only 20 of the 40 years in their study.

When the full 40 year interval for the D4 core is shown (Figure 1), two of the five highest summer nitrate peaks display no associated biomass burning signal.

Similar results also can be observed in the Zoe core.

Given these issues, nitrate spike source conclusions must be considered speculative.


We also agree that impulsive nitrate spikes produced by SPEs are difficult to isolate from nitrate produced by other sources without additional chemical information, which is why we support multispecies analyses in our call for fine-resolution, follow-on studies.

However, the concluding statement at the end of Wolff et al. ’s [2012] abstract and Wolff et al. ’s [2016] main message continues to be “Nitrate spikes cannot be used to derive the statistics of (SPEs).” Given that Wolff et al. [ 2012] did not resolve impulsive nitrate events in any of their ice cores used to dispute an association with SPEs, the subsequent effect of their absolute conclusion on the glaciology and space physics communities compelled us to take issue with their publication.