{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,8,25]],"date-time":"2026-08-25T16:37:11Z","timestamp":1787675831973,"version":"build-2784847793"},"reference-count":60,"publisher":"MDPI AG","issue":"4","license":[{"start":{"date-parts":[[2021,2,7]],"date-time":"2021-02-07T00:00:00Z","timestamp":1612656000000},"content-version":"vor","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0\/"}],"funder":[{"name":"California Tobacco Related Research Program","award":["T30IP0998"],"award-info":[{"award-number":["T30IP0998"]}]},{"DOI":"10.13039\/100000054","name":"National Cancer Institute","doi-asserted-by":"publisher","award":["CA 69375"],"award-info":[{"award-number":["CA 69375"]}],"id":[{"id":"10.13039\/100000054","id-type":"DOI","asserted-by":"publisher"}]}],"content-domain":{"domain":[],"crossmark-restriction":false},"short-container-title":["JCM"],"abstract":"<jats:p>Seasons can affect human inflammatory status and the occurrence of diseases, and foods may also have differential impacts on inflammation across seasons; however, few studies have investigated whether there are independent and joint impacts of seasons and red meat, fruit and vegetable intakes on inflammation in breast cancer survivors. We conducted a cross-sectional study by leveraging a large cohort, the Women\u2019s Healthy Eating and Living (WHEL) study. The WHEL study comprised primarily early stage breast cancer survivors and collected blood samples, dietary intake, demographic, and health status information at baseline. We selected 2919 participants who provided baseline dietary information and had measurement of C-reactive protein (CRP), a general marker of inflammation. In our multivariable-adjusted analyses, we found that red meat intakes were positively associated, while fruit and vegetable intakes were inversely associated with CRP; blood collected in the winter season was associated with lower CRP when compared to summer; and increased smoking intensity and body mass index (BMI) as well as having cardio-metabolic conditions (such as heart disease or diabetes) were positively associated with CRP. Furthermore, we examined the joint associations of food intakes and the season of blood draw with CRP in different subgroups. We found that moderate intakes of red meat were associated with a reduction of CRP in winter but not in other seasons; increased intakes of fruit and vegetables were associated with reduced inflammation in most seasons except winter. These associations were observed in most subgroups except past smokers with pack-years \u2265 15, in whom we observed no benefit of red meat intakes in winter. Our study provides valuable evidence for considering seasonal impacts on inflammation and seasonal food impacts in different subgroups among breast cancer survivors. The results of our study are in line with one of the emphases of the current NIH 2020\u20132030 nutrition strategy plan\u2014namely, pay attention to what, when, and who should eat.<\/jats:p>","DOI":"10.3390\/jcm10040636","type":"journal-article","created":{"date-parts":[[2021,2,8]],"date-time":"2021-02-08T20:51:51Z","timestamp":1612817511000},"page":"636","update-policy":"https:\/\/doi.org\/10.3390\/mdpi_crossmark_policy","source":"Crossref","is-referenced-by-count":8,"title":["Interrelationship of Seasons with Inflammation, Red Meat, Fruit, and Vegetable Intakes, Cardio-Metabolic Health, and Smoking Status among Breast Cancer Survivors"],"prefix":"10.3390","volume":"10","author":[{"ORCID":"https:\/\/orcid.org\/0000-0003-1679-3511","authenticated-orcid":false,"given":"Tianying","family":"Wu","sequence":"first","affiliation":[{"name":"Division of Epidemiology and Biostatistics, School of Public Health, San Diego State University, San Diego, CA 92182, USA"},{"name":"Moores Cancer Center, School of Medicine, University of California, San Diego, CA 92093, USA"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Rajashree","family":"Shinde","sequence":"additional","affiliation":[{"name":"Division of Epidemiology and Biostatistics, School of Public Health, San Diego State University, San Diego, CA 92182, USA"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-4025-0077","authenticated-orcid":false,"given":"Robert","family":"Castro","sequence":"additional","affiliation":[{"name":"School of Exercise and Nutritional Sciences, San Diego State University, San Diego, CA 92182, USA"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"John P.","family":"Pierce","sequence":"additional","affiliation":[{"name":"Moores Cancer Center, School of Medicine, University of California, San Diego, CA 92093, USA"}],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"1968","published-online":{"date-parts":[[2021,2,7]]},"reference":[{"key":"ref_1","first-page":"982","article-title":"Seasonal effects on human physiological adaptation factors, thermotolerance and plasma fibronectin","volume":"63","author":"DuBose","year":"1992","journal-title":"Aviat. Space Environ. Med."},{"key":"ref_2","unstructured":"Case, R.M. (1985). Variations in Human Physiology, Manchester University Press."},{"key":"ref_3","doi-asserted-by":"crossref","first-page":"545","DOI":"10.1016\/j.physbeh.2004.05.001","article-title":"Seasonal changes in metabolic and temperature responses to cold air in humans","volume":"82","author":"Westerterp","year":"2004","journal-title":"Physiol. Behav."},{"key":"ref_4","doi-asserted-by":"crossref","first-page":"338","DOI":"10.1016\/j.ijcard.2005.03.045","article-title":"Seasonal variation of C-reactive protein in apparently healthy Koreans","volume":"107","author":"Sung","year":"2006","journal-title":"Int. J. Cardiol."},{"key":"ref_5","doi-asserted-by":"crossref","first-page":"313","DOI":"10.1373\/clinchem.2008.111245","article-title":"Seasonal and sex variation of high-sensitivity C-reactive protein in healthy adults: A lon-gitudinal study","volume":"55","author":"Chiriboga","year":"2009","journal-title":"Clin. Chem."},{"key":"ref_6","doi-asserted-by":"crossref","first-page":"676","DOI":"10.1093\/ndt\/gfu367","article-title":"Season affects body composition and estimation of fluid overload in haemodialysis patients: Variations in body composition; a survey from the European MONDO database","volume":"30","author":"Broers","year":"2015","journal-title":"Nephrol. Dial. Transplant."},{"key":"ref_7","first-page":"47","article-title":"Seasonal disease activity and serum vitamin D levels in rheumatoid arthritis, ankylosing spondylitis and osteoarthritis","volume":"13","author":"Yazmalar","year":"2013","journal-title":"Afr. Health Sci."},{"key":"ref_8","doi-asserted-by":"crossref","first-page":"373","DOI":"10.1007\/s10654-013-9772-4","article-title":"Stroke seasonality associations with subtype, etiology and laboratory results in the Ludwigshafen Stroke Study (LuSSt)","volume":"28","author":"Palm","year":"2013","journal-title":"Eur. J. Epidemiol."},{"key":"ref_9","doi-asserted-by":"crossref","first-page":"1558S","DOI":"10.1093\/ajcn\/87.5.1558S","article-title":"Protein, weight management, and satiety","volume":"87","author":"Westman","year":"2008","journal-title":"Am. J. Clin. Nutr."},{"key":"ref_10","doi-asserted-by":"crossref","first-page":"5","DOI":"10.1186\/1743-7075-1-5","article-title":"Diet induced thermogenesis","volume":"1","author":"Westerterp","year":"2004","journal-title":"Nutr. Metab."},{"key":"ref_11","doi-asserted-by":"crossref","first-page":"493","DOI":"10.1007\/s00394-019-01918-5","article-title":"Seasonal variation of diet quality in a large middle-aged and elderly Dutch popula-tion-based cohort","volume":"59","author":"Cepeda","year":"2020","journal-title":"Eur. J. Nutr."},{"key":"ref_12","doi-asserted-by":"crossref","first-page":"129","DOI":"10.1023\/A:1017542928978","article-title":"Seasonal variations in dietary intake affect the consistency of dietary assessment","volume":"17","author":"Shahar","year":"2001","journal-title":"Eur. J. Epidemiol."},{"key":"ref_13","doi-asserted-by":"crossref","first-page":"1015","DOI":"10.1038\/ejcn.2015.22","article-title":"Seasonal variation in food intake and the interaction effects of sex and age among adults in southern Brazil","volume":"69","author":"Rossato","year":"2015","journal-title":"Eur. J. Clin. Nutr."},{"key":"ref_14","doi-asserted-by":"crossref","first-page":"346","DOI":"10.1016\/j.jgo.2018.07.010","article-title":"Breast cancer treatment and its effects on aging","volume":"10","author":"Chang","year":"2019","journal-title":"J. Geriatr. Oncol."},{"key":"ref_15","doi-asserted-by":"crossref","first-page":"e000250","DOI":"10.1136\/esmoopen-2017-000250","article-title":"Biology of premature ageing in survivors of cancer","volume":"2","author":"Kirkland","year":"2017","journal-title":"ESMO Open"},{"key":"ref_16","doi-asserted-by":"crossref","first-page":"2493","DOI":"10.1002\/ijc.28241","article-title":"Mortality risk in former smokers with breast cancer: Pack-years vs. smoking status","volume":"133","author":"Saquib","year":"2013","journal-title":"Int. J. Cancer"},{"key":"ref_17","doi-asserted-by":"crossref","unstructured":"Lafourcade, A., His, M., Baglietto, L., Boutron-Ruault, M.-C., Dossus, L., and Rondeau, V. (2018). Factors associated with breast cancer recurrences or mortality and dynamic prediction of death using history of cancer recurrences: The French E3N cohort. BMC Cancer, 18.","DOI":"10.1186\/s12885-018-4076-4"},{"key":"ref_18","doi-asserted-by":"crossref","first-page":"2170","DOI":"10.1200\/JCO.2008.17.5935","article-title":"Impact of Diabetes Mellitus on Complications and Outcomes of Adjuvant Chemotherapy in Older Patients With Breast Cancer","volume":"27","author":"Srokowski","year":"2009","journal-title":"J. Clin. Oncol."},{"key":"ref_19","doi-asserted-by":"crossref","first-page":"32","DOI":"10.1016\/j.advms.2018.10.003","article-title":"Hypertension prevalence in early breast cancer patients un-dergoing primary surgery","volume":"64","author":"Kozlowska","year":"2019","journal-title":"Adv. Med. Sci."},{"key":"ref_20","doi-asserted-by":"crossref","first-page":"728","DOI":"10.1016\/S0197-2456(02)00241-6","article-title":"A randomized trial of the effect of a plant-based dietary pattern on additional breast cancer events and survival: The Women\u2019s Healthy Eating and Living (WHEL) Study","volume":"23","author":"Pierce","year":"2002","journal-title":"Control Clin. Trials"},{"key":"ref_21","doi-asserted-by":"crossref","first-page":"193","DOI":"10.5993\/AJHB.31.2.8","article-title":"Validation of the WHI Brief Physical Activity Questionnaire among Women Diagnosed with Breast Cancer","volume":"31","author":"Rock","year":"2007","journal-title":"Am. J. Health Behav."},{"key":"ref_22","doi-asserted-by":"crossref","first-page":"225","DOI":"10.1007\/s10549-006-9284-y","article-title":"Correlates of physical activity level in breast cancer survivors participating in the Women\u2019s Healthy Eating and Living (WHEL) Study","volume":"101","author":"Hong","year":"2007","journal-title":"Breast Cancer Res. Treat."},{"key":"ref_23","doi-asserted-by":"crossref","first-page":"210","DOI":"10.1017\/S0007114517001908","article-title":"Alternative Healthy Eating Index 2010, Dietary Inflammatory Index and risk of mortality: Results from the Whitehall II cohort study and meta-analysis of previous Dietary Inflammatory Index and mortality studies","volume":"118","author":"Shivappa","year":"2017","journal-title":"Br. J. Nutr."},{"key":"ref_24","doi-asserted-by":"crossref","first-page":"2398","DOI":"10.1002\/ijc.30208","article-title":"Dietary inflammatory index and prostate cancer survival","volume":"139","author":"Zucchetto","year":"2016","journal-title":"Int. J. Cancer"},{"key":"ref_25","doi-asserted-by":"crossref","first-page":"289","DOI":"10.1159\/000333148","article-title":"Age-Dependent Changes in Temperature Regulation\u2014A Mini Review","volume":"58","author":"Blatteis","year":"2012","journal-title":"Gerontology"},{"key":"ref_26","doi-asserted-by":"crossref","first-page":"74","DOI":"10.2741\/3677","article-title":"Central neural pathways for thermoregulation","volume":"16","author":"Morrison","year":"2011","journal-title":"Front. Biosci."},{"key":"ref_27","doi-asserted-by":"crossref","first-page":"1135","DOI":"10.1093\/ajcn\/72.5.1135","article-title":"Effect of fat-reduced diets on 24-h energy expenditure: Comparisons between animal protein, vegetable protein, and carbohydrate","volume":"72","author":"Mikkelsen","year":"2000","journal-title":"Am. J. Clin. Nutr."},{"key":"ref_28","doi-asserted-by":"crossref","first-page":"635","DOI":"10.1097\/00075197-200311000-00005","article-title":"The significance of protein in food intake and body weight regulation","volume":"6","year":"2003","journal-title":"Curr. Opin. Clin. Nutr. Metab. Care"},{"key":"ref_29","doi-asserted-by":"crossref","first-page":"968S","DOI":"10.1093\/jn\/134.4.968S","article-title":"Dietary Protein Impact on Glycemic Control during Weight Loss","volume":"134","author":"Layman","year":"2004","journal-title":"J. Nutr."},{"key":"ref_30","doi-asserted-by":"crossref","first-page":"1173","DOI":"10.3945\/ajcn.114.104976","article-title":"Red meat, dairy, and insulin sensitivity: A randomized crossover intervention study","volume":"101","author":"Turner","year":"2015","journal-title":"Am. J. Clin. Nutr."},{"key":"ref_31","doi-asserted-by":"crossref","first-page":"2474","DOI":"10.2337\/db11-0194","article-title":"Inflammation Is Necessary for Long-Term but Not Short-Term High-Fat Diet-Induced Insulin Resistance","volume":"60","author":"Lee","year":"2011","journal-title":"Diabetes"},{"key":"ref_32","doi-asserted-by":"crossref","first-page":"E1610","DOI":"10.1210\/jc.2013-2038","article-title":"Does Inflammation Determine Metabolic Health Status in Obese and Nonobese Adults?","volume":"98","author":"Phillips","year":"2013","journal-title":"J. Clin. Endocrinol. Metab."},{"key":"ref_33","doi-asserted-by":"crossref","unstructured":"Wu, T., Seaver, P., Lemus, H., Hollenbach, K., Wang, S.E., and Pierce, J.P. (2019). Associations between Dietary Acid Load and Biomarkers of Inflammation and Hyperglycemia in Breast Cancer Survivors. Nutrients, 11.","DOI":"10.3390\/nu11081913"},{"key":"ref_34","doi-asserted-by":"crossref","first-page":"803","DOI":"10.7326\/0003-4819-82-6-803","article-title":"Lactic Acidosis from Carboxyhemoglobinemia After Smoke Inhalation","volume":"82","author":"Buehler","year":"1975","journal-title":"Ann. Intern. Med."},{"key":"ref_35","doi-asserted-by":"crossref","first-page":"843","DOI":"10.1093\/carcin\/bgr048","article-title":"Urinary pH, cigarette smoking and bladder cancer risk","volume":"32","author":"Alguacil","year":"2011","journal-title":"Carcinogenesis"},{"key":"ref_36","doi-asserted-by":"crossref","first-page":"41","DOI":"10.1016\/j.maturitas.2018.01.016","article-title":"Seasonality of physical activity, sedentary behavior, and sleep in a middle-aged and elderly population: The Rotterdam study","volume":"110","author":"Cepeda","year":"2018","journal-title":"Maturitas"},{"key":"ref_37","unstructured":"Schonbaum, E., and Lomax, P. (1990). Response of microcirculation to hot and cold environment. Thermoregulation Physiology and Bio-Chemistry, Pergamon Press."},{"key":"ref_38","doi-asserted-by":"crossref","unstructured":"Kenny, G.P., and Flouris, A.D. (2014). Thermoregulatory system and its response to thermal stress. Protective Clothing: Managing Thermal Stress, Woodhead Publishing Ltd.","DOI":"10.1533\/9781782420408.3.319"},{"key":"ref_39","first-page":"17","article-title":"The effect of physical training on sweating responses measured during muscular exercises and resting postures in hot environments","volume":"22","author":"Araki","year":"1976","journal-title":"Kobe J. Med Sci."},{"key":"ref_40","doi-asserted-by":"crossref","unstructured":"Keino, S., Borne, B.V.D., and Plasqui, G. (2014). Body composition, water turnover and physical activity among women in Narok County, Kenya. BMC Public Health, 14.","DOI":"10.1186\/1471-2458-14-1212"},{"key":"ref_41","doi-asserted-by":"crossref","first-page":"90","DOI":"10.1111\/jhn.12077","article-title":"Evaluation of seasonality on total water intake, water loss and water balance in the general population in Greece","volume":"26","author":"Malisova","year":"2013","journal-title":"J. Hum. Nutr. Diet."},{"key":"ref_42","doi-asserted-by":"crossref","first-page":"1604","DOI":"10.1038\/sj.ejcn.1602013","article-title":"Variation in nutrient intakes among women in Shanghai, China","volume":"58","author":"Cai","year":"2004","journal-title":"Eur. J. Clin. Nutr."},{"key":"ref_43","doi-asserted-by":"crossref","unstructured":"Dmitrieva, N.I., and Burg, M.B. (2015). Elevated sodium and dehydration stimulate inflammatory signaling in endo-thelial cells and promote atherosclerosis. PLoS ONE, 10.","DOI":"10.1371\/journal.pone.0128870"},{"key":"ref_44","first-page":"23","article-title":"Electrolyte and acid-base disorders in inflammatory bowel disease","volume":"26","author":"Barkas","year":"2013","journal-title":"Ann. Gastroenterol."},{"key":"ref_45","doi-asserted-by":"crossref","first-page":"1911","DOI":"10.1093\/jn\/135.8.1911","article-title":"Grape Polyphenols Exert a Cardioprotective Effect in Pre- and Postmenopausal Women by Lowering Plasma Lipids and Reducing Oxidative Stress","volume":"135","author":"Zern","year":"2005","journal-title":"J. Nutr."},{"key":"ref_46","doi-asserted-by":"crossref","first-page":"317S","DOI":"10.1093\/ajcn\/81.1.317S","article-title":"Polyphenols and disease risk in epidemiologic studies","volume":"81","author":"Arts","year":"2005","journal-title":"Am. J. Clin. Nutr."},{"key":"ref_47","doi-asserted-by":"crossref","first-page":"611","DOI":"10.1200\/JCO.2015.64.3809","article-title":"American Cancer Society\/American Society of Clinical Oncology Breast Cancer Survivorship Care Guideline","volume":"34","author":"Runowicz","year":"2016","journal-title":"J. Clin. Oncol."},{"key":"ref_48","doi-asserted-by":"crossref","first-page":"43","DOI":"10.3322\/caac.21319","article-title":"American Cancer Society\/American Society of Clinical Oncology Breast Cancer Survivorship Care Guideline","volume":"66","author":"Runowicz","year":"2016","journal-title":"CA Cancer J. Clin."},{"key":"ref_49","unstructured":"WCRF (2021, January 17). World Cancer Research Fund International. Available online: https:\/\/www.wcrf.org\/dietandcancer\/exposures\/meat-fish-dairy2."},{"key":"ref_50","doi-asserted-by":"crossref","unstructured":"Wu, T., Hsu, F.-C., and Pierce, J.P. (2020). Increased Acid-Producing Diet and Past Smoking Intensity Are Associated with Worse Prognoses among Breast Cancer Survivors: A Prospective Cohort Study. J. Clin. Med., 9.","DOI":"10.3390\/jcm9061817"},{"key":"ref_51","doi-asserted-by":"crossref","first-page":"50","DOI":"10.1186\/1475-2891-9-50","article-title":"A review and meta-analysis of prospective studies of red and processed meat intake and prostate cancer","volume":"9","author":"Alexander","year":"2010","journal-title":"Nutr. J."},{"key":"ref_52","doi-asserted-by":"crossref","first-page":"349","DOI":"10.1017\/S0954422410000235","article-title":"A review and meta-analysis of red and processed meat consumption and breast cancer","volume":"23","author":"Alexander","year":"2010","journal-title":"Nutr. Res. Rev."},{"key":"ref_53","doi-asserted-by":"crossref","first-page":"1","DOI":"10.1186\/s12937-015-0111-3","article-title":"A review and meta-analysis of prospective studies of red and processed meat, meat cooking methods, heme iron, heterocyclic amines and prostate cancer","volume":"14","author":"Bylsma","year":"2015","journal-title":"Nutr. J."},{"key":"ref_54","doi-asserted-by":"crossref","first-page":"191","DOI":"10.1007\/s10549-015-3380-9","article-title":"Red and processed meat intake and risk of breast cancer: A meta-analysis of prospective studies","volume":"151","author":"Guo","year":"2015","journal-title":"Breast Cancer Res. Treat"},{"key":"ref_55","doi-asserted-by":"crossref","first-page":"230","DOI":"10.1002\/ijc.31046","article-title":"Red and processed meat intake and cancer risk: Results from the prospective NutriNet-Sante cohort study","volume":"142","author":"Diallo","year":"2018","journal-title":"Int. J. Cancer"},{"key":"ref_56","doi-asserted-by":"crossref","unstructured":"Chan, D.S.M., Lau, R., Aune, D., Vieira, R., Greenwood, D.C., Kampman, E., and Norat, T. (2011). Red and Processed Meat and Colorectal Cancer Incidence: Meta-Analysis of Prospective Studies. PLoS ONE, 6.","DOI":"10.1371\/journal.pone.0020456"},{"key":"ref_57","doi-asserted-by":"crossref","first-page":"106","DOI":"10.1053\/j.gastro.2011.04.013","article-title":"Nonlinear reduction in risk for colorectal cancer by fruit and vegetable intake based on me-ta-analysis of prospective studies","volume":"141","author":"Aune","year":"2011","journal-title":"Gastroenterology"},{"key":"ref_58","doi-asserted-by":"crossref","first-page":"576","DOI":"10.1093\/ajcn\/68.3.576","article-title":"Estimation of net endogenous noncarbonic acid production in humans from diet potassium and protein contents","volume":"68","author":"Frassetto","year":"1998","journal-title":"Am. J. Clin. Nutr."},{"key":"ref_59","first-page":"S33","article-title":"A practical approach to the balance between acid production and renal acid excretion in humans","volume":"19","author":"Frassetto","year":"2006","journal-title":"J. Nephrol."},{"key":"ref_60","doi-asserted-by":"crossref","first-page":"791","DOI":"10.1016\/S0002-8223(95)00219-7","article-title":"Potential Renal Acid Load of Foods and its Influence on Urine pH","volume":"95","author":"Remer","year":"1995","journal-title":"J. Am. Diet. Assoc."}],"container-title":["Journal of Clinical Medicine"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/www.mdpi.com\/2077-0383\/10\/4\/636\/pdf","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2025,10,11]],"date-time":"2025-10-11T05:20:58Z","timestamp":1760160058000},"score":1,"resource":{"primary":{"URL":"https:\/\/www.mdpi.com\/2077-0383\/10\/4\/636"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2021,2,7]]},"references-count":60,"journal-issue":{"issue":"4","published-online":{"date-parts":[[2021,2]]}},"alternative-id":["jcm10040636"],"URL":"https:\/\/doi.org\/10.3390\/jcm10040636","relation":{},"ISSN":["2077-0383"],"issn-type":[{"value":"2077-0383","type":"electronic"}],"subject":[],"published":{"date-parts":[[2021,2,7]]}}}