Innate and adaptive immune parameters and adiposity in non-obese adults
DOI:
https://doi.org/10.18778/1898-6773.89.1.05Keywords:
BMI, body fat percentage, waist to height ratio, innate immunity, adaptive immunityAbstract
Introduction
Excess body weight, mainly resulting from high body fat mass, is known to negatively affect immune system functioning due to the proinflammatory and prooxidative roles of adipose tissue. In general, most studies have documented the immunosuppressive role of adiposity by comparing selected immune markers between individuals of normal weight and those with obesity.
Study aims
This study investigates whether the amount of adipose tissue observed in overweight individuals may already negatively affect immune function.
Methods
We examined a broad panel of immunological parameters – both innate (WBC, neutrophil count, phagocytic uptake, respiratory burst, complement activity, lysozyme activity) and adaptive (total IgA, total IgG, CD3 count, CD19 count, the strength of antibody response to flu vaccination), in 85 women and 98 men aged 18–37 years, with a BMI between 18.5 and 29.99. As measures of adiposity, we used BMI on a continuous scale, BMI categorized as normal weight or overweight, and body fat mass percentage.
Results
In women, CD3 count was positively associated with continuous BMI (p = 0.03) and categorized BMI (p = 0.006). CD19 was positively associated with continuous BMI (p = 0.03), categorized BMI (p = 0.01), and fat mass percentage (p = 0.02). In men, categorized BMI was positively associated with phagocytic uptake (p = 0.04). However, none of these relationships would remain statistically significant after applying corrections for multiple comparisons.
Conclusion
Our results suggest that there is no relationship between adiposity and the analyzed immunity markers in non-obese (normal weight and overweight) adults.
Downloads
References
Adab, P., Pallan, M., & Whincup, P. H. (2018). Is BMI the best measure of obesity? BMJ, 360. https://doi.org/10.1136/bmj.k1274
Ahmad, R. M. A. H., & Al-Domi, H. A. (2017). Complement 3 serum levels as a pro-inflammatory biomarker for insulin resistance in obesity. Diabetes & Metabolic Syndrome: Clinical Research & Reviews, 11, S229–S232. https://doi.org/10.1016/j.dsx.2016.12.036
Alam, I., Larbi, A., & Pawelec, G. (2012). Nutritional status influences peripheral immune cell phenotypes in healthy men in rural Pakistan. Immunity & Ageing, 9(1), 16. https://doi.org/10.1186/1742-4933-9-16
Alberca, R. W., Oliveira, L. D. M., Branco, A. C. C. C., Pereira, N. Z., & Sato, M. N. (2021). Obesity as a risk factor for COVID-19: an overview. Critical Reviews in Food Science and Nutrition, 61(13), 2262–2276. https://doi.org/10.1080/10408398.2020.1775546
Alberts, B., Johnson, A., Lewis, J., Raff, M., Roberts, K., & Walter, P. (2002). Lymphocytes and the cellular basis of adaptive immunity. In Molecular Biology of the Cell. 4th edition. Garland Science.
Alasagheirin, M. H., Clark, M. K., Ramey, S. L., & Grueskin, E. F. (2011). Body mass index misclassification of obesity among community police officers. AAOHN Journal, 59(11), 469–475. https://doi.org/10.3928/08910162-20111017-01
Alhabeeb, H., Baradwan, S., Kord-Varkaneh, H., Tan, S. C., Low, T. Y., Alomar, O., Salem, H., Al-Badawi, I.A. & Abu-Zaid, A. (2021). Association between body mass index and urinary tract infection: a systematic review and meta-analysis of observational cohort studies. Eating and Weight Disorders- Studies on Anorexia, Bulimia and Obesity, 26(7), 2117–2125. https://doi.org/10.1007/s40519-020-01101-4
Al-Sufyani, A. A., & Mahassni, S. H. (2011). Obesity and immune cells in Saudi females. Innate Immunity, 17(5), 439–450. https://doi.org/10.1177/1753425910372536
Arulanandam, B., Beladi, H., & Chakrabarti, A. (2023). Obesity and COVID-19 mortality are correlated. Scientific Reports, 13(1), 5895. https://doi.org/10.1038/s41598-023-33093-3
Ashwell, M., & Clarke, G. (2009). Obesity risk: importance of the waist-toheight ratio. Nursing Standard (through 2013), 23(41), 49. https://doi.org/10.7748/ns2009.06.23.41.49.c7050
Ashwell, M., & Lejeune, S. (1996). Ratio of waist circumference to height may be better indicator of need for weight management. BMJ, 312(7027), 377. https://doi.org/10.1136/bmj.312.7027.377
Averhoff, F., Mahoney, F., Coleman, P., Schatz, G., Hurwitz, E., & Margolis, H. (1998). Immunogenicity of hepatitis B vaccines: implications for persons at occupational risk of hepatitis B virus infection. American Journal of Preventive Medicine, 15(1), 1–8. https://doi.org/10.1016/s0749-3797(98)00003-8
Banga, N., Guss, P., Banga, A., & Rosenman, K. D. (2014). Incidence and variables associated with inadequate antibody titers after pre-exposure rabies vaccination among veterinary medical students. Vaccine, 32(8), 979–983. https://doi.org/10.1016/j.vaccine.2013.12.019
Befus, M., Lowy, F. D., Miko, B. A., Mukherjee, D. V., Herzig, C. T., & Larson, E. L. (2015). Obesity as a determinant of Staphylococcus aureus colonization among inmates in maximum-security prisons in New York State. American Journal of Epidemiology, 182(6), 494–502. https://doi.org/10.10 93/aje/kwv062
Błogowski, W., Budkowska, M., Sałata, D., Serwin, K., Dołęgowska, B., Łokaj, M., Prowans, P., & Starzyńska, T. (2013). Clinical analysis of selected complement-derived molecules in human adipose tissue. Journal of Translational Medicine, 11(1), 11. https://doi.org/10.1186/1479-5876-11-11
Boero, E., Brinkman, I., Juliet, T., van Yperen, E., van Strijp, J. A., Rooijakkers, S. H., & van Kessel, K. P. (2021). Use of flow cytometry to evaluate phagocytosis of Staphylococcus aureus by human neutrophils. Frontiers in Immunology, 12, 635825. https://doi.org/10.3389/fimmu.2021.635825
Bucataru, A., Balasoiu, M., Ghenea, A. E., Zlatian, O. M., Vulcanescu, D. D., Horhat, F. G., Bagiu, I. C., Sorop, V. B., Sorop, M. I., Oprisoni, A. and Boeriu, E. & Mogoanta, S. S. (2023). Factors contributing to surgical site infections: a comprehensive systematic review of etiology and risk factors. Clinics and Practice, 14(1), 52–68 https://doi.org/10.3390/clinpract14010006
Callahan, S. T., Wolff, M., Hill, H. R., Edwards, K. M., Keitel, W., Atmar, R., Patel, S., Sahly, H. E., Munoz, F., Paul Glezen, W., Brady, R. & Todd Callahan, S. (2014). Impact of body mass index on immunogenicity of pandemic H1N1 vaccine in children and adults. The Journal of Infectious Diseases, 210(8), 1270–1274. https://doi.org/10.1093/infdis/jiu245
Campbell, K. A., Cunningham, C., Hasan, S., Hutzler, L., & Bosco III, J. A. (2015). Risk factors for developing Staphylococcus aureus nasal colonization in spine and arthroplasty surgery. Bulletin of the Hospital for Joint Diseases, 73(4), 276–281.
Cauchemez, S., Horby, P., Fox, A., Mai, L. Q., Thanh, L. T., Thai, P. Q., Hoa, L. N. M., Hien, N. T. & Ferguson, N. M. (2012). Influenza infection rates, measurement errors and the interpretation of paired serology. PLoS pathogens, 8(12), e1003061. https://doi.org/10.1371/journal.ppat.1003061
Chatzigeorgiou, A., Karalis, K. P., Bornstein, S. R., & Chavakis, T. (2012). Lymphocytes in obesity-related adipose tissue inflammation. Diabetologia, 55(10), 2583–2592. https://doi.org/10.1007/s00125-012-2607-0
Cheong, H. S., Chang, Y., Joo, E. J., Cho, A., & Ryu, S. (2019). Metabolic obesity phenotypes and risk of cellulitis: a cohort study. Journal of Clinical Medicine, 8(7), 953. https://doi.org/10.3390/jcm8070953
Cianflone, K., Lu, H., Smith, J., Yu, W., & Wang, H. (2005). Adiponectin, acylation stimulating protein and complement C3 are altered in obesity in very young children. Clinical Endocrinology, 62(5), 567–572. https://doi.org/10.1111/j.1365-2265.2005.02260.x
Dahlgren, C., & Karlsson, A. (1999). Respiratory burst in human neutrophils. Journal of immunological methods, 232(1–2), 3–14. https://doi.org/10.1016/s0022-1759(99)00146-5
Di Lorenzo, G., Balistreri, C. R., Candore, G., Cigna, D., Colombo, A., Romano, G. C., Colucci, A.T., Gervasi, F., Listí, F., Potestio, M. & Caruso, C. (1999). Granulocyte and natural killer activity in the elderly. Mechanisms of Ageing and Development, 108(1), 25–38. https://doi.org/10.1016/s0047-6374(98)00156-0
Dixon, J. B., & O’Brien, P. E. (2006). Obesity and the white blood cell count: changes with sustained weight loss. Obesity Surgery, 16(3), 251–257. https://doi.org/10.1381/096089206776116453
Dobner, J., & Kaser, S. (2018). Body mass index and the risk of infection-from underweight to obesity. Clinical Microbiology and Infection, 24(1), 24–28. https://doi.org/10.1016/j.cmi.2017.02.013
Emery, E. M., Schmid, T. L., Kahn, H. S., & Filozof, P. P. (1993). A review of the association between abdominal fat distribution, health outcome measures, and modifiable risk factors. American Journal of Health Promotion, 7(5), 342–353. https://doi.org/10.4278/0890-1171-7.5.342
Erikstrup, L. T., Dinh, K. M., Andersen, P. S., Skov, R. L., Kaspersen, K. A., Nielsen, K. R., Ellermann-Eriksen, S. & Erikstrup, C. (2019). Cohort description: the Danish blood donor Staphylococcus aureus carriage study. Clinical Epidemiology, 885–900. https://doi.org/10.2147/clep.s218637
Fan, W., Chen, X. F., Shen, C., Guo, Z. R., & Dong, C. (2016). Hepatitis B vaccine response in obesity: a meta-analysis. Vaccine, 34(40), 4835–4841. https://doi.org/10.1016/j.vaccine.2016.08.027
Fezeu, L., Julia, C., Henegar, A., Bitu, J., Hu, F. B., Grobbee, D. E., Kengne, A. P., Hercberg, S. & Czernichow, S. (2011). Obesity is associated with higher risk of intensive care unit admission and death in influenza A (H1N1) patients: a systematic review and meta-analysis. Obesity Reviews, 12(8), 653–659. https://doi.org/10.1111/j.1467-789x.2011.00864.x
Fülöp Jr, T., Fóris, G., Worum, I., & Leövey, A. (1985). Age-dependent alterations of Fc gamma receptor-mediated effector functions of human polymorphonuclear leucocytes. Clinical and Experimental Immunology, 61(2), 425.
Gao, F., Zheng, K. I., Wang, X. B., Sun, Q. F., Pan, K. H., Wang, T. Y., Chen, Y.P., Targher, G., Byrne, C. D., George, J.& Zheng, M. H. (2020). Obesity is a risk factor for greater COVID-19 severity. Diabetes Care 43(7), e72–4. https://doi.org/10.2337/dc20-0682
Gabrielsson, B. G., Johansson, J. M., Lönn, M., Jernås, M., Olbers, T., Peltonen, M., Larsson, I., Lönn, L., Sjöström, L., Carlsson, B. & Carlsson, L. M. (2003). High expression of complement components in omental adipose tissue in obese men. Obesity Research, 11(6), 699–708. https://doi.org/10.1038/oby.2003.100
Gottschlich, M. M., Mayes, T., Khoury, J. C., & Warden, G. D. (1993). Significance of obesity on nutritional, immunologic, hormonal, and clinical outcome parameters in burns. Journal of the American Dietetic Association, 93(11), 1261–1268. https://doi.org/10.1016/0002-8223(93)91952-m
Grant, R. W., & Dixit, V. D. (2015). Adipose tissue as an immunological organ. Obesity, 23(3), 512–518. https://doi.org/10.1002/oby.21003
Guglielmi, V., Colangeli, L., Scipione, V., Ballacci, S., Di Stefano, M., Hauser, L., Colella Bisogno, M., D’Adamo, M., Medda, E. & Sbraccia, P. (2022). Inflammation, underweight, malignancy and a marked catabolic state as predictors for worse outcomes in COVID-19 patients with moderate-to-severe disease admitted to Internal Medicine Unit. PLoS One, 17(5), e0268432. https://doi.org/10.1371/journal.pone.0268432
Harpsøe, M. C., Nielsen, N. M., Friis-Møller, N., Andersson, M., Wohlfahrt, J., Linneberg, A., Nohr, E.A. & Jess, T. (2016). Body mass index and risk of infections among women in the Danish National Birth Cohort. American Journal of Epidemiology, 183(11), 1008–1017. https://doi.org/10.1093/aje/kwv300
Hernandez-Mijares, A., Jarabo-Bueno, M. M., López-Ruiz, A., Solá-Izquierdo, E., Morillas- Arino, C., & Martínez-Triguero, M. L. (2007). Levels of C3 in patients with severe, morbid and extreme obesity: its relationship to insulin resistance and different cardiovascular risk factors. International Journal of Obesity, 31(6), 927–932. https://doi.org/10.1038/sj.ijo.0803543
Herwaldt, L. A., Cullen, J. J., French, P., Hu, J., Pfaller, M. A., Wenzel, R. P., & Perl, T. M. (2004). Preoperative risk factors for nasal carriage of Staphylococcus aureus. Infection Control & Hospital Epidemiology, 25(6), 481–484. https://doi.org/10.1086/502426
Hongbao, M., Young, M., & Yan, Y. (2015). Cluster of differentiation (CD). NY Science Journal, 8, 49–53.
Ibrahim, M. M. (2010). Subcutaneous and visceral adipose tissue: structural and functional differences. Obesity Reviews, 11(1), 11–18. https://doi.org/10.1111/j.1467-789x.2009.00623.x
Ilavská, S., Horváthová, M., Szabová, M., Nemessányi, T., Jahnová, E., Tulinská, J., Líšková, A., Wsolová, L., Staruchová, M. & Volkovová, K. (2012). Association between the human immune response and body mass index. Human Immunology, 73(5), 480–485. https://doi.org/10.1016/j.humimm.2012.02.023
Karki, S., Muscatello, D. J., Banks, E., MacIntyre, C. R., McIntyre, P., & Liu, B. (2018). Association between body mass index and laboratory-confirmed influenza in middle aged and older adults: a prospective cohort study. International Journal of Obesity, 42(8), 1480–1488. https://doi.org/10.1038/s41366-018-0029-x
Kato, M., Shimazu, M., Moriguchi, S., & Kishino, Y. (1996). Body mass index (BMI) is a reliable index to estimate obesity as a risk factor for deteriorating health. The Tokushima Journal of Experimental Medicine, 43(1–2), 1–6.
Kawamoto, R., Oka, Y., Tomita, H., Kodama, A., & Ootsuka, N. (2005). Association between abdominal wall fat index on ultrasonography and carotid atherosclerosis in non-obese men. Journal of Atherosclerosis and Thrombosis, 12(2), 85–91. https://doi.org/10.5551/jat.12.85
King, J. P., Nguyen, H. Q., Kiniry, E. L., Phillips, C. H., Gaglani, M., Martin, E. T., Geffel, K. M., Nowalk, M. P., Chung, J. R., Flannery, B. and Belongia, E. A. & Belongia, E. A. (2024). Elevated body mass index is not significantly associated with reduced influenza vaccine effectiveness. Scientific Reports, 14(1), 21466. https://doi.org/10.1038/s41598-024-72081-z
Kolaczkowska, E., & Kubes, P. (2013). Neutrophil recruitment and function in health and inflammation. Nature reviews immunology, 13(3), 159–175. https://doi.org/10.1038/nri3399
Koutsoumbelis, S., Hughes, A. P., Girardi, F. P., Cammisa Jr, F. P., Finerty, E. A., Nguyen, J. T., Gausden, E. & Sama, A. A. (2011). Risk factors for postoperative infection following posterior lumbar instrumented arthrodesis. JBJS, 93(17), 1627– 1633. https://doi.org/10.2106/jbjs.j.00039
Kullo, I. J., Hensrud, D. D., & Allison, T. G. (2002). Comparison of numbers of circulating blood monocytes in men grouped by body mass index (< 25, 25 to < 30, ≥ 30). American Journal of Cardiology, 89(12), 1441–1443. https://doi.org/10.1016/s0002-9149(02)02366-4
Kumar, R., & Burns, E. A. (2008). Age-related decline in immunity: implications for vaccine responsiveness. Expert Review of Vaccines, 7(4), 467–479. https://doi.org/10.1586/14760584.7.4.467
Leliefeld, P. H., Wessels, C. M., Leenen, L. P., Koenderman, L., & Pillay, J. (2016). The role of neutrophils in immune dysfunction during severe inflammation. Critical Care, 20(1), 73. https://doi.org/10.1186/s13054-016-1250-4
Liu, F., Guo, Z., & Dong, C. (2017). Influences of obesity on the immunogenicity of Hepatitis B vaccine. Human Vaccines & Immunotherapeutics, 13(5), 1014–1017. https://doi.org/10.1080/21645515.2016.1274475
Louie, J. K., Acosta, M., Samuel, M. C., Schechter, R., Vugia, D. J., Harriman, K., & Matyas, B. T. (2011). A novel risk factor for a novel virus: obesity and 2009 pandemic influenza A (H1N1). Clinical Infectious Diseases, 52(3), 301–312. https://doi.org/10.1093/cid/ciq152
Lukács, A., Horváth, E., Máté, Z., Szabó, A., Virág, K., Papp, M., Sándor, J., Ádány, R. & Paulik, E. (2019). Abdominal obesity increases metabolic risk factors in nonobese adults: a Hungarian cross-sectional study. BMC Public Health, 19(1), 1533. https://doi.org/10.1186/s12889-019-7839-1
Mahassni, S. H. (2020). Overweight and Obesity and the Immune System, Lipids and C-reactive Protein in Young and Middle-aged Saudi Female University Workers. Journal of Biochemical Technology, 11(1–2020), 49–56.
Mahassni, S. H., & Bashanfar, N. O. (2019). High Levels of Inflammatory Adipokines and C-reactive protein, and Minimal Changes in Immune Cells in Overweight and Obese Saudi Female University Students. International Journal of Pharmaceutical Research & Allied Sciences, 8(1).
Maier, H. E., Kuan, G., Gresh, L., Lopez, R., Sanchez, N., Schiller, A., Ojeda S., Harris E., Balmaseda A., & Gordon, A. (2021). Obesity is associated with increased susceptibility to influenza A (H1N1pdm) but not H3N2 infection. Clinical Infectious Diseases, 73(11), e4345–e4352. https://doi.org/10.1093/cid/ciaa928
Marshall, J. S., Warrington, R., Watson, W., & Kim, H. L. (2018). An introduction to immunology and immunopathology. Allergy, Asthma & Clinical Immunology, 14(Suppl 2), 49. https://doi.org/10.1186/s13223-018- 0278-1
Martin, E. T., Archer, C., McRoberts, J., Kulik, J., Thurston, T., Lephart, P., & Kaye, K. S. (2013). Epidemiology of severe influenza outcomes among adult patients with obesity in Detroit, Michigan, 2011. Influenza and Other Respiratory Viruses, 7(6), 1004–1007. https://doi.org/10.1111/irv.12115
Marzullo, P., Minocci, A., Giarda, P., Marconi, C., Tagliaferri, A., Walker, G. E., Scacchi, M., Aimaretti, G. & Liuzzi, A. (2014). Lymphocytes and immunoglobulin patterns across the threshold of severe obesity. Endocrine, 45(3), 392–400. https://doi.org/10.1007/s12020-013-0006-z
Matsuzawa, Y., Nakamura, T., Shimomura, I., & Kotani, K. (1995). Visceral fat accumulation and cardiovascular disease. Obesity Research, 3(S5), 645S–647S. https://doi.org/10.1002/j.1550-8528.1995.tb00481.x
Mehta, A. I., Babu, R., Karikari, I. O., Grunch, B., Agarwal, V. J., Owens, T. R., Friedman, A. H., Bagley, C. A. & Gottfried, O. N. (2012). 2012 Young Investigator Award winner: the distribution of body mass as a significant risk factor for lumbar spinal fusion postoperative infections. Spine, 37(19), 1652–1656. https://doi.org/10.1097/brs.0b013e318241b186
Mohajan, D., & Mohajan, H. K. (2023). Body mass index (BMI) is a popular anthropometric tool to measure obesity among adults. Journal of Innovations in Medical Research, 2(4), 25–33.
Moreno-Navarrete, J. M., & Fernández- Real, J. M. (2019, January). The complement system is dysfunctional in metabolic disease: Evidences in plasma and adipose tissue from obese and insulin resistant subjects. In Seminars in Cell & Developmental Biology (Vol. 85, pp. 164–172). Academic Press.
Moser, J. A. S., Galindo‐Fraga, A., Ortiz‐ Hernández, A. A., Gu, W., Hunsberger, S., Galán‐Herrera, J. F., Guerrero, M.L., Ruiz‐ Palacios, G.M., Beigel, J. H., La Red ILI 002 Study Group, Magaña‐Aquino, M. & Cherpitel, D. E. N. (2019). Underweight, overweight, and obesity as independent risk factors for hospitalization in adults and children from influenza and other respiratory viruses. Influenza and Other Respiratory Viruses, 13(1), 3–9. https://doi.org/10.1111/irv.12618
Muscari, A., Massarelli, G., Bastagli, L., Poggiopollini, G., Tomassetti, V., Drago, G., Martignani, C., Pacilli, P., Boni, P. & Puddu, P. (2000). Relationship of serum C3 to fasting insulin, risk factors and previous ischaemic events in middle-aged men. European Heart Journal, 21(13), 1081–1090. https://doi.org/10.1053/euhj.1999.2013
Muscari, A., Massarelli, G., Bastagli, L., Poggiopollini, G., Tomassetti, V., Volta, U., Puddu, G.M. & Puddu, P. (1998). Relationship between serum C3 levels and traditional risk factors for myocardial infarction. Acta Cardiologica, 53(6), 345–354.
Nagel, J. E., Pyle, R. S., Chrest, F. J., & Adler, W. H. (1982). Oxidative metabolism and bactericidal capacity of polymorphonuclear leukocytes from normal young and aged adults. Journal of Gerontology, 37(5), 529–534. https://doi.org/10.1093/geronj/37.5.529
Neidich, S. D., Green, W. D., Rebeles, J., Karlsson, E. A., Schultz-Cherry, S., Noah, T. L., Chakladar, S., Hudgens, M. G., Weir, S. S. & Beck, M. A. (2017). Increased risk of influenza among vaccinated adults who are obese. International Journal of Obesity, 41(9), 1324–1330. https://doi.org/10.1038/ijo.2017.131
NHLBI. 1998. NHLBI Obesity Education Initiative Expert Panel on the Identification, Evaluation, and Treatment of Overweight and Obesity in Adults. NIH publication no. 98–4083.
Nieman, D. C., Henson, D. A., Nehlsen- Cannarella, S. L., Ekkens, M., Utter, A. C., Butterworth, D. E., & Fagoaga, O. R. (1999). Influence of obesity on immune function. Journal of the American Dietetic Association, 99(3), 294–299. https://doi.org/10.1016/s0002-8223(99)00077-2
Nieto, F. J., Szklo, M., Folsom, A. R., Rock, R., & Mercuri, M. (1992). Leukocyte count correlates in middle-aged adults: the Atherosclerosis Risk in Communities (ARIC) Study. American Journal of Epidemiology, 136(5), 525–537. https://doi.org/10.1093/oxfordjournals.aje.a116530
Nilsson, B., Hamad, O. A., Ahlström, H., Kullberg, J., Johansson, L., Lindhagen, L., Haenni, A., Ekdahl, K. N. & Lind, L. (2014). C3 and C4 are strongly related to adipose tissue variables and cardiovascular risk factors. European Journal of Clinical Investigation, 44(6), 587–596. https://doi.org/10.1111/eci.12275
Nowak, J., Pawłowski, B., Borkowska, B., Augustyniak, D., & Drulis-Kawa, Z. (2018). No evidence for the immunocompetence handicap hypothesis in male humans. Scientific Reports, 8(1), 7392. https://doi.org.10.1038/s41598-018-25694-0
Nseir, W., Farah, R., Mahamid, M., Sayed-Ahmad, H., Mograbi, J., Taha, M., & Artul, S. (2015). Obesity and recurrent urinary tract infections in premenopausal women: a retrospective study. International Journal of Infectious Diseases, 41, 32–35. https://doi.org/10.1016/j.ijid.2015.10.014
Ode, J. J., Pivarnik, J. M., Reeves, M. J., & Knous, J. L. (2007). Body mass index as a predictor of percent fat in college athletes and nonathletes. Medicine & Science in Sports & Exercise, 39(3), 403–409. https://doi.org/10.1249/01.mss.0000247008.19127.3e
Olsen, M. A., Nepple, J. J., Riew, K. D., Lenke, L. G., Bridwell, K. H., Mayfield, J., & Fraser, V. J. (2008). Risk factors for surgical site infection following orthopaedic spinal operations. JBJS, 90(1), 62–69. https://doi.org/10.2106/jbjs.f.01515
Olsen, K., Danielsen, K., Wilsgaard, T., Sangvik, M., Sollid, J. U., Thune, I., Eggen, A. E., Simonsen, G. S. & Furberg, A. S. (2013). Obesity and Staphylococcus aureus nasal colonization among women and men in a general population. PloS one, 8(5), e63716. https://doi.org/10.1371/journal.pone.0063716
Panagiotakos, D. B., Pitsavos, C., Yannakoulia, M., Chrysohoou, C., & Stefanadis, C. (2005). The implication of obesity and central fat on markers of chronic inflammation: The ATTICA study. Atherosclerosis, 183(2), 308–315. https://doi.org/10.1016/j.atherosclerosis.2005.03.010
Pangrazzi, L., Naismith, E., Miggitsch, C., Carmona Arana, J. A., Keller, M., Grubeck-Loebenstein, B., & Weinberger, B. (2020). The impact of body mass index on adaptive immune cells in the human bone marrow. Immunity & Ageing, 17(1), 15. https://doi.org/10.1186/s12979-020-00186-w
Phung, D. T., Wang, Z., Rutherford, S., Huang, C., & Chu, C. (2013). Body mass index and risk of pneumonia: a systematic review and meta‐analysis. Obesity Reviews, 14(10), 839–857. https://doi.org/10.1111/obr.12055
Poly, T. N., Islam, M. M., Yang, H. C., Lin, M. C., Jian, W. S., Hsu, M. H., & Jack Li, Y. C. (2021). Obesity and mortality among patients diagnosed with COVID-19: a systematic review and meta-analysis. Frontiers in Medicine, 8, 620044. https://doi.org/10.3389/fmed.2021.620044
Pond, C. M. (2005). Adipose tissue and the immune system. Prostaglandins, Leukotrienes and Essential Fatty Acids, 73(1), 17–30. https://doi.org/10.1016/j.plefa.2005.04.005
Quach, H. Q., Chen, J., Monroe, J. M., Ratishvili, T., Warner, N. D., Grill, D. E., Haralambieva, I. H., Ovsyannikova, I. G., Poland, G. A. & Kennedy, R. B. (2023). The influence of sex, body mass index, and age on cellular and humoral immune responses against measles after a third dose of measles-mumps-rubella vaccine. The Journal of Infectious Diseases, 227(1), 141– 150. https://doi.org/10.1093/infdis/jiac351
Qin, X., Lu, Y., Yang, X., Peng, Q., Wang, J., Mo, C., Wu, J., Sui, J., Liu, Y., Huang, X., Zhai, L., Yang, S., Li, R., Li, S., Yang, X., Gao, Y. & Mo, Z. (2014). Determination of reference intervals for serum complement C3 and C4 levels in Chinese Han ethnic males. Clinical Laboratory, 60(5), 775–781. https://doi.org/10.7754/clin.lab.2013.130514
Ren, Y. Y., Yin, Y. Y., Li, W. Q., Lin, Y., Liu, T., Wang, S. & Bi, Z. Q. (2013). Risk factors associated with severe manifestations of 2009 pandemic influenza A (H1N1) infection in China: a case–control study. Virology Journal, 10(1), 149. https://doi.org/10.1186/1743-422x-10-149
Ribeiro, A. F., Pellini, A. C. G., Kitagawa, B. Y., Marques, D., Madalosso, G., de Cassia Nogueira Figueira, G., Fred, J., Albernaz, R. K. M., Carvalhanas, T. R. M. P. & Zanetta, D. M. T. (2015). Risk factors for death from Influenza A (H1N1) pdm09, State of São Paulo, Brazil, 2009. PloS one, 10(3), e0118772. https://doi.org/10.1371/journal.pone.0118772
Saadatian-Elahi, M., Teyssou, R., & Vanhems, P. (2008). Staphylococcus aureus, the major pathogen in orthopaedic and cardiac surgical site infections: a literature review. International Journal of Surgery, 6(3), 238–245. https://doi.org/10.1016/j.ijsu.2007.05.001
Schwartz, J., & Weiss, S. T. (1991). Host and environmental factors influencing the peripheral blood leukocyte count. American Journal of Epidemiology, 134(12), 1402– 1409. https://doi.org/10.1093/oxfordjournals.aje.a116045
Scully, I. L., McNeil, L. K., Pathirana, S., Singer, C. L., Liu, Y., Mullen, S., Girgenti, D., Gurtman, A., Pride, M. W., Jansen, K. U., Huang, P. L., & Anderson, A. S. (2017). Neutrophil killing of Staphylococcus aureus in diabetes, obesity and metabolic syndrome: a prospective cellular surveillance study. Diabetology & Metabolic Syndrome, 9(1), 76. https://doi.org/10.1186/s13098-017-0276-3
Semins, M. J., Shore, A. D., Makary, M. A., Weiner, J., & Matlaga, B. R. (2012). The impact of obesity on urinary tract infection risk. Urology, 79(2), 266–269. https://doi.org/10.1016/j.urology.2011.09.040
Shaw, A. C., Goldstein, D. R., & Montgomery, R. R. (2013). Age-dependent dysregulation of innate immunity. Nature Reviews Immunology, 13(12), 875–887. https://doi.org/10.1038/nri3547
Sheridan, P. A., Paich, H. A., Handy, J., Karlsson, E. A., Hudgens, M. G., Sammon, A. B., Holland, L. A., Weir, S., Noah, T. L. & Beck, M. A. (2012). Obesity is associated with impaired immune response to influenza vaccination in humans. International Journal of Obesity, 36(8), 1072– 1077. https://doi.org/10.1038/ijo.2011.208
Silva, E. A., Flexa, F., & Zanella, M. T. (2009). Impact of abdominal fat and insulin resistance on arterial hypertension in non-obese women. Arquivos Brasileiros de Endocrinologia & Metabologia, 53(3), 340–343. https://doi.org/10.1590/s0004-27302009000300007
Stefan, N., Birkenfeld, A. L., Schulze, M. B., & Ludwig, D. S. (2020). Obesity and impaired metabolic health in patients with COVID-19. Nature Reviews Endocrinology, 16(7), 341–342. https://doi.org/10.1038/s41574-020-0364-6
Taira, K. G., Wang, M., Guo, W., Kam, O., & Kaufmann, T. (2024). Association of cellulitis with obesity: systematic review and meta-analysis. JMIR dermatology, 7, e54302. https://doi.org/10.2196/54302
Tamara, A., & Tahapary, D. L. (2020). Obesity as a predictor for a poor prognosis of COVID-19: A systematic review. Diabetes & Metabolic Syndrome: Clinical Research & Reviews, 14(4), 655–659. https://doi.org/10.1016/j.dsx.2020.05.020
Tanaka, S. I., Inoue, S., Isoda, F., Waseda, M., Ishihara, M., Yamakawa, T., Sugiyama, A., Takamura, Y. & Okuda, K. (1993). Impaired immunity in obesity: suppressed but reversible lymphocyte responsiveness. International journal of obesity and related metabolic disorders: journal of the International Association for the Study of Obesity, 17(11), 631–636.
Vaillant, L., La Ruche, G., Tarantola, A., & Barboza, P. (2009). Epidemiology of fatal cases associated with pandemic H1N1 influenza 2009. Eurosurveillance, 14(33), 19309. https://doi.org/10.2807/ese.14.33.19309-en
Von Eyben, F. E., Mouritsen, E., Holm, J., Montvilas, P., Dimcevski, G., Suciu, G., Helleberg, I., Kristensen, L.& Von Eyben, R. (2003). Intra-abdominal obesity and metabolic risk factors: a study of young adults. International Journal of Obesity, 27(8), 941–949. https://doi.org/10.1038/sj.ijo.0802309
Waisbren, E., Rosen, H., Bader, A. M., Lipsitz, S. R., Rogers Jr, S. O., & Eriksson, E. (2010). Percent body fat and prediction of surgical site infection. Journal of the American College of Surgeons, 210(4), 381–389. https://doi.org/10.1016/j.jamcollsurg.2010.01.004
Wang, R., Lan, C., Benlagha, K., Camara, N. O. S., Miller, H., Kubo, M., Heegaard, S., Lee, P., Yang, L., Forsman, H. & Liu, C. (2024). The interaction of innate immune and adaptive immune system. MedComm, 5(10), e714. https://doi.org/10.1002/mco2.714
Wärnberg, J., Nova, E., Moreno, L. A., Romeo, J., Mesana, M. I., Ruiz, J. R., Ortega, F. B., Sjöström, M., Bueno, M., Marcos, A. & AVENA Study Group. (2006). Inflammatory proteins are related to total and abdominal adiposity in a healthy adolescent population: the AVENA Study. The American Journal of Clinical Nutrition, 84(3), 505–512. https://doi.org/10.1093/ajcn/84.3.505
Wenisch, C., Patruta, S., Daxböck, F., Krause, R., & Hörl, W. (2000). Effect of age on human neutrophil function. Journal of Leukocyte Biology, 67(1), 40–45. https://doi.org/10.1002/jlb.67.1.40
WHO. Fact Sheet on Obesity and Overweight. Available at: http://www.who.int/mediacentre/factsheets/fs311/en/ [accessed 28 May 2025]
Witt, K. A., & Bush, E. A. (2005). College athletes with an elevated body mass index often have a high upper arm muscle area, but not elevated triceps and subscapular skinfolds. Journal of the American Dietetic Association, 105(4), 599–602. https://doi.org/10.1016/j.jada.2005.01.008
Womack, J., Tien, P. C., Feldman, J., Shin, J. H., Fennie, K., Anastos, K., Cohen, M.H., Bacon, M. C. & Minkoff, H. (2007). Obesity and immune cell counts in women. Metabolism, 56(7), 998–1004. https://doi.org/10.1016/j.metabol.2007.03.008
Wu, X., Li, C., Chen, S., Zhang, X., Wang, F., Shi, T., Li, Q.& Lin, L. (2021). Association of body mass index with severity and mortality of COVID-19 pneumonia: a two-center, retrospective cohort study from Wuhan, China. Aging (Albany NY), 13(6), 7767. https://doi.org/10.18632/aging.202813
Yang, J., Hu, J., & Zhu, C. (2021). Obesity aggravates COVID‐19: a systematic review and meta‐analysis. Journal of Medical Virology, 93(1), 257–261. https://doi.org/10.1002/jmv.26237
Yang, W. S., Chang, Y. C., Chang, C. H., Wu, L. C., Wang, J. L., & Lin, H. H. (2021, January). The association between body mass index and the risk of hospitalization and mortality due to infection: a prospective cohort study. In Open Forum Infectious Diseases (Vol. 8, No. 1, p. ofaa545). US: Oxford University Press.
Yoshimura, A., Ohnishi, S., Orito, C., Kawahara, Y., Takasaki, H., Takeda, H., Sakamoto, N. & Hashino, S. (2015). Association of peripheral total and differential leukocyte counts with obesity-related complications in young adults. Obesity Facts, 8(1), 1–16. https://doi.org/10.1159/000373881
Young, K. M., Gray, C. M., & Bekker, L. G. (2013). Is obesity a risk factor for vaccine non-responsiveness? PloS one, 8(12), e82779. https://doi.org/10.1371/journal.pone.0082779
Zarb, P., Coignard, B. P., Griškevičiene, J., Muller, A. A., Vankerckhoven, V. V., Weist, K., Goossens, M. M., Vaerenberg, S., Hopkins, S. M., Catry, B., Monnet, D. L. & Suetens, C. (2012). The European Centre for Disease Prevention and Control (ECDC) pilot point prevalence survey of healthcare-associated infections and antimicrobial use. Eurosurveillance 17(46), 20316. https://doi.org/10.2807/ese.17.46.20316-en
Downloads
Published
Issue
Section
License

This work is licensed under a Creative Commons Attribution-NonCommercial-NoDerivatives 4.0 International License.
How to Cite
Funding data
-
Narodowym Centrum Nauki
Grant numbers OPUS 4 2012/07/B/NZ8/02666


