Skip to main content
Log in

Seasonal Dynamics of Red Blood Parameters in Healthy People in Regions with Different Types of Climate: a Meta-Analysis

  • Published:
Izvestiya, Atmospheric and Oceanic Physics Aims and scope Submit manuscript

Abstract

It is known that in mammals living in climates other than tropical, hemoconcentration is usually observed in winter. The average modern person actively uses artificial lighting, heating, air conditioning, and also does not experience prolonged periods of hunger and thirst. The purpose of this work is to investigate, using a meta-analysis of publications, the seasonal dynamics of red blood parameters (hematocrit, hemoglobin, red blood cells count) in healthy human, as well as to study its dependence on gender and climate characteristics of the region. We analyzed data on the seasonal dynamics of red blood parameters in healthy people from 27 panel and 2 cross-sectional studies conducted in 26 regions of the world. The conducted meta-analysis showed that in humans, hematocrit and hemoglobin are significantly higher in winter than in summer. There was no pronounced seasonal dynamics of red blood cells count. Gender had no effect on the seasonal dynamics of red blood parameters. The meta-analysis showed that in regions with a large amplitude of circannual fluctuations in air temperature, seasonal changes in hemoglobin were maximum, and in a climate with a small difference between winter and summer temperatures, seasonal fluctuations in hemoglobin were not pronounced. Pronounced seasonal changes in hematocrit were noted in a climate in which atmospheric pressure was significantly higher in winter than in summer. In a climate in which atmospheric pressure in winter and summer did not differ significantly, seasonal changes in hematocrit were not pronounced. As a result, in modern humans, the seasonal dynamics of red blood parameters is mainly caused by circannual fluctuations in air temperature and atmospheric pressure. Our present and previous studies have shown that atmospheric pressure, along with the photoperiod and air temperature, influences seasonal changes in the functioning of the body, most likely through the mechanisms of oxygenation.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1.
Fig. 2.
Fig. 3.
Fig. 4.
Fig. 5.
Fig. 6.
Fig. 7.

Similar content being viewed by others

REFERENCES

  1. Agadzhanyan, N.A., Ignat’ev, L.I., and Radysh, I.V., Influence of climatic factors on seasonal rhythms of the blood system in inhabitants of Kislovodsk, Ekol. Chel., 2007, vol. 3, pp. 3–8. https://www.elibrary.ru/item. asp?id=9428348.

    Google Scholar 

  2. Alon, D.B., Chaimovitz, C., Dvilansky, A., Lugassy, G., Douvdevani, A., Shany, S., and Nathan, I., Novel role of 1,25(OH)(2)D(3) in induction of erythroid progenitor cell proliferation, Exp. Hematol., 2002, vol. 30, no. 5, pp. 403–409. https://doi.org/10.1016/s0301-472x(02)00789-0

    Article  Google Scholar 

  3. Anthanont, P., Levine, J.A., McCrady-Spitzer, S.K., and Jensen, M.D., Lack of seasonal differences in basal metabolic rate in humans: A cross-sectional study, Horm. Metab. Res., 2017, vol. 49, no. 1, pp. 30–35. https://doi.org/10.1055/s-0042-107793

    Article  Google Scholar 

  4. Azizi-Soleiman, F., Vafa, M., Abiri, B., and Safavi, M., Effects of iron on vitamin D metabolism: A systematic review, Int. J. Prev. Med., 2016, vol. 7, p. 126. https://doi.org/10.4103/2008-7802.195212

  5. Backstrand, J.R., Allen, L.H., Black, A.K., de Mata, M., and Pelto, G.H., Diet and iron status of nonpregnant women in rural Central Mexico, Am. J. Clin. Nutr., 2002, vol. 76, no. 1, pp. 156–164. https://doi.org/10.1093/ajcn/76.1.156

    Article  Google Scholar 

  6. Balzan, S., Del Carratore, R., Nicolini, G., Forini, F., Lubrano, V., Simili, M., Benedetti, P.A., and Iervasi, G., TSH induces co-localization of TSH receptor and Na/K-ATPase in human erythrocytes, Cell. Biochem. Funct., 2009, vol. 27, no. 5, pp. 259–263. https://doi.org/10.1002/cbf.1567

    Article  Google Scholar 

  7. Barney, C.C. and Kuhrt, D.M., Intermittent heat exposure and thirst in rats, Physiol. Rep., 2016, vol. 4, no. 8, id e12767. https://doi.org/10.14814/phy2.12767

  8. Bäckman, S., Larjo, A., Soikkeli, J., Castren, J., Ihalainen, J., and Syrjala, M., Season and time of day affect capillary blood hemoglobin level and low hemoglobin deferral in blood donors: Analysis in a national blood bank, Transfusion, 2016, vol. 56, no. 6, pp. 1287–1294. https://doi.org/10.1111/trf.13578

    Article  Google Scholar 

  9. Bella, L.M., Fieri, I., Tessaro, F.H.G., Nolasco, E.L., Nunes, F.P.B., Ferreira, S.S., Azevedo, C.B., and Martins, J.O., Vitamin D modulates hematological parameters and cell migration into peritoneal and pulmonary cavities in Alloxan-Diabetic mice, Biomed. Res. Int., 2017, id 7651815. https://doi.org/10.1155/2017/7651815

  10. Boiko, E.R. and Tkachev, A.V., Lipid metabolism in permanent residents of the North, Fiziol. Chel., 1994, vol. 20, no. 2, pp. 136–142.

    Google Scholar 

  11. Borenstein, M., Hedges, L.V., Higgins, J.P.T., and Rothstein, H.R., Introduction to Meta-Analysis, Chichester: Wiley, 2009.

    Book  Google Scholar 

  12. Braekkan, S.K., Mathiesen, E.B., Njolstad, I., Wilsgaard, T., and Hansen, J.B., Hematocrit and risk of venous thromboembolism in a general population. The Tromsø study, Haematologica, 2010, vol. 95, no. 2, pp. 270–275. https://doi.org/10.3324/haematol.2009.008417

    Article  Google Scholar 

  13. Bremner, A.P., Feddema, P., Joske, D.J., Leedman, P.J., O’Leary, P.C., Olynyk, J.K., and Walsh, J.P., Significant association between thyroid hormones and erythrocyte indices in euthyroid subjects, Clin. Endocrinol. (Oxford, U. K.), 2012, vol. 76, no. 2, pp. 304–311. https://doi.org/10.1111/j.1365-2265.2011.04228.x

    Article  Google Scholar 

  14. Broadbent, S., Seasonal changes in haematology, lymphocyte transferrin receptors and intracellular iron in ironman triathletes and untrained men, Eur. J. Appl. Physiol., 2011, vol. 111, no. 1, pp. 93–100. https://doi.org/10.1007/s00421-010-1635-z

    Article  Google Scholar 

  15. Calton, E.K., Keane, K.N., Raizel, R., Rowlands, J., Soares, M.J., and Newsholme, P., Winter to summer change in vitamin d status reduces systemic inflammation and bioenergetic activity of human peripheral blood mononuclear cells, Redox. Biol., 2017, no. 12, pp. 814–820. https://doi.org/10.1016/j.redox.2017.04.009

  16. Chaudhary, S.S., Singh, V.K., Upadhyay, R.C., Puri, G., Odedara, A.B., and Patel, P.A., Evaluation of physiological and biochemical responses in different seasons in Surti buffaloes, Vet. World, 2015, vol. 8, no. 6, pp. 727–731. https://doi.org/10.14202/vetworld.2015.727-731

    Article  Google Scholar 

  17. Checinska-Maciejewska, Z., Niepolski, L., Checinska, A., Korek, E., Kolodziejczak, B., Kopczynski, Z., Krauss, H., Pruszynska-Oszmalek, E., Kolodziejski, P., and Gibas-Dorna, M., Regular cold water swimming during winter time affects resting hematological parameters and serum erythropoietin, J. Physiol. Pharmacol., 2019, vol. 70, no. 5, pp. 747–756. https://doi.org/10.26402/jpp.2019.5.10

    Article  Google Scholar 

  18. Cheung, S.S. and Daanen, H.A., Dynamic adaptation of the peripheral circulation to cold exposure, Microcirculation, 2012, vol. 19, no. 1, pp. 65–77. https://doi.org/10.1111/j.1549-8719.2011.00126.x

    Article  Google Scholar 

  19. Cunliffe, W.J., Burton, J.L., and Shuster, S., The effect of local temperature variations on the sebum excretion rate, Brit. J. Dermatol., 1970, vol. 83, no. 6, pp. 650–654. https://doi.org/10.1111/j.1365-2133.1970.tb15759.x

    Article  Google Scholar 

  20. D’Alesandro, M.M., Reed, H.L., and Lopez, A., Hematological parameters are altered during cold air exposure, Arct. Med. Res., 1992, vol. 51, no. 1, pp. 16–22. https:// pubmed.ncbi.nlm.nih.gov/1562290/.

  21. Dardente, H., Wyse, C.A., Birnie, M.J., Dupré, S.M., Loudon, A.S., Lincoln, G.A., and Hazlerigg, D.G., A molecular switch for photoperiod responsiveness in mammals, Curr. Biol., 2010, vol. 20, no. 24, pp. 2193–2208. https://doi.org/10.1016/j.cub.2010.10.048

    Article  Google Scholar 

  22. Dardente, H., Hazlerigg, D.G., and Ebling, F.J., Thyroid hormone and seasonal rhythmicity, Front. Endocrinol., 2014, vol. 5, p. 19. https://doi.org/10.3389/fendo.2014.00019

  23. De Luca, C. and Valacchi, G., Surface lipids as multifunctional mediators of skin responses to environmental stimuli, Mediators Inflammation, 2010, id 321494. https://doi.org/10.1155/2010/321494

  24. Dobrowolska, A. and Gromadzka-Ostrowska, J., Age and androgen-related changes in morphological parameters, haematological indices and serum protein fraction in common vole (Microtus arvalis Pall.) growing in different photoperiods, Comp. Biochem. Physiol., Part A: Comp. Physiol., 1984, vol. 79, no. 2, pp. 241–249. https://doi.org/10.1016/0300-9629(84)90423-7

    Article  Google Scholar 

  25. Francesconi, R.P. and Hubbard, R.W., Chronic low-sodium diet in rats: Responses to severe heat exposure, J. Appl. Physiol., 1985, vol. 58, no. 1, pp. 152–156. https://doi.org/10.1152/jappl.1985.58.1.152

    Article  Google Scholar 

  26. Francesconi, R., Hubbard, R., and Mager, M., Thermoregulatory responses in the rat to exercise in the heat following prolonged heat exposure, J. Appl. Physiol.: Respir., Environ. Exercise Physiol., 1982, vol. 52, no. 3, pp. 734–738. https://doi.org/10.1152/jappl.1982.52.3.734

    Article  Google Scholar 

  27. Fröhlich, M., Sund, M., Russ, S., Hoffmeister, A., Fischer, H.G., Hombach, V., and Koenig, W., Seasonal variations of rheological and hemostatic parameters and acute-phase reactants in young, healthy subjects, Arterioscler., Thromb., Vasc. Biol., 1997, vol. 17, no. 11, pp. 2692–2697. https://doi.org/10.1161/01.atv.17.11.2692

    Article  Google Scholar 

  28. Gagnon, D.R., Zhang, T.J., Brand, F.N., and Kannel, W.B., Hematocrit and the risk of cardiovascular disease—the Framingham study: A 34-year follow-up, Am. Heart. J., 1994, vol. 127, no. 3, pp. 674–682. https://doi.org/10.1016/0002-8703(94)90679-3

    Article  Google Scholar 

  29. Goldberg, M.S., Giannetti, N., Burnett, R.T., Mayo, N.E., Valois, M.F., and Brophy, J.M., A panel study in congestive heart failure to estimate the short-term effects from personal factors and environmental conditions on oxygen saturation and pulse rate, Occup. Environ. Med., 2008, vol. 65, no. 10, pp. 659–666. https://doi.org/10.1136/oem.2007.034934

    Article  Google Scholar 

  30. Goswami, N., Taucher, A.A., Brix, B., Roessler, A., Koestenberger, M., Reibnegger, G., and Cvirn, G., Coagulation changes during central hypovolemia across seasons, J. Clin. Med., 2020, vol. 9, no. 11, p. 3461. https://doi.org/10.3390/jcm9113461

  31. Grœsli, A.R., Evans, A.L., Fahlman, Å., Bertelsen, M.F., Blanc, S., and Arnemo, J.M., Seasonal variation in haematological and biochemical variables in free-ranging subadult brown bears (Ursus arctos) in Sweden, BMC Vet. Res., 2015, vol. 11, p. 301. https://doi.org/10.1186/s12917-015-0615-2

  32. Hata, T., Ogihara, T., Maruyama, A., Mikami, H., Nakamaru, M., Naka, T., Kumahara, Y., and Nugent, C.A., The seasonal variation of blood pressure in patients with essential hypertension, Clin. Exp. Hypertens., Part A, 1982, vol. 4, no. 3, pp. 341–354. https://doi.org/10.3109/10641968209060747

    Article  Google Scholar 

  33. Hawley, A.W. and Peden, D.G., Effects of ration, season and animal handling on composition of bison and cattle blood, J. Wildl. Dis., 1982, vol. 18, no. 3, pp. 321–338. https://doi.org/10.7589/0090-3558-18.3.321

    Article  Google Scholar 

  34. Hoekstra, T., Veldhuizen, I., van Noord, P.A., and de Kort, W.L., Seasonal influences on hemoglobin levels and deferral rates in whole-blood and plasma donors, Transfusion, 2007, vol. 47, no. 5, pp. 895–900. https://doi.org/10.1111/j.1537-2995.2007.01207.x

    Article  Google Scholar 

  35. Hu, M., Finni, T., Sedliak, M., Zhou, W., Alen, M., and Cheng, S., Seasonal variation of red blood cell variables in physically inactive men: Effects of strength training, Int. J. Sports Med., 2008, vol. 29, no. 7, pp. 564–568. https://doi.org/10.1055/s-2007-989320

    Article  Google Scholar 

  36. Huffman, S.L., Wolff, M., and Lowell, S., Nutrition and fertility in Bangladesh: Nutritional status of nonpregnant women, Am. J. Clin. Nutr., 1985, vol. 42, no. 4, pp. 725–738. https://doi.org/10.1093/ajcn/42.4.725

    Article  Google Scholar 

  37. Ikeda, M., Watanabe, T., Koizumi, A., Ishihara, N., Cha, C.W., Sadarangani, C.P., Trishnananda, M., Ratanamaneechat, S., Kurosawa, K., Saito, K., et al., Seasonal variation in hemoglobin concentration in non-agricultural populations under various climatic conditions, Hum. Biol., 1986, vol. 58, no. 2, pp. 189–196. https://pubmed.ncbi.nlm.nih.gov/3710460/.

    Google Scholar 

  38. Ingley, E., Chappell, D., Poon, S.Y., Sarna, M.K., Beaumont, J.G., Williams, J.H., Stillitano, J.P., Tsai, S., Leedman, P.J., Tilbrook, P.A., and Klinken, S.P., Thyroid hormone receptor-interacting protein 1 modulates cytokine and nuclear hormone signaling in erythroid cells, J. Biol. Chem., 2001, vol. 276, no. 46, pp. 43428–43434. https://doi.org/10.1074/jbc.M106645200

    Article  Google Scholar 

  39. Inoue, Y., Ichinose-Kuwahara, T., Nakamura, S., Ueda, H., Yasumatsu, H., Kondo, N., and Araki, T., Cutaneous vasodilation response to a linear increase in air temperature from 28 degrees C to 40 degrees C in prepubertal boys and young men, J. Physiol. Anthropol., 2009, vol. 28, no. 3, pp. 137–144. https://doi.org/10.2114/jpa2.28.137

    Article  Google Scholar 

  40. Inoue, Y., Hayashi, Y., Kangawa, K., Suzuki, Y., Murakami, N., and Nakahara, K., Des-acyl ghrelin prevents heatstroke-like symptoms in rats exposed to high temperature and high humidity, Neurosci. Lett., 2016, vol. 615, pp. 28–32. https://doi.org/10.1016/j.neulet.2016.01.003

    Article  Google Scholar 

  41. Jin, Y.Z., Zheng, D.H., Duan, Z.Y., Lin, Y.Z., Zhang, X.Y., Wang, J.R., Han, S., Wang, G.F., and Zhang, Y.J., Relationship between hematocrit level and cardiovascular risk factors in a community-based population, J. Clin. Lab. Anal., 2015, vol. 29, no. 4, pp. 289–293. https://doi.org/10.1002/jcla.21767

    Article  Google Scholar 

  42. Jøsephson, B. and Dahlberg, G., Variations in the cell-content and chemical composition of the human blood due to age, sex and season, Scand. J. Clin. Lab. Invest., 1952, vol. 4, no. 3, pp. 216–236. https://doi.org/10.3109/00365515209060661

    Article  Google Scholar 

  43. Kamezaki, F., Sonoda, S., Tomotsune, Y., Yunaka, H., and Otsuji, Y., Seasonal variation in serum lipid levels in Japanese workers, J. Atheroscler. Thromb., 2010, vol. 17, no. 6, pp. 638–643. https://doi.org/10.5551/jat.3566

    Article  Google Scholar 

  44. Karimungi, M.G. and Joshi, B.N., Diurnal sensitivity in melatonin-induced hematological changes in the male albino rat, Biol. Signals, 1996, vol. 5, no. 5, pp. 283–290. https://doi.org/10.1159/000109201

    Article  Google Scholar 

  45. Keatinge, W.R., Coleshaw, S.R., Cotter, F., Mattock, M., Murphy, M., and Chelliah, R., Increases in platelet and red cell counts, blood viscosity, and arterial pressure during mild surface cooling: Factors in mortality from coronary and cerebral thrombosis in winter, Brit. Med. J. (Clin. Res. Ed.), 1984, vol. 289, no. 6456, pp. 405–408. https://doi.org/10.1136/bmj.289.6456.1405

    Article  Google Scholar 

  46. Keatinge, W.R., Coleshaw, S.R., Easton, J.C., Cotter, F., Mattock, M.B., and Chelliah, R., Increased platelet and red cell counts, blood viscosity, and plasma cholesterol levels during heat stress, and mortality from coronary and cerebral thrombosis, Am. J. Med., 1986, vol. 81, no. 5, pp. 795–800. https://doi.org/10.1016/0002-9343(86)90348-7

    Article  Google Scholar 

  47. Kim, L.B., Kim, E.B., and Kulikov, V.Yu., Cold resistance estimated on the basis of fetal hemoglobin changes during acute general cooling, Arct. Med. Res., 1992, vol. 51, no. 1, pp. 32–34. https://pubmed.ncbi.nlm. nih.gov/1373284/.

  48. Koono, N., Reciprocal changes in serum concentrations of triiodothyronine and reverse triiodothyronine between summer and winter in normal adult men, Endocrinol. Jpn., 1980, vol. 27, no. 4, pp. 471–476. https://doi.org/10.1507/endocrj1954.27.471

    Article  Google Scholar 

  49. Kreindl, C., Olivares, M., Brito, A., Araya, M., and Pizarro, F., Variación estacional del perfil lipídico en adultos aparentemente sanos de Santiago, Chile, Arch. Latinoam. Nutr., 2014, vol. 64, no. 3, pp. 145–152.

    Google Scholar 

  50. Kristal-Boneh, E., Froom, P., Harari, G., Shapiro, Y., and Green, M.S., Seasonal changes in red blood cell parameters, Br. J. Haematol., 1993, vol. 85, no. 3, pp. 603–607. https://doi.org/10.1111/j.1365-2141.1993.tb03354.x

    Article  Google Scholar 

  51. Kristal-Boneh, E., Froom, P., Harari, G., and Ribak, J., Seasonal differences in blood cell parameters and the association with cigarette smoking, Clin. Lab. Haematol., 1997, vol. 19, no. 3, pp. 177–181. https://pubmed. ncbi.nlm.nih.gov/9352141/.

    Article  Google Scholar 

  52. Kuroshima, A., Kurahashi, M., Doi, K., Ono, T., and Fukita, I., Effect of cold adaptation and high-fat diet on cold resistance and metabolic responses to acute cold exposure in rats, Jpn. J. Physiol., 1974, vol. 24, no. 3, pp. 277–292. https://doi.org/10.2170/jjphysiol.24.277

    Article  Google Scholar 

  53. Kuroshima, A., Doi, K., and Ohno, T., Seasonal variation of plasma glucagon concentrations in men, Jpn. J. Physiol., 1979, vol. 29, no. 6, pp. 661–668. https://doi.org/10.2170/jjphysiol.29.661

    Article  Google Scholar 

  54. Kuzmenko, N.V. and Galagudza, M.M., Dependence of seasonal dynamics of hemorrhagic and ischemic strokes on the climate of a region: A meta-analysis, Int. J. Stroke, 2021, 17474930211006296. https://doi.org/10.1177/17474930211006296

  55. Kuzmenko, N.V., Tsyrlin, V.A., and Pliss, M.G., Seasonal dynamics of melatonin, prolactin, sex hormones and adrenal hormones in healthy people: A meta-analysis, J. Evol. Biochem. Physiol., 2021a, vol. 57, no. 3, pp. 451–472.

    Article  Google Scholar 

  56. Kuzmenko, N.V., Tsyrlin, V.A., Pliss, M.G., and Galagudza, M.M., Seasonal variations in levels of human thyroid-stimulating hormone and thyroid hormones: A meta-analysis, Chronobiol. Int., 2021b, vol. 3, pp. 1–17. https://doi.org/10.1080/07420528.2020.1865394

    Article  Google Scholar 

  57. Lacas, S., Allevard, A.M., Ag’Atteinine, S., Gallo-Bona, N., Gauquelin-Koch, G., Hardin-Pouzet, H., Gharib, C., Sicard, B., and Maurel, D., Cardiac natriuretic peptide response to water restriction in the hormonal adaptation of two semidesert rodents from West Africa (Steatomys caurinus, Taterillus gracilis), Gen. Comp. Endocrinol., 2000, vol. 120, no. 2, pp. 176–189. https://doi.org/10.1006/gcen.2000.7545

    Article  Google Scholar 

  58. Lee, C.J., Lawler, G.S., and Panemangalore, M., Nutritional status of middle-aged and elderly females in Kentucky in two seasons. Pt. 2. Hematological parameters, J. Am. Coll. Nutr., 1987, vol. 6, no. 3, pp. 217–222. https://doi.org/10.1080/07315724.1987.10720184

    Article  Google Scholar 

  59. Leiper, J.B., Seonaid Primrose, C., Primrose, W.R., Phillimore, J., and Maughan, R.J., A comparison of water turnover in older people in community and institutional settings, J. Nutr. Health Aging, 2005, vol. 9, no. 3, pp. 189–193. https://pubmed.ncbi.nlm.nih.gov/15864399/.

    Google Scholar 

  60. Levy, S.B., Leonard, W.R., Tarskaia, L.A., Klimova, T.M., Fedorova, V.I., and Baltakhinova, M.E., Josh Snodgrass, J., Lifestyle mediates seasonal changes in metabolic health among the Yakut (Sakha) of Northeastern Siberia, Am. J. Hum. Biol., 2016, vol. 28, no. 6, pp. 868–878. https://doi.org/10.1002/ajhb.22879

    Article  Google Scholar 

  61. Lim, Y.H., Park, M.S., Kim, Y., Kim, H., and Hong, Y.C., Effects of cold and hot temperature on dehydration: a mechanism of cardiovascular burden, Int. J. Biometeorol., 2015, vol. 59, no. 8, pp. 1035–1043. https://doi.org/10.1007/s00484-014-0917-2

    Article  Google Scholar 

  62. Maclean, G.S. and Lee, A.K., Effects of season, temperature, and activity on some blood parameters of feral house mice (Mus musculus), J. Mammal., 1973, vol. 54, no. 3, pp. 660–667. https://pubmed.ncbi.nlm.nih.gov/ 4744931/.

    Article  Google Scholar 

  63. Maes, M., Scharpé, S., Cooreman, W., Wauters, A., Neels, H., Verkerk, R., De Meyer, F., D’Hondt, P., Peeters, D., and Cosyns, P., Components of biological, including seasonal, variation in hematological measurements and plasma fibrinogen concentrations in normal humans, Experientia, 1995, vol. 51, no. 2, pp. 141–149. https://doi.org/10.1007/BF01929358

    Article  Google Scholar 

  64. Maginniss, L.A. and Milsom, W.K., Effects of hibernation on blood oxygen transport in the golden-mantled ground squirrel, Respir. Physiol., 1994, vol. 95, no. 2, pp. 195–208. https://doi.org/10.1016/0034-5687(94)90116-3

    Article  Google Scholar 

  65. Malisova, O., Bountziouka, V., Panagiotakos, D.B., Zampelas, A., and Kapsokefalou, M., Evaluation of seasonality on total water intake, water loss and water balance in the general population in Greece, J. Hum. Nutr. Diet, 2013, vol. 26, no. 1, pp. 90–96. https://doi.org/10.1111/jhn.12077

    Article  Google Scholar 

  66. Malisova, O., Athanasatou, A., Pepa, A., Husemann, M., Domnik, K., Braun, H., Mora-Rodriguez, R., Ortega, J.F., Fernandez-Elias, V.E., and Kapsokefalou, M., Water intake and hydration indices in healthy European adults: The European hydration research study (EHRS), Nutrients, 2016, vol. 8, no. 4, id 204. https://doi.org/10.3390/nu8040204

  67. Marti-Soler, H., Gubelmann, C., Aeschbacher, S., et al., Seasonality of cardiovascular risk factors: An analysis including over 230 000 participants in 15 countries, Heart, 2014, vol. 100, pp. 1517–1523. https://doi.org/10.1136/heartjnl-2014-305623

    Article  Google Scholar 

  68. Mcdonough, J.R., Hames, C.G., Garrison, G.E., Stulb, S.C., Lichtman, M.A., and Hefelfinger, D.C., The relationship of hematocrit to cardiovascular states of health in the negro and white population of Evans county, Georgia, J. Chronic. Dis., 1965, vol. 18, pp. 243–257. https://doi.org/10.1016/0021-9681(65)90151-7

    Article  Google Scholar 

  69. Mech, L.D. and Buhl, D.A., Seasonal cycles in hematology and body mass in free-ranging gray wolves (Canis lupus) from Northeastern Minnesota, USA, J. Wildl. Dis., 2020, vol. 56, no. 1, pp. 179–185. https://doi.org/10.7589/2018-06-156

    Article  Google Scholar 

  70. Moher, D., et al. (PRISMA Group), Preferred reporting items for systematic reviews and mete-analyses: the PRISMA statement, PLoS Med., 2009, vol. 6, p. e1000097. https://doi.org/10.1371/iournal.pmed1000097

    Article  Google Scholar 

  71. Morimoto, T., Shiraki, K., and Asayama, M., Seasonal difference in responses of body fluids to heat stress, Jpn. J. Physiol., 1974, vol. 24, no. 3, pp. 249–262. https://doi.org/10.2170/jjphysiol.24.249

    Article  Google Scholar 

  72. Murciano Revert, J., Martínez-Lahuerta, J.J., and Aleixandre Porcar, L., Seasonal change in blood concentration of uric acid and its potential clinical implications, Aten Primaria, 2000, vol. 26, no. 7, pp. 468–471. https://doi.org/10.1016/s0212-6567(00)78705-1

    Article  Google Scholar 

  73. Ockene, I.S., Chiriboga, D.E., Stanek, E.J. III, Harmatz, M.G., Nicolosi, R., Saperia, G., Well, A.D., Freedson, P., Merriam, P.A., Reed, G., Ma, Y., Matthews, C.E., and Hebert, J.R., Seasonal variation in serum cholesterol levels: Treatment implications and possible mechanisms, Arch. Int. Med., 2004, vol. 164, no. 8, pp. 863–870. https://doi.org/10.1001/archinte.164.8.863

    Article  Google Scholar 

  74. Otto, C., Donner, M.G., Schwandt, P., and Richter, W.O., Seasonal variations of hemorheological and lipid parameters in middle-aged healthy subjects, Clin. Chim. Acta, 1996, vol. 256, no. 1, pp. 87–94. https://doi.org/10.1016/s0009-8981(96)06414-5

    Article  Google Scholar 

  75. Pope, C.A. III, Dockery, D.W., Kanner, R.E., Villegas, G.M., and Schwartz, J., Oxygen saturation, pulse rate, and particulate air pollution: A daily time-series panel study, Am. J. Respir. Crit. Care Med., 1999, vol. 159, no. 2, pp. 365–372. https://doi.org/10.1164/ajrccm.159.2.9702103

    Article  Google Scholar 

  76. Portaluppi, F., Smolensky, M.H., and Touitou, Y., Ethics and methods for biological rhythm research on animals and human beings, Chronobiol. Int., 2010, vol. 27, nos. 9–10, pp. 1911–1929. https://doi.org/10.3109/07420528.2010.516381

    Article  Google Scholar 

  77. Post, R.L. and Spealman, C.R., Variation of total circulating hemoglobin and reticulocyte count of man with season and following hemorrhage, J. Appl. Physiol., 1948, vol. 1, no. 3, pp. 227–233. https://doi.org/10.1152/jappl.1948.1.3.227

    Article  Google Scholar 

  78. Puchalski, W. and Heldmaier, G., Seasonal changes of heart weight and erythrocytes in the Djungarian hamster, Phodopus sungorus, Comp. Biochem. Physiol., Part A: Comp. Physiol., 1986, vol. 84, no. 2, pp. 259–263. https://doi.org/10.1016/0300-9629(86)90610-9

    Article  Google Scholar 

  79. Quisumbing, T.L., Wong, T.M., Jen, L.S., and Loh, T.T., Biochemical effects of mild iron deficiency and cold acclimatization on rat skeletal muscle, Biochem. Med., 1985, vol. 34, no. 3, pp. 355–363. https://doi.org/10.1016/0006-2944(85)90098-5

    Article  Google Scholar 

  80. Rahardja, D.P., Toleng, A.L., and Lestari, V.S., Thermoregulation and water balance in fat-tailed sheep and Kacang goat under sunlight exposure and water restriction in a hot and dry area, Animal, 2011, vol. 5, no. 10, pp. 1587–1593. https://doi.org/10.1017/S1751731111000577

    Article  Google Scholar 

  81. Refaat, B., Prevalence and characteristics of anemia associated with thyroid disorders in non-pregnant Saudi women during the childbearing age: A cross-sectional study, Biomed. J., 2015, vol. 38, no. 4, pp. 307–316. https://doi.org/10.4103/2319-4170.151032

    Article  Google Scholar 

  82. Renassia, C. and Peyssonnaux, C., New insights into the links between hypoxia and iron homeostasis, Curr. Opin. Hematol., 2019, vol. 26, no. 3, pp. 125–130. https://doi.org/10.1097/MOH.0000000000000494

    Article  Google Scholar 

  83. Rodland, K.D. and Hainsworth, F.R., Evaporative water loss and tissue dehydration of hamsters in the heat, Comp. Biochem. Physiol., Part A: Comp. Physiol., 1974, vol. 49, no. 2A, pp. 331–345. https://doi.org/10.1016/0300-9629(74)90124-8

    Article  Google Scholar 

  84. Ronnenberg, A.G., Goldman, M.B., Aitken, I.W., and Xu, X., Anemia and deficiencies of folate and vitamin B-6 are common and vary with season in Chinese women of childbearing age, J. Nutr., 2000, vol. 130, no. 11, pp. 2703–2710. https://doi.org/10.1093/jn/130.11.2703

    Article  Google Scholar 

  85. Roubicek, C.B. and Ray, D.E., Measures of skewness and kurtosis of distributions of blood and liver constituents of rats (Rattus norvegicus) at two environmental temperatures, Comp. Biochem. Physiol., Part A: Comp. Physiol., 1974, vol. 48, no. 2, pp. 205–216. https://doi.org/10.1016/0300-9629(74)90700-2

    Article  Google Scholar 

  86. Roukoyatkina, N.I., Chefer, S.I., Rifkind, J., Ajmani, R., and Talan, M.I., Cold acclimation-induced increase of systolic blood pressure in rats is associated with volume expansion, Am. J. Hypertens., 1999, vol. 12, no. 1, pp. 54–62. https://doi.org/10.1016/s0895-7061(98)00213-1

    Article  Google Scholar 

  87. Ruíz-Argüelles, G.J., Sánchez-Medal, L., Loría, A., Piedras, J., and Córdova, M.S., Red cell indices in normal adults residing at altitude from sea level to 2670 meters, Am. J. Hematol., 1980, vol. 8, no. 3, pp. 265–271. https://doi.org/10.1002/ajh.2830080304

    Article  Google Scholar 

  88. Sant’Anna, G.M. and Mortola, J.P., Thermal and respiratory control in young rats exposed to cold during postnatal development, Comp. Biochem. Physiol., Part A: Mol. Integr. Physiol., 2003, vol. 134, no. 2, pp. 449–459. https://doi.org/10.1016/s1095-6433(02)00321-5

    Article  Google Scholar 

  89. Sarne, D., Effects of the environment, chemicals and drugs on thyroid function, in Endotext, Feingold, KR, Anawalt, B, Boyce, A, et al., Eds., South Dartmouth, Mass., MDText.com, Inc., 2016. https://pubmed.ncbi. nlm.nih.gov/25905415/.

  90. Schindhelm, R.K., Boekel, E., Heima, N.E., van Schoor, N.M., and Simsek, S., Thyroid hormones and erythrocyte indices in a cohort of euthyroid older subjects, Eur. J. Int. Med., 2013, vol. 24, no. 3, pp. 241–244. https://doi.org/10.1016/j.ejim.2012.12.004

    Article  Google Scholar 

  91. Schrammel, N., Deichsel, K., Aurich, J., and Aurich, C., A long-day light program accelerates seasonal coat changes but is without effect on semen and metabolic parameters in Shetland pony stallions, Theriogenology, 2016, vol. 85, no. 5, pp. 946–953. https://doi.org/10.1016/j.theriogenology.2015.11.003

  92. Sealander, J.A., Seasonal variations in hemoglobin and hematocrit values in the northern red-backed mouse, Clethrionomys rutilus dawsoni (Merriam), in interior Alaska, Can. J. Zool., 1966, vol. 44, no. 2, pp. 213–224. https://doi.org/10.1139/z66-019

    Article  Google Scholar 

  93. Sennels, H.P., Jørgensen, H.L., Hansen, A.L., Goetze, J.P., and Fahrenkrug, J., Diurnal variation of hematology parameters in healthy young males: The Bispebjerg study of diurnal variations, Scand. J. Clin. Lab. Invest., 2011, vol. 71, no. 7, pp. 532–541. https://doi.org/10.3109/00365513.2011.602422

    Article  Google Scholar 

  94. Shapiro, Y., Hubbard, R.W., Kimbrough, C.M., and Pandolf, K.B., Physiological and hematologic responses to summer and winter dry-heat acclimation, J. Appl. Physiol.: Respir., Environ. Exercise Physiol., 1981, vol. 50, no. 4, pp. 792–798. https://doi.org/10.1152/jappl.1981.50.4.792

    Article  Google Scholar 

  95. Sharma, S. and Hashmi, M.F., Partial pressure of oxygen, in StatPearls, Treasure Island, Fla.: StatPearls, 2021. https://www.statpearls.com/ArticleLibrary/viewarticle/ 26710. https://pubmed.ncbi.nlm.nih.gov/29630271/.

    Google Scholar 

  96. Singh, K. and Kaushik, N.K., Seasonal variations in hematological and hemodynamic parameters, Int. Arch. Integr. Med., 2016, vol. 3, no. 9, pp. 54–60. https://www.iaimjournal.com/wp-content/uploads/2016/08/iaim_2016_ 0309_07.pdf.

  97. Stookey, J.D., Burg, M., Sellmeyer, D.E., Greenleaf, J.E., Arieff, A., van Hove, L., Gardner, C., and King, J.C., A proposed method for assessing plasma hypertonicity in vivo, Eur. J. Clin. Nutr., 2007, vol. 61, no. 1, pp. 143–146. https://doi.org/10.1038/sj.ejcn.1602481

    Article  Google Scholar 

  98. Sun, Z., Genetic AVP deficiency abolishes cold-induced diuresis but does not attenuate cold-induced hypertension, Am. J. Physiol. Renal. Physiol., 2006, vol. 290, no. 6, pp. F1472–F1477. https://doi.org/10.1152/ajprenal.00430.2005

    Article  Google Scholar 

  99. Tanaka, S., Fujishiro, M., Watanabe, K., Imatake, K., Suzuki, Y., Abe, M., Ishihara, H., and Tani, S., Seasonal variation in hydration status among community-dwelling elderly in Japan, Geriatr. Gerontol. Int., 2020, vol. 20, no. 10, pp. 904–910. https://doi.org/10.1111/ggi.14010

    Article  Google Scholar 

  100. Tempel, G.E. and Musacchia, X.J., Erythrocyte 2,3-diphosphoglycerate concentrations in hibernating, hypothermic, and rewarming hamsters (38589), Proc. Soc. Exp. Biol. Med., 1975, vol. 148, no. 2, pp. 588–592. https://doi.org/10.3181/00379727-148-38589

    Article  Google Scholar 

  101. Thirup, P., Haematocrit: Within-subject and seasonal variation, Sports Med., 2003, vol. 33, no. 3, pp. 231–243. https://doi.org/10.2165/00007256-200333030-00005

    Article  Google Scholar 

  102. Thorling, E.B. and Erslev, A.J., The “tissue” tension of oxygen and its relation to hematocrit and erythropoiesis, Blood, 1968, vol. 31, no. 3, pp. 332–343. https:// pubmed.ncbi.nlm.nih.gov/5640631/.

    Article  Google Scholar 

  103. Tong, E., Murphy, W.G., Kinsella, A., Darragh, E., Woods, J., Murphy, C., and McSweeney, E., Capillary and venous haemoglobin levels in blood donors: A 42-month study of 36,258 paired samples, Vox Sang, 2010, vol. 98, no. 4, pp. 547–553. https://doi.org/10.1111/j.1423-0410.2009.01285.x

    Article  Google Scholar 

  104. Touitou, Y., Touitou, C., Bogdan, A., Reinberg, A., Auzeby, A., Beck, H., and Guillet, P., Differences between young and elderly subjects in seasonal and circadian variations of total plasma proteins and blood volume as reflected by hemoglobin, hematocrit, and erythrocyte counts, Clin. Chem., 1986, vol. 32, no. 5, pp. 801–804. https://pubmed.ncbi.nlm.nih.gov/3698272/.

    Article  Google Scholar 

  105. Uchida, K., Shibuya, I., and Doi, K., Difference in the mode of acute cold-induced hypothermia between rat and hamster, Jpn. J. Physiol., 1987, vol. 37, no. 2, pp. 207–222. https://doi.org/10.2170/jjphysiol.37.207

    Article  Google Scholar 

  106. van Bergen, P., Fregly, M.J., and Papanek, P.E., Effect of a reduction in sodium intake on cold-induced elevation of blood pressure in the rat, Proc. Soc. Exp. Biol. Med., 1992, vol. 200, no. 4, pp. 472–479. https://doi.org/10.3181/00379727-200-43456

    Article  Google Scholar 

  107. van den Burg, P.J., Hospers, J.E., van Vliet, M., Mosterd, W.L., Bouma, B.N., and Huisveld, I.A., Effect of endurance training and seasonal fluctuation on coagulation and fibrinolysis in young sedentary men, J. Appl. Physiol.(1985), 1997, vol. 82, no. 2, pp. 613–620. https://doi.org/10.1152/jappl.1997.82.2.613

  108. Visaitova, H.A., Dzhambekova, A.Sh., and Anzorov, V.A., Seasonal dynamics of the level of erythrocytes and hemoglobin in the blood of students, in Science and Youth: Proceedings of the All-Russian Scientific–Practical Conference of Students, Young Scientists and Graduate Students, Grozny, 2017, pp. 71–74.

  109. Waltz, X., Hardy-Dessources, M.D., Lemonne, N., Mougenel, D., Lalanne-Mistrih, M.L., Lamarre, Y., Tarer, V., Tressieres, B., Etienne-Julan, M., Hue, O., and Connes, P., Is there a relationship between the hematocrit-to-viscosity ratio and microvascular oxygenation in brain and muscle?, Clin. Hemorheol. Microcirc., 2015, vol. 59, no. 1, pp. 37–43. https://doi.org/10.3233/CH-131742

    Article  Google Scholar 

  110. Watanabe, G.I., Climatic effect on the packed red-cell volume, Br. J. Haematol., 1958, vol. 4, no. 1, pp. 108–112. https://doi.org/10.1111/j.1365-2141.1958.tb03840.x

    Article  Google Scholar 

  111. Watanabe, T., Ishihara, N., Miyasaka, M., Koizumi, A., Fujita, H., and Ikeda, M., Hemoglobin levels among Japanese farmers: With special reference to climate and work intensity, Hum. Biol., 1986, vol. 58, no. 2, pp. 197–208. https://pubmed.ncbi.nlm.nih.gov/3710461/.

    Google Scholar 

  112. Wood, W.G., Increased HBF in adult life, Baillieres Clin. Haematol., 1993, vol. 6, no. 1, pp. 177–213. https:// pubmed.ncbi.nlm.nih.gov/7688998/.https://doi.org/10.1016/s0950-3536(05)80070-8

    Article  Google Scholar 

  113. Xu, D.L. and Hu, X.K., Season and sex have different effects on hematology and cytokines in striped hamsters (Cricetulus barabensis), J. Comp. Physiol., Part B, 2020, vol. 190, no. 1, pp. 87–100. https://doi.org/10.1007/s00360-019-01246-4

    Article  Google Scholar 

  114. Yildiz, A., Sezen, Y., Gunebakmaz, O., Kaya, Z., Altiparmak, I.H., Erkus, E., Demirbag, R., and Yilmaz, R., Association of meteorological variables and coronary blood flow, Clin. Appl. Thromb./Hemostasis, 2015, vol. 21, no. 6, pp. 570–578. https://doi.org/10.1177/1076029614554994

    Article  Google Scholar 

  115. Yoshimura, H., Seasonal changes in human body fluids, Jpn. J. Physiol., 1958, vol. 8, no. 2, pp. 165–179. https://doi.org/10.2170/jjphysiol.8.165

    Article  Google Scholar 

  116. Zeng, S.G., Zeng, T.T., Jiang, H., Wang, L.L., Tang, S.Q., Sun, Y.M., Ying, B.W., and Jia, Y.Q., A simple, fast correction method of triglyceride interference in blood hemoglobin automated measurement, J. Clin. Lab. Anal., 2013, vol. 27, no. 5, pp. 341–345. https://doi.org/10.1002/jcla.21568

    Article  Google Scholar 

  117. Zhou, R., Wang, J., Liu, J., Zhang, D., Qian, R., and Zhao, T., Changes in blood gas parameters of heatstroke rats in dry-heat environment of desert, Zhonghua Wei Zhong Bing Ji Jiu Yi Xue, 2015, vol. 27, no. 8, pp. 653–657. https://doi.org/10.3760/cma.j.issn.2095-4352.2015.08.007

    Article  Google Scholar 

  118. Zinchuk, V. and Borisiuk, M., The effect of no synthase inhibition on blood oxygen-carrying function during hyperthermia in rats, Respir. Physiol., 1998, vol. 113, no. 1, pp. 39–45. https://doi.org/10.1016/s0034-5687(98)00049-8

    Article  Google Scholar 

Download references

Funding

The work was supported within state assignment no. 056-00109-21-02.

Author information

Authors and Affiliations

Authors

Corresponding authors

Correspondence to N. V. Kuzmenko, V. A. Tsyrlin or M. G. Pliss.

Ethics declarations

The authors declare that they have no conflicts of interest.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Kuzmenko, N.V., Tsyrlin, V.A. & Pliss, M.G. Seasonal Dynamics of Red Blood Parameters in Healthy People in Regions with Different Types of Climate: a Meta-Analysis. Izv. Atmos. Ocean. Phys. 57, 1271–1292 (2021). https://doi.org/10.1134/S0001433821100078

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1134/S0001433821100078

Keywords:

Navigation