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Season-of-birth phenomenon in health and longevity: epidemiologic evidence and mechanistic considerations

Published online by Cambridge University Press:  10 December 2020

Alexander Vaiserman Open the ORCID record for Alexander Vaiserman [Opens in a new window]
Alexander Vaiserman*
Affiliation:
Laboratory of Epigenetics, D.F. Chebotarev Institute of Gerontology, NAMS, 67 Vyshgorodska str., Kyiv04114, Ukraine
*
Address for correspondence: Alexander Vaiserman, Laboratory of Epigenetics, D.F. Chebotarev Institute of Gerontology, NAMS, 67 Vyshgorodska str., Kyiv 04114, Ukraine. Email: [email protected]
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Abstract

In many human populations, especially those living in regions with pronounced climatic differences between seasons, the most sensitive (prenatal and neonatal) developmental stages occur in contrasting conditions depending on the season of conception. The difference in prenatal and postnatal environments may be a factor significantly affecting human development and risk for later life chronic diseases. Factors potentially contributing to this kind of developmental programming include nutrition, outdoor temperature, infectious exposures, duration of sunlight, vitamin D synthesis, etc. Month of birth is commonly used as a proxy for exposures which vary seasonally around the perinatal period. Season-of-birth patterns have been identified for many chronic health outcomes. In this review, the research evidence for the seasonality of birth in adult-life disorders is provided and potential mechanisms underlying the phenomenon of early life seasonal programming of chronic disease and longevity are discussed.

Keywords

DOHaDdevelopmental programmingseasonality of birthdisease risklongevity
Type
Review
Information
Journal of Developmental Origins of Health and Disease , Volume 12 , Issue 6 , December 2021 , pp. 849 - 858
Copyright
© The Author(s), 2020. Published by Cambridge University Press in association with International Society for Developmental Origins of Health and Disease

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References

Passarino, G, De Rango, F, Montesanto, A. Human longevity: genetics or lifestyle? It takes two to tango. Immun Ageing. 2016; 13(1), 1–6.CrossRefGoogle ScholarPubMed
Vaiserman, AM. Early-life nutritional programming of longevity. J Dev Orig Health Dis. 2014; 5(5), 325–338.CrossRefGoogle ScholarPubMed
Vaiserman, A, Koliada, A, Lushchak, O. Developmental programming of aging trajectory. Ageing Res Rev. 2018; 47, 105–122.CrossRefGoogle ScholarPubMed
Watson, PE, McDonald, BW. Seasonal variation of nutrient intake in pregnancy: effects on infant measures and possible influence on diseases related to season of birth. Eur J Clin Nutr. 2007; 61, 1271–1280.CrossRefGoogle ScholarPubMed
Poeran, J, Birnie, E, Steegers, EA, Bonsel, GJ. The impact of extremes in outdoor temperature and sunshine exposure on birth weight. J Environ Health. 2016; 78(6), 92–100.Google ScholarPubMed
Li, S, Wang, J, Xu, Z, et al. Exploring associations of maternal exposure to ambient temperature with duration of gestation and birth weight: a prospective study. BMC Pregnancy Childbirth. 2018; 18(1), 513.CrossRefGoogle ScholarPubMed
Roy, MP. Maternal infection, malnutrition, and low birth weight. J Postgrad Med. 2016; 62(4), 270–271.CrossRefGoogle ScholarPubMed
Ideraabdullah, FY, Belenchia, AM, Rosenfeld, CS, et al. Maternal vitamin D deficiency and developmental origins of health and disease (DOHaD). J Endocrinol. 2019; JOE–18–0541.R2.CrossRefGoogle Scholar
Smith, AD, Crippa, A, Woodcock, J, Brage, S. Physical activity and incident type 2 diabetes mellitus: a systematic review and dose–response meta–analysis of prospective cohort studies. Diabetologia. 2016; 59(12), 2527–2545.CrossRefGoogle ScholarPubMed
Vaiserman, AM. Early–life exposure to substance abuse and risk of type 2 diabetes in adulthood. Curr Diabetes Rep. 2015; 15(8), 48.CrossRefGoogle ScholarPubMed
Chodick, G, Flash, S, Deoitch, Y, Shalev, V. Seasonality in birth weight: review of global patterns and potential causes. Hum Biol. 2009; 81(4), 463–477.CrossRefGoogle ScholarPubMed
Day, FR, Forouhi, NG, Ong, KK, Perry, JR. Season of birth is associated with birth weight, pubertal timing, adult body size and educational attainment: a UK Biobank study. Heliyon. 2015; 1(2), e00031.CrossRefGoogle ScholarPubMed
Hemati, Z, Keikha, M, Riahi, R, et al. A systematic review on the association of month and season of birth with future anthropometric measures. Pediatr Res. 2020 [Epub ahead of print].CrossRefGoogle Scholar
Martin, A, Connelly, A, Bland, RM, Reilly, JJ. Health impact of catch–up growth in low–birth weight infants: systematic review, evidence appraisal, and meta–analysis. Matern Child Nutr. 2017a; 13(1). doi: 10.1111/mcn.12297.CrossRefGoogle ScholarPubMed
Kliś, K, Jarzebak, K, Borowska-Strugińska, B, et al. Season of birth influences the timing of first menstruation. Am J Hum Biol. 2016; 28(2), 226–232.CrossRefGoogle ScholarPubMed
Liczbińska, G, Gautam, RK, Dubey, P, Ahirwar, AK, Chaurasia, A, Kosińska, M. Season of birth is not associated with age at menarche in young adults from Central India. Am J Hum Biol. 2020; 32(3), e23373.CrossRefGoogle ScholarPubMed
Si, JH, Meng, RR, Lyu, J, et al. Associations between season of birth and age both at menarche and at menopause. Zhonghua Liu Xing Bing Xue Za Zhi. 2017a; 38(7), 877–882.Google Scholar
Cagnacci, A, Pansini, FS, Bacchi-Modena, A, et al. Season of birth influences the timing of menopause. Hum Reprod. 2005; 20(8), 2190–2193.CrossRefGoogle ScholarPubMed
Vaiserman, AM. Birth weight predicts aging trajectory: a hypothesis. Mech Ageing Dev. 2018; 173, 61–70.CrossRefGoogle ScholarPubMed
Abeliansky, AL, Strulik, H. Season of birth, health and aging. Econ Hum Biol. 2020; 36, 100812.CrossRefGoogle ScholarPubMed
Didikoglu, A, Maharani, A, Payton, A, Pendleton, N, Canal, MM. Longitudinal change of sleep timing: association between chronotype and longevity in older adults. Chronobiol Int. 2019; 36(9), 1285–1300.CrossRefGoogle ScholarPubMed
Didikoglu, A, Canal, MM, Pendleton, N, Payton, A. Seasonality and season of birth effect in the UK Biobank cohort. Am J Hum Biol. 2020; 32(6), e23417.CrossRefGoogle ScholarPubMed
Frisard, M, Ravussin, E. Energy metabolism and oxidative stress: impact on the metabolic syndrome and the aging process. Endocrine. 2006; 29(1), 27–32.CrossRefGoogle ScholarPubMed
Knutson, KL, von Schantz, M. Associations between chronotype, morbidity and mortality in the UK Biobank cohort. Chronobiol Int. 2018; 35(8), 1045–1053.Google ScholarPubMed
Boland, MR, Shahn, Z, Madigan, D, Hripcsak, G, Tatonetti, NP. Birth month affects lifetime disease risk: a phenome–wide method. J Am Med Inf Assoc. 2015; 22(5) 1042–1053.CrossRefGoogle ScholarPubMed
Borsi, JP. Hypothesis–free search for connections between birth month and disease prevalence in large, geographically varied cohorts. AMIA Annu Symp Proc. 2017; 2016, 319–325.Google Scholar
Ringen, PA, Engh, JA, Birkenaes, AB, Dieset, I, Andreassen, OA. Increased mortality in schizophrenia due to cardiovascular disease – a non–systematic review of epidemiology, possible causes, and interventions. Front Psychiatry. 2014; 5, 137.CrossRefGoogle ScholarPubMed
Demler, TL. Challenging the hypothesized link to season of birth in patients with schizophrenia. Innov Clin Neurosci. 2011; 8(9), 14–19.Google ScholarPubMed
Escott-Price, V, Smith, DJ, Kendall, K, et al. Polygenic risk for schizophrenia and season of birth within the UK Biobank cohort. Psychol Med. 2019; 49(15), 2499–2504.CrossRefGoogle ScholarPubMed
Tochigi, M, Okazaki, Y, Kato, N, Sasaki, T. What causes seasonality of birth in schizophrenia? Neurosci Res. 2004; 48(1), 1–11.CrossRefGoogle Scholar
Lee, BK, Gross, R, Francis, RW, et al. Birth seasonality and risk of autism spectrum disorder. Eur J Epidemiol. 2019; 34(8), 785–792.CrossRefGoogle ScholarPubMed
Schnittker, J. Season of birth and depression in adulthood: revisiting historical forerunner evidence for in–utero effects. SSM Popul Health. 2018; 4, 307–316.CrossRefGoogle ScholarPubMed
Procopio, M, Marriott, PK, Williams, P. Season of birth: aetiological implications for epilepsy. Seizure. 1997; 6(2), 99–105.CrossRefGoogle ScholarPubMed
Ghasemi, N, Razavi, S, Nikzad, E. Multiple sclerosis: pathogenesis, symptoms, diagnoses and cell–based therapy. Cell J. 2017; 19(1), 1–10.Google ScholarPubMed
Pantavou, KG, Bagos, PG. Season of birth and multiple sclerosis: a systematic review and multivariate meta–analysis. J Neurol. 2020; 267(10), 2815–2822.CrossRefGoogle ScholarPubMed
Dobson, R, Giovannoni, G, Ramagopalan, S. The month of birth effect in multiple sclerosis: systematic review, meta–analysis and effect of latitude. J Neurol Neurosurg Psychiatry. 2013; 84(4), 427–432.CrossRefGoogle ScholarPubMed
Philpot, M, Rottenstein, M, Burns, A, Der, G. Season of birth in Alzheimer’s disease. Br J Psychiatry. 1989; 155, 662–666.CrossRefGoogle ScholarPubMed
Frazee, J, Russell, M, Chicota, C, et al. Seasonality of birth in Alzheimer’s disease. J Orthomol Med. 2004; 19(3), 162–166.Google Scholar
Vézina, H, Houde, L, Charbonneau, H, et al. Season of birth and Alzheimer’s disease: a population–based study in Saguenay–Lac–St–Jean/Québec (IMAGE Project). Psychol Med. 1996; 26(1), 143–149.CrossRefGoogle Scholar
Ding, R, He, P, Song, X, Zheng, X. Season of birth and dementia: findings from Chinese elderly based on a nationwide data. Am J Hum Biol. 2020; 32(2), e23319.CrossRefGoogle ScholarPubMed
Dysken, MW, Kuskowski, M, Skare, SS, et al. Seasonal distribution of births in Alzheimer’s disease. Int Psychogeriatr. 1991; 3(1), 53–58.CrossRefGoogle ScholarPubMed
Vitiello, B, Hill, JL, Molchan, SE, et al. Lack of seasonal variation in the births of patients with dementia of the Alzheimer type. Psychiatry Res. 1991; 39(1), 21–24.CrossRefGoogle ScholarPubMed
Ptok, U, Papassotiropoulos, A, Maier, W, Heun, R. Seasonal distribution of births in patients with Alzheimer’s disease and elderly depressive patients. Eur Psychiatry. 2001; 16(3), 157–161.CrossRefGoogle ScholarPubMed
Tolppanen, AM, Ahonen, R, Koponen, M, et al. Month and season of birth as a risk factor for Alzheimer’s disease: a nationwide nested case–control study. J Prev Med Public Health. 2016; 49(2), 134–138.CrossRefGoogle ScholarPubMed
Henderson, AS, Korten, AE, Jorm, AF, et al. Season of birth for Alzheimer’s disease in the southern hemisphere. Psychol Med. 1991; 21(2), 371–374.CrossRefGoogle ScholarPubMed
de Lau, LM, Breteler, MM. Epidemiology of Parkinson’s disease. Lancet Neurol. 2006; 5, 525–535.CrossRefGoogle ScholarPubMed
Gardener, H, Gao, X, Chen, H, et al. Prenatal and early life factors and risk of Parkinson’s disease. Mov Disord. 2010; 25(11), 1560–1567.CrossRefGoogle ScholarPubMed
Postuma, RB, Wolfson, C, Rajput, A, et al. Is there seasonal variation in risk of Parkinson’s disease? Mov Disord. 2007; 22(8), 1097–1101.CrossRefGoogle ScholarPubMed
Palladino, R, Moccia, M, De Pascale, T, et al. Season of birth and Parkinson’s disease: possible relationship? Neurol Sci. 2015; 36(8), 1457–1462.CrossRefGoogle ScholarPubMed
Martin, S, Al Khleifat, A, Al-Chalabi, A. What causes amyotrophic lateral sclerosis? F1000Res. 2017b; 6, 371.CrossRefGoogle ScholarPubMed
Ajdacic-Gross, V, Wang, J, Gutzwiller, F. Season of birth in amyotrophic lateral sclerosis. Eur J Epidemiol. 1998; 14(4), 359–361.CrossRefGoogle ScholarPubMed
Fang, F, Valdimarsdóttir, U, Bellocco, R, et al. Amyotrophic lateral sclerosis in Sweden, 1991–2005. Arch Neurol. 2009; 66(4), 515–519.CrossRefGoogle Scholar
Pamphlett, R, Fang, F. Season and weather patterns at time of birth in amyotrophic lateral sclerosis. Amyotroph Lateral Scler. 2012; 13(5), 459–464.CrossRefGoogle ScholarPubMed
Phillips, DI, Young, JB. Birth weight, climate at birth and the risk of obesity in adult life. Int J Obes Relat Metab Disord. 2000; 24, 281–287.CrossRefGoogle ScholarPubMed
Wattie, N, Ardern, CI, Baker, J. Season of birth and prevalence of overweight and obesity in Canada. Early Hum Dev. 2008; 84, 539–547.CrossRefGoogle ScholarPubMed
Laron, Z, Lewy, H, Wilderman, I, et al. Seasonality of month of birth of children and adolescents with type 1 diabetes mellitus in homogenous and heterogeneous populations. Isr Med Assoc J. 2005; 7, 381–384.Google ScholarPubMed
Grover, V, Lipton, RB, Sclove, SL. Seasonality of month of birth among African American children with diabetes mellitus in the city of Chicago. J Pediatr Endocrinol Metab. 2004; 17, 289–296.CrossRefGoogle ScholarPubMed
Jongbloet, PH, van Soestbergen, M, van der Veen, EA. Month–of–birth distribution of diabetics and ovopathy: a new aetiological view. Diabetes Res. 1988; 9, 51–58.Google ScholarPubMed
Vaiserman, AM, Khalangot, MD, Carstensen, B, et al. Seasonality of birth in adult type 2 diabetic patients in three Ukrainian regions. Diabetologia. 2009; 52, 2665–2667.CrossRefGoogle ScholarPubMed
Lumey, LH, Khalangot, MD, Vaiserman, AM. Association between type 2 diabetes and prenatal exposure to the Ukraine famine of 1932–33: a retrospective cohort study. Lancet Diabetes Endocrinol. 2015; 3(10), 787–794.CrossRefGoogle Scholar
Si, J, Yu, C, Guo, Y, et al. Season of birth and the risk of type 2 diabetes in adulthood: a prospective cohort study of 0.5 million Chinese adults. Diabetologia. 2017b; 60(5), 836–842.CrossRefGoogle ScholarPubMed
Jensen, CB, Zimmermann, E, Gamborg, M, et al. No evidence of seasonality of birth in adult type 2 diabetes in Denmark. Diabetologia. 2015; 58(9), 2045–2050.CrossRefGoogle ScholarPubMed
Banegas, JB, Rodríguez-Artalejo, F, de la Cruz, JJ, et al. Adult men born in spring have lower blood pressure. J Hypertens. 2000; 18, 1763–1766.CrossRefGoogle ScholarPubMed
Zhang, BB, Zhao, GA, Yang, M, et al. Birth month associates with risk of coronary artery disease and its complications: a propensity score matched analysis. Med Clin (Barc). 2019a; 153(12), 454–459.CrossRefGoogle ScholarPubMed
Li, L, Boland, MR, Miotto, R, Tatonetti, NP, Dudley, JT. Replicating cardiovascular condition–birth month associations. Sci Rep. 2016; 6, 33166.CrossRefGoogle ScholarPubMed
Poltavskiy, E, Spence, JD, Kim, J, Bang, H. Birth month and cardiovascular disease risk association: is meaningfulness in the eye of the beholder? Online J Public Health Inform. 2016; 8(2), e186.CrossRefGoogle ScholarPubMed
Lawlor, DA, Davey Smith, G, Mitchell, R, Ebrahim, S. Temperature at birth, coronary heart disease, and insulin resistance: cross sectional analyses of the British women’s heart and health study. Heart. 2004; 90, 381–388.CrossRefGoogle ScholarPubMed
Basta, NO, James, PW, Craft, AW, McNally, RJ. Season of birth and diagnosis for childhood cancer in Northern England, 1968–2005. Paediatr Perinat Epidemiol. 2010; 24(3), 309–318.CrossRefGoogle Scholar
van Laar, M, Kinsey, SE, Picton, SV, Feltbower, RG. First description of seasonality of birth and diagnosis amongst teenagers and young adults with cancer aged 15–24 years in England, 1996–2005. BMC Cancer. 2013; 13, 365.CrossRefGoogle Scholar
Higgins, CD, dos-Santos-Silva, I, Stiller, CA, Swerdlow, AJ. Season of birth and diagnosis of children with leukaemia: an analysis of over 15 000 UK cases occurring from 1953–1995. Br J Cancer. 2001; 84(3), 406–412.CrossRefGoogle Scholar
Crump, C, Sundquist, J, Sieh, W, Winkleby, MA, Sundquist, K. Season of birth and risk of Hodgkin and non–Hodgkin lymphoma. Int J Cancer. 2014; 135(11), 2735–2739.CrossRefGoogle ScholarPubMed
Georgakis, MK, Ntinopoulou, E, Chatzopoulou, D, Petridou, ET. Season of birth and primary central nervous system tumors: a systematic review of the literature with critical appraisal of underlying mechanisms. Ann Epidemiol. 2017; 27(9), 593–602.CrossRefGoogle ScholarPubMed
La Rosa, F, Liso, A, Bianconi, F, Duca, E, Stracci, F. Seasonal variation in the month of birth in patients with skin cancer. Br J Cancer. 2014; 111(9), 1810–1813.CrossRefGoogle ScholarPubMed
Francis, NK, Curtis, NJ, Noble, E, Cortina-Borja, M, Salib, E. Is month of birth a risk factor for colorectal cancer? Gastroenterol Res Pract. 2017; 2017, 1–5.CrossRefGoogle ScholarPubMed
Hao, Y, Yan, L, Ke, E, Wang, H, He, J. Birth in winter can reduce the risk of lung cancer: a retrospective study of the birth season of patients with lung cancer in Beijing area, China. Chronobiol Int. 2017; 34(4), 511–518.CrossRefGoogle ScholarPubMed
Yuen, J, Ekbom, A, Trichopoulos, D, Hsieh, CC, Adami, HO. Season of birth and breast cancer risk in Sweden. Br J Cancer. 1994; 70(3), 564–568.CrossRefGoogle ScholarPubMed
Doblhammer, G, Vaupel, JW. Lifespan depends on month of birth. Proc Natl Acad Sci U S A. 2001; 98(5), 2934–2939.CrossRefGoogle ScholarPubMed
Doblhammer, G. Differences in lifespan by month of birth for the United States: the impact of early life events and conditions on late life mortality. MPIDR Working Paper 2002–19. 2002.CrossRefGoogle Scholar
Zhang, Y, Devore, EE, Strohmaier, S, Grodstein, F, Schernhammer, ES. Birth month, birth season, and overall and cardiovascular disease mortality in US women: prospective cohort study. BMJ. 2019b; 367, l6058.CrossRefGoogle ScholarPubMed
Sohn, K. The influence of birth season on mortality in the United States. Am J Hum Biol. 2016; 28(5), 662–670.CrossRefGoogle ScholarPubMed
Gavrilov, LA, Gavrilova, NS. Season of birth and human longevity. J Anti–Aging Med. 1999; 2(4), 365–366.CrossRefGoogle Scholar
Gagnon, A. Effect of birth season on longevity: thrifty and hopeful phenotypes in historical Quebec. Am J Hum Biol. 2012; 24(5), 654–660.CrossRefGoogle ScholarPubMed
Muñoz-Tudurí, M, García-Moro, C. Season of birth affects short– and long–term survival. Am J Phys Anthropol. 2008; 135(4), 462–468.CrossRefGoogle ScholarPubMed
Flouris, AD, Spiropoulos, Y, Sakellariou, GJ, Koutedakis, Y. Effect of seasonal programming on fetal development and longevity: links with environmental temperature. Am J Hum Biol. 2009; 21(2), 214–216.CrossRefGoogle ScholarPubMed
Vaiserman, AM, Collinson, AC, Koshel, NM, Belaja, II, Voitenko, VP. Seasonal programming of adult longevity in Ukraine. Int J Biometeorol. 2002; 47(1), 49–52.Google ScholarPubMed
Ueda, P, Edstedt Bonamy, AK, Granath, F, Cnattingius, S. Month of birth and mortality in Sweden: a nation–wide population–based cohort study. PLoS One. 2013; 8(2), e56425.CrossRefGoogle ScholarPubMed
Ueda, P, Edstedt Bonamy, AK, Granath, F, Cnattingius, S. Month of birth and cause–specific mortality between 50 and 80 years: a population–based longitudinal cohort study in Sweden. Eur J Epidemiol. 2014; 29(2), 89–94.CrossRefGoogle ScholarPubMed
Lerchl, A. Month of birth and life expectancy: role of gender and age in a comparative approach. Naturwissenschaften. 2004; 91(9), 422–425.CrossRefGoogle Scholar
Inoue, Y, Stickley, A, Yazawa, A, et al. Month of birth is associated with mortality among older people in Japan: findings from the JAGES cohort. Chronobiol Int. 2016; 33(4), 441–447.CrossRefGoogle ScholarPubMed
Moore, S, Cole, T, Poskitt, E, et al. Season of birth predicts mortality in rural Gambia. Nature. 1997; 388, 434.CrossRefGoogle ScholarPubMed
Moore, SE, Cole, TJ, Collinson, AC, et al. Prenatal or early postnatal events predict infectious deaths in young adulthood in rural Africa. Int J Epidemiol. 1999; 28, 1088–1095.CrossRefGoogle ScholarPubMed
Moore, SE, Fulford, AJ, Streatfield, PK, Persson, LA, Prentice, AM. Comparative analysis of patterns of survival by season of birth in rural Bangladeshi and Gambian populations. Int J Epidemiol. 2004; 33, 137–143.CrossRefGoogle ScholarPubMed
Simondon, KB, Elguero, E, Marra, A, et al. Season of birth is not associated with risk of early adult death in rural Senegal. Int J Epidemiol. 2004; 33(1), 130–136.CrossRefGoogle Scholar
Gavrilov, LA, Gavrilova, NS. Season of birth and exceptional longevity: comparative study of American centenarians, their siblings, and spouses. J Aging Res. 2011; 2011(2), 1–11.CrossRefGoogle ScholarPubMed
Gavrilov, LA, Gavrilova, NS. Predictors of exceptional longevity: effects of early–life childhood conditions, midlife environment and parental characteristics. Living 100 Monogr. 2014; 2014, 1–18.Google ScholarPubMed
Doblhammer, G, Scholz, R, Maier, H. Month of birth and survival to age 105+: evidence from the age validation study of German semi–supercentenarians. Exp Gerontol. 2005; 40(10), 829–835.CrossRefGoogle ScholarPubMed
Rojansky, N, Brzezinski, A, Schenker, JG. Seasonality in human reproduction: an update. Hum Reprod. 1992; 7(6), 735–745.CrossRefGoogle ScholarPubMed
Jongbloet, PH, Groenewoud, HM, Huber, S, Fieder, M, Roeleveld, N. Month of birth related to fecundity and childlessness among contemporary women. Hum Biol. 2007; 79(5), 479–490.Google ScholarPubMed
Zhu, Z, Cao, F, Li, X. Epigenetic programming and fetal metabolic programming. Front Endocrinol (Lausanne). 2019; 10, 764.CrossRefGoogle ScholarPubMed
Kim, JB. Dynamic cross talk between metabolic organs in obesity and metabolic diseases. Exp Mol Med. 2016; 48(3), e214.CrossRefGoogle ScholarPubMed
Zeltser, LM. Feeding circuit development and early–life influences on future feeding behaviour. Nat Rev Neurosci. 2018; 19(5), 302–316.CrossRefGoogle ScholarPubMed
Spencer, SJ, Galic, MA, Pittman, QJ. Neonatal programming of innate immune function. Am J Physiol Endocrinol Metab. 2011; 300(1), E11–E18.CrossRefGoogle ScholarPubMed
Rajendran, P, Chen, YF, Chen, YF, et al. The multifaceted link between inflammation and human diseases. J Cell Physiol. 2018; 233(9), 6458–6471.CrossRefGoogle ScholarPubMed
Fisman, D. Seasonality of viral infections: mechanisms and unknowns. Clin Microbiol Infect. 2012; 18(10), 946–954.CrossRefGoogle ScholarPubMed
Vandenplas, Y, Carnielli, VP, Ksiazyk, J, et al. Factors affecting early–life intestinal microbiota development. Nutrition. 2020; 78, 110812.CrossRefGoogle ScholarPubMed
Koleva, PT, Kim, JS, Scott, JA, Kozyrskyj, AL. Microbial programming of health and disease starts during fetal life. Birth Defects Res C Embryo Today. 2015; 105, 265−277.Google Scholar
Codagnone, MG, Spichak, S, O’Mahony, SM, et al. Programming bugs: microbiota and the developmental origins of brain health and disease. Biol Psychiatry. 2019; 85(2), 150–163.CrossRefGoogle ScholarPubMed
Stinson, LF. Establishment of the early–life microbiome: a DOHaD perspective. J Dev Orig Health Dis. 2020; 11(3), 201–210.CrossRefGoogle ScholarPubMed
Butel, MJ, Waligora-Dupriet, AJ, Wydau-Dematteis, S. The developing gut microbiota and its consequences for health. J Dev Orig Health Dis. 2018; 22, 1–8.Google Scholar
Dahl, WJ, Rivero Mendoza, D, , Lambert JM. Diet, nutrients and the microbiome. Prog Mol Biol Transl Sci. 2020; 171, 237–263.Google Scholar
Karl, JP, Hatch, AM, Arcidiacono, SM, et al. Effects of psychological, environmental and physical stressors on the gut microbiota. Front Microbiol. 2018; 9, 2013.CrossRefGoogle ScholarPubMed
McGrath, J. Does ‘imprinting’ with low prenatal vitamin D contribute to the risk of various adult disorders? Med Hypotheses. 2001; 56(3), 367–371.CrossRefGoogle Scholar
Flandroy, L, Poutahidis, T, Berg, G, et al. The impact of human activities and lifestyles on the interlinked microbiota and health of humans and of ecosystems. Sci Total Environ. 2018; 627, 1018–1038.CrossRefGoogle ScholarPubMed
Smits, SA, Leach, J, Sonnenburg, ED, et al. Seasonal cycling in the gut microbiome of the Hadza hunter–gatherers of Tanzania. Science. 2017; 357(6353), 802–806.CrossRefGoogle ScholarPubMed
Davenport, ER, Mizrahi-Man, O, Michelini, K, et al. Seasonal variation in human gut microbiome composition. PLoS One. 2014; 9(3), e90731.CrossRefGoogle ScholarPubMed
Korownyk, C, Liu, F, Garrison, S. Population level evidence for seasonality of the human microbiome. Chronobiol Int. 2018; 35(4), 573–577.CrossRefGoogle ScholarPubMed
Zhang, J, Guo, Z, Lim, AA, et al. Mongolians core gut microbiota and its correlation with seasonal dietary changes. Sci Rep. 2014; 4, 5001.CrossRefGoogle ScholarPubMed
Koliada, A, Moseiko, V, Romanenko, M, et al. Seasonal variation in gut microbiota composition: cross–sectional evidence from Ukrainian population. BMC Microbiol. 2020; 20(1), 100.CrossRefGoogle ScholarPubMed
Safi-Stibler, S, Gabory, A. Epigenetics and the developmental origins of health and disease: parental environment signalling to the epigenome, critical time windows and sculpting the adult phenotype. Semin Cell Dev Biol. 2020; 97, 172–180.CrossRefGoogle Scholar
Lockett, GA, Soto-Ramírez, N, Ray, MA, et al. Association of season of birth with DNA methylation and allergic disease. Allergy. 2016a; 71(9), 1314–1324.CrossRefGoogle ScholarPubMed
Dugué, PA, Geurts, YM, Milne, RL. Is there an association between season of birth and blood DNA methylation in adulthood? Allergy. 2016; 71, 1501–1502.CrossRefGoogle ScholarPubMed
Lockett, GA, Zhang, H, Karmaus, W, Holloway, JW. Epigenetic association with season of birth: a complex relationship. Allergy. 2016b; 71, 1503–1504.CrossRefGoogle Scholar
Hales, CN, Barker, DJ. The thrifty phenotype hypothesis. Br Med Bull. 2001; 60:5–20.CrossRefGoogle ScholarPubMed
Crawford, C, Dearden, L, Greaves, E. The drivers of month-of-birth differences in children’s cognitive and non-cognitive skills. J R Stat Soc Ser A Stat Soc. 2014;177(4), 829–860.CrossRefGoogle ScholarPubMed
Doebler, S., Shuttleworth, I., Gould, M. Does the month of birth affect educational and health outcomes? A population-based analysis using the Northern Ireland longitudinal study. Econ Soc Rev. 2017; 48, 281–304.Google Scholar
Solli, IF. Left behind by birth month. Educ Econ. 2017; 25(4), 323–346.CrossRefGoogle Scholar
Verachtert, P, De Fraine, B, Onghena, P, Ghesquière, P. Season of birth and school success in the early years of primary education. Oxford Rev Educ. 2010; 36 (3), 285–306.CrossRefGoogle Scholar
Xavier, MJ, Roman, SD, Aitken, RJ, Nixon, B. Transgenerational inheritance: how impacts to the epigenetic and genetic information of parents affect offspring health. Hum Reprod Update. 2019; 25(5), 518–540.CrossRefGoogle Scholar
King, SE, Skinner, MK. Epigenetic transgenerational inheritance of obesity susceptibility. Trends Endocrinol Metab. 2020; 31(7), 478–494.CrossRefGoogle ScholarPubMed
Vaiserman, AM, Koliada, AK, Jirtle, RL. Non–genomic transmission of longevity between generations: potential mechanisms and evidence across species. Epigenetics Chromatin. 2017; 10(1), 38.CrossRefGoogle ScholarPubMed