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Lingering prenatal effects of the 1918 influenza pandemic on cardiovascular disease

Published online by Cambridge University Press:  01 October 2009

B. Mazumder
Affiliation:
Federal Reserve Bank of Chicago, Chicago, IL, USA
D. Almond
Affiliation:
Department of Economics and SIPA, Columbia University, New York, NY, USA
K. Park
Affiliation:
Harris School of Public Policy, University of Chicago, Chicago, IL, USA
E. M. Crimmins
Affiliation:
Andrus Gerontology Center, University of Southern California, Los Angeles, CA, USA
C. E. Finch*
Affiliation:
Andrus Gerontology Center, University of Southern California, Los Angeles, CA, USA
*
Address for correspondence: C. E. Finch, Andrus Gerontology Center, University of Southern California, 3715 McClintock Avenue, Los Angeles, CA 90089, USA. (Email cefinch@usc.edu)

Abstract

Prenatal exposure to the 1918 influenza pandemic (Influenza A, H1N1 subtype) is associated with ⩾20% excess cardiovascular disease at 60 to 82 years of age, relative to cohorts born without exposure to the influenza epidemic, either prenatally or postnatally (defined by the quarter of birth), in the 1982–1996 National Health Interview Surveys of the USA. Males showed stronger effects of influenza on increased later heart disease than females. Adult height at World War II enlistment was lower for the 1919 birth cohort than for those born in adjacent years, suggesting growth retardation. Calculations on the prevalence of maternal infections indicate that prenatal exposure to even uncomplicated maternal influenza may have lasting consequences later in life. These findings suggest novel roles for maternal infections in the fetal programming of cardiovascular risk factors that are independent of maternal malnutrition.

Type
Original Article
Copyright
Copyright © Cambridge University Press and the International Society for Developmental Origins of Health and Disease 2009

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References

1.Morens, DM, Taubenberger, JK, Fauci, AS. Predominant role of bacterial pneumonia as a cause of death in pandemic influenza: implications for pandemic influenza preparedness. J Infect Dis. 2008; 198, 962970.CrossRefGoogle ScholarPubMed
2.Brundage, JF, Shanks, GD. Deaths from bacterial pneumonia during 1918–19 influenza pandemic. Emerg Infect Dis. 2008; 4, 11931199.CrossRefGoogle Scholar
3.Morens, DM, Taubenberger, JK, Fauci, AS. Persistent legacy of the 1918 influenza virus. N Engl J Med. 2009; 361, 225229.Google Scholar
4.Almond, D. Is the 1918 Influenza pandemic over? Long-term effects of in utero influenza exposure in the post-1940 US population. J Polit Econ. 2006; 114, 672712.Google Scholar
5.Brown, AS, Begg, MD, Gravenstein, S, et al. Serologic evidence of prenatal influenza in the etiology of schizophrenia. Arch Gen Psychiatry. 2004; 61, 774780.CrossRefGoogle ScholarPubMed
6.Patterson, PH. Immune involvement in schizophrenia and autism: etiology, pathology and animal models. Behav Brain Res. 2009; 313321.CrossRefGoogle ScholarPubMed
7.Fatemi, SH, Earle, J, Kanodia, R, et al. Prenatal viral infection leads to pyramidal cell atrophy and macrocephaly in adulthood: implications for genesis of autism and schizophrenia. Cell Mol Neurobiol. 2002; 22, 2533.CrossRefGoogle ScholarPubMed
8.Barker, DJ. The origins of the developmental origins theory. J Intern Med. 2007; 261, 412417.Google Scholar
9.Gluckman, PD, Hanson, MA, Beedle, AS, Raubenheimer, D. Fetal and neonatal pathways to obesity. Front Horm Res. 2008; 36, 6172.CrossRefGoogle ScholarPubMed
10.Lynch, J, Davey Smith, G. A life course approach to chronic disease epidemiology. Annu Rev Public Health. 2005; 26, 135.CrossRefGoogle ScholarPubMed
11.Finch, CE. The Biology of Human Longevity: Inflammation, Nutrition, and Aging in the Evolution of Lifespans, 2007. Academic Press, San Diego.Google Scholar
12.Hampton, T. Virulence of 1918 influenza virus linked to inflammatory innate immune response. JAMA. 2007; 297, 580.Google ScholarPubMed
13.Heltzer, ML, Coffin, SE, Maurer, K, et al. Immune dysregulation in severe influenza. J Leukoc Biol. 2009; 85, 10361043.CrossRefGoogle ScholarPubMed
14.Samuelsson, AM, Ohrn, I, Dahlgren, J, et al. Prenatal exposure to interleukin-6 results in hypertension and increased hypothalmic-pituitary-adrenal axis activity in adult rats. Endocrinology. 2004; 145, 48974911.CrossRefGoogle Scholar
15.Smith, SE, Li, J, Garbett, K, Mirnics, K, Patterson, PH. Maternal immune activation alters fetal brain development through interleukin-6. J Neurosci. 2007; 27, 1069510702.CrossRefGoogle ScholarPubMed
16.Gayle, DA, Beloosesky, R, Desai, M, Amidi, F, Nuñez, SE, Ross, MG. Maternal LPS induces cytokines in the amniotic fluid and corticotropin releasing hormone in the fetal rat brain. Am J Physiol Regul Integr Comp Physiol. 2004; 286, R1024R1029.CrossRefGoogle ScholarPubMed
17.Ortiz, LA, Quan, A, Zarzar, F, Weinberg, A, Baum, M. Prenatal dexamethasone programs hypertension and renal injury in rat. Hypertension. 2003; 41, 328334.CrossRefGoogle Scholar
18.Doblhammer, G, Vaupel, JW. Lifespan depends on month of birth. Proc Natl Acad Sci USA. 2001; 98, 29342939.Google Scholar
19.McEniry, M, Palloni, A, Dávila, AL, Gurucharri, AG. Early life exposure to poor nutrition and infectious diseases and its effects on the health of older Puerto Rican adults. J Gerontol B Psychol Sci Soc Sci. 2008; 63, S337S348.Google Scholar
20.Crimmins, EM, Finch, CE. Infection, inflammation, height, and longevity. Proc Natl Acad Sci USA. 2006; 103, 498503.CrossRefGoogle ScholarPubMed
21.Harris, JW. Influenza occurring in pregnant women: a statistical study of thirteen hundred and fifty cases. JAMA. 1919; 72, 978980.CrossRefGoogle Scholar
22.Titus, P, Jamison, JM. Pregnancy complicated by epidemic influenza. JAMA. 1919; 72, 16651668.Google Scholar
23.Freeman, DW, Barno, A. Deaths from Asian influenza associated with pregnancy. Am J Obstet Gynecol. 1959; 78, 11721175.Google Scholar
24.Linder, FE, Grove, RD. Vital Statistics Rates in the United States, 1900–1940, 1947. United State Public Health Service, National Office of Vital Statistics. Washington, Retrieved from http://www.nber.org/vital-stats-books/vsrates1900_40.CV.pdfGoogle Scholar
25.Almond, D, Mazumder, B. The 1918 influenza pandemic and subsequent health outcomes: an analysis of SIPP data. Am Econ Rev. 2005; 95, 258262.CrossRefGoogle ScholarPubMed
26.Bergmann, MM, Byers, T, Freedman, DS, Mokdad, A. Validity of self-reported diagnoses leading to hospitalization: a comparison of self-reports with hospital records in a prospective study of American adults. Am J Epidemiol. 1998; 147, 969977.CrossRefGoogle Scholar
27.Colditz, GA, Martin, P, Stampfer, MJ, et al. Validation of questionnaire information on risk factors and disease outcomes in a prospective cohort study of women. Am J Epidemiol. 1986; 123, 894900.CrossRefGoogle Scholar
28.Engstad, T, Bønaa, KH, Viitanen, M. Validity of self-reported stroke. The Tromso Study. Stroke 2000; 31, 16021607.Google Scholar
29.Kehoe, R, Wu, S-Y, Leske, MC, Chylack, LT Jr. Comparing self-reported and physician-reported medical history. Am J Epidemiol. 1994; 139, 813818.CrossRefGoogle ScholarPubMed
30.Edwards, WS, Winn, DM, Kurlantzick, V, et al. Evaluation of National Health Interview Survey diagnostic reporting. Hyattsville, Maryland: US Department of Health and Human Services, Public Health Service, CDC, National Center for Health Statistics. Vital and Health Statistics, 1994; vol. 2, No. 120, 2(12).Google Scholar
31.Luk, J, Gross, P, Thomson, WW. Observations on mortality during the 1918 influenza pandemic. Clin Infect Dis. 2001; 33, 13751378.CrossRefGoogle ScholarPubMed
32.Rastogi, D, Wang, C, Mao, X, Lendor, C, Rothman, PB, Miller, RL. Antigen-specific immune responses to influenza vaccine in utero. J Clin Invest. 2007; 117, 16371646.CrossRefGoogle ScholarPubMed
33.Drevenstedt, GL, Crimmins, EM, Vasunilashorn, S, Finch, CE. The rise and fall of excess male infant morality. Proc Natl Acad Sci USA. 2008; 105, 50165021.CrossRefGoogle Scholar
34.Ramsey, PS, Ramin, KD. Pneumonia in pregnancy. Obstet Gyneco Clin North Am. 2001; 28, 553569.Google Scholar
35.Goodnight, WH, Soper, DE. Pneumonia in pregnancy. Crit Care Med. 2005; 33, S390S397.CrossRefGoogle ScholarPubMed
36.Ács, N, Bánhidy, F, Puhó, E, Czeizel, AE. Pregnancy complications and delivery outcomes of pregnant women with influenza. J Matern Fetal Neonatal Med. 2006; 19, 135140.CrossRefGoogle ScholarPubMed
37.Svare, JA, Schmidt, H, Hansen, BB, Lose, G. Bacterial vaginosis in a cohort of Danish pregnant women: prevalence and relationship with preterm delivery, low birthweight and perinatal infection. BJOG. 2006; 113, 14191425.CrossRefGoogle Scholar
38.Stein, Z, Susser, M, Saenger, G, Marolla, F. Famine and Human Development. The Dutch Hunger Winter of 1944–1945, 1975. Oxford University Press.Google Scholar
39.Painter, RC, de Rooij, SR, Bossuyt, PM, et al. Early onset of coronary artery disease after prenatal exposure to the Dutch famine. Am J Clin Nutr. 2006; 84, 322327.Google Scholar
40.Hoek, HW, Brown, AS, Susser, E. The Dutch famine and schizophrenia spectrum disorders. Soc Psychiatry Psychiatr Epidemiol. 1998; 33, 373379.Google Scholar
41.de Rooij, SR, Painter, RC, Roseboom, TJ, et al. Glucose tolerance at age 58 and the decline of glucose tolerance in comparison with age 50 in people prenatally exposed to the Dutch famine. Diabetologia. 2006; 49, 637643.CrossRefGoogle Scholar
42.Heijmans, BT, Tobi, EW, Stein, AD, et al. Persistent epigenetic differences associated with prenatal exposure to famine in humans. Proc Natl Acad Sci USA. 2008; 105, 1704617049.Google Scholar
43.Gluckman, PD, Hanson, MA, Buklijas, T, Low, FM, Beedle, AS. Epigenetic mechanisms that underpin metabolic and cardiovascular diseases. Natl Rev Endocrinol. 2009; 5, 401408.CrossRefGoogle ScholarPubMed
44.Burger, GCE, Drummond, JC, Sandstead, HR. Malnutrition and starvation in Western Netherlands, 1948. General State Publishing Office, The Hague.Google Scholar
45.Hemmes, GD. Besmettelijke Ziekten. Epidemiologie en praeventieve maaatregelen. In Medische Ervaringen in Nederland Tijdens de Bezetting 1940–1945 (ed. Boerma I), 1945; pp. 105129. JB Wolters, Gronningen. Translated for C.E.F. by Paulus van Noord; see ref 11, p. 285.Google Scholar
46.Bobetsis, YA, Barros, SP, Lin, DM, et al. Bacterial infection promotes DNA hypermethylation. J Dent Res. 2007; 86, 169174.CrossRefGoogle ScholarPubMed
47.Yamashita, T, Freigang, S, Eberle, C, et al. Maternal immunization programs postnatal immune responses and reduces atherosclerosis in offspring. Circ Res. 2006; 99, E51E64.Google Scholar
48.Fatemi, SH, Earle, J, Kanodia, R, et al. Prenatal viral infection leads to pyramidal cell atrophy and macrocephaly in adulthood: implications for genesis of autism and schizophrenia. Cell Mol Neurobiol. 2002; 22, 2533.Google Scholar
49.Shi, L, Tu, N, Patterson, PH. Maternal influenza infection is likely to alter fetal brain development indirectly: the virus is not detected in the fetus. Int J Dev Neurosci. 2005; 23, 299305.CrossRefGoogle Scholar
50.Shi, L, Smith, SE, Malkova, N, Tse, D, Su, Y, Patterson, PH. Activation of the maternal immune system alters cerebellar development in the offspring. Brain Behav Immun. 2009; 23, 116123.CrossRefGoogle ScholarPubMed
51.Napoli, C, D’Armiento, FP, Mancini, FP, et al. Fatty streak formation occurs in human fetal aortas and is greatly enhanced by maternal hypercholesterolemia. Intimal accumulation of low density lipoprotein and its oxidation precede monocyte recruitment into early artherosclerotic lesions. J Clin Invest. 1997; 100, 26802690.CrossRefGoogle Scholar
52.Franceschi, C, Capri, M, Monti, D, et al. Inflammaging and anti-inflammaging: a systemic perspective on aging and longevity emerged from studies in humans. Mech Ageing Dev. 2007; 128, 92105.Google Scholar
53.Ward, JR, Wilson, HL, Francis, SE, Crossman, DC, Sabroe, I. Translational mini-review series on immunology of vascular disease: inflammation, infections and Toll-like receptors in cardiovascular disease. Clin Exp Immunol. 2009; 156, 386394.CrossRefGoogle ScholarPubMed
54.Fatemi, SH, Folsom, TD, Reutiman, TJ, Huang, H, Oishi, K, Mori, S. Prenatal viral infection of mice at E16 causes changes in gene expression in hippocampi of the offspring. Eur Neuropsychopharmacol. 2009; 19, 648653.Google Scholar