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Prenatal and Early-Life Exposure to the Great Chinese Famine Increased the Risk of Tuberculosis in Adulthood Across Two Generations

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Prenatal and Early-Life Exposure to the Great Chinese Famine Increased the Risk of Tuberculosis in Adulthood Across Two Generations Prenatal and early-life exposure to the Great Chinese Famine increased the risk of tuberculosis in adulthood across two generations Qu Chenga, Robert Tranguccib, Kristin N. Nelsonc, Wenjiang Fud, Philip A. Collendera, Jennifer R. Heade, Christopher M. Hoovera, Nicholas K. Skaffa, Ting Lif, Xintong Lig, Yue Youh, Liqun Fangi, Song Liangj, Changhong Yangk, Jin’ge Hef, Jonathan L. Zelnerl,m, and Justin V. Remaisa,1 aDivision of Environmental Health Sciences, School of Public Health, University of California, Berkeley, CA 94720; bDepartment of Statistics, University of Michigan, Ann Arbor, MI 48109; cRollins School of Public Health, Emory University, Atlanta, GA 30322; dDepartment of Mathematics, University of Houston, Houston, TX 77204; eDivision of Epidemiology, School of Public Health, University of California, Berkeley, CA 94720; fInstitute of Tuberculosis Control and Prevention, Sichuan Center for Disease Control and Prevention, 610041 Chengdu, China; gDepartment of Biostatistics, Rollins School of Public Health, Emory University, Atlanta, GA 30322; hDivision of Biostatistics, School of Public Health, University of California, Berkeley, CA 94720; iDepartment of Infectious Disease Epidemiology, Institute of Microbiology and Epidemiology, 100850 Beijing, China; jDepartment of Environmental and Global Health, College of Public Health and Health Professions, University of Florida, Gainesville, FL 32611; kInstitute of Health Informatics, Sichuan Center for Disease Control and Prevention, 610041 Chengdu, China; lDepartment of Epidemiology, University of Michigan, Ann Arbor, MI 48109; and mCenter for Social Epidemiology and Population Health, School of Public Health, University of Michigan, Ann Arbor, MI 48109 Edited by Trudi Schüpbach, Princeton University, Princeton, NJ, and approved September 7, 2020 (received for review May 16, 2020) Global food security is a major driver of population health, and single infectious agent in 2016 (15, 16). According to China’s food system collapse may have complex and long-lasting effects web-based National Infectious Disease Reporting System on health outcomes. We examined the effect of prenatal exposure (NIDRS) that collects case-level data on 40 notifiable infectious – — to the Great Chinese Famine (1958 1962) the largest famine in diseases from almost all healthcare facilities in the country (17), — human history on pulmonary tuberculosis (PTB) across consecu- pulmonary tuberculosis (PTB) contributed the fourth highest tive generations in a major center of ongoing transmission in number of incident cases in 2018 (823,342 out of 7,770,749 cases, China. We analyzed >1 million PTB cases diagnosed between MEDICAL SCIENCES 2005 and 2018 in Sichuan Province using age–period–cohort anal- 10.6%) and the second highest number of deaths (3,149 out of ysis and mixed-effects metaregression to estimate the effect of 23,377 deaths, 13.5%) (18). In the short term, exposure to the famine on PTB risk in the directly affected birth cohort (F1) famine is associated with an increased likelihood of latent PTB and their likely offspring (F2). The analysis was repeated on certain progressing to active disease, an increased probability of com- sexually transmitted and blood-borne infections (STBBI) to explore plications and deaths in active cases, and a reduced immune potential mechanisms of the intergenerational effects. A substan- response following bacille Calmette–Guérin (bacillus Calmette– tial burden of active PTB in the exposed F1 cohort and their off- Guérin) vaccination (10). However, the long-term impacts of spring was attributable to the Great Chinese Famine, with more famine on the burden of PTB at a population level is poorly ENVIRONMENTAL SCIENCES > than 12,000 famine-attributable active PTB cases ( 1.23% of all understood. cases reported between 2005 and 2018). An interquartile range increase in famine intensity resulted in a 6.53% (95% confidence interval [CI]: 1.19–12.14%) increase in the ratio of observed to Significance expected incidence rate (incidence rate ratio, IRR) in the absence of famine in F1, and an 8.32% (95% CI: 0.59–16.6%) increase in F2 Food system collapse incurs major societal costs that may ex- IRR. Increased risk of STBBI was also observed in F2. Prenatal and tend across generations. The Great Chinese Famine—widely early-life exposure to malnutrition may increase the risk of active acknowledged as the largest famine in human history—was PTB in the exposed generation and their offspring, with the inter- associated with tremendous short-term adverse health conse- generational effect potentially due to both within-household quences, yet its long-term effect on infectious disease inci- transmission and increases in host susceptibility. dence has not been estimated. We conducted a cohort analysis of >1 million pulmonary tuberculosis (PTB) cases in a major food systems | tuberculosis | Great Chinese Famine | infectious disease | center of ongoing transmission that experienced high famine nutrition mortality, finding a substantial burden of active PTB potentially attributable to the famine in the birth cohort that experienced he impact of prenatal exposure to famine on the risk of prenatal and early-life exposure to famine, as well in their Tchronic conditions—including hypertension, coronary heart putative offspring. The Great Chinese Famine occurred >60 y disease, type 2 diabetes, metabolic syndrome, and schizophrenia—in ago, yet continues to contribute to the high PTB burden adulthood has been widely studied (1–5). Higher risks of in China. chronic diseases have also been identified among the children of individuals from famine birth cohorts (6–8). While there is Author contributions: Q.C., K.N.N., P.A.C., J.R.H., C.M.H., N.K.S., X.L., L.F., J.L.Z., and J.V.R. designed research; Q.C. and R.T. performed research; R.T., W.F., and J.L.Z. contributed an extensive literature on short-term effects of prenatal expo- new reagents/analytic tools; Q.C., W.F., P.A.C., T.L., and Y.Y. analyzed data; and Q.C., R.T., sure to famine and malnutrition on infectious diseases (9, 10), K.N.N., P.A.C., J.R.H., C.M.H., N.K.S., T.L., X.L., Y.Y., L.F., S.L., C.Y., J.H., J.L.Z., and J.V.R. research on long-term and intergenerational effects is limited wrote the paper. (11–13). The authors declare no competing interest. Tuberculosis (TB) is a primarily airborne bacterial infection This article is a PNAS Direct Submission. caused by the pathogen Mycobacterium tuberculosis. After in- Published under the PNAS license. fection, the latent period can range from months to years, with a 1To whom correspondence may be addressed. Email: [email protected]. relatively small proportion (∼5–10%) of infected individuals This article contains supporting information online at https://www.pnas.org/lookup/suppl/ progressing to active disease (14). Worldwide, TB caused 1.6 doi:10.1073/pnas.2008336117/-/DCSupplemental. million deaths in 2017 and was the leading cause of death from a www.pnas.org/cgi/doi/10.1073/pnas.2008336117 PNAS Latest Articles | 1of7 Downloaded by guest on September 27, 2021 The Great Chinese Famine of 1959–1961 is widely considered intensity at the prefecture level, and the analysis was repeated on the largest famine in human history in terms of total lives lost certain sexually transmitted and blood-borne infections (STBBI) (19). An estimated 30 million people died from starvation, and to explore potential mechanisms of the intergenerational effects. an estimated 33 million births were lost or postponed (19). Rural Assuming a low probability of sexual and/or blood contact be- residents were affected more severely because of shortages in tween the F1 and F2 generations, the existence of intergenera- grain supplies following their fulfillment of compulsory grain tional effects for STBBI would suggest an important role of procurement quotas, while urban residents’ food supplies were increased host susceptibility, whereas the absence of these effects secured by legal and other protections (20). This urban bias in would suggest increased contact with high-risk parents among the food distribution system, combined with provincial differ- the F2 generation as a dominant mechanism. ences in the rural and urban population shares, led to substantial spatial heterogeneity in famine severity across China (21, 22). Results The province of Sichuan is located in southwest China and has The severity of famine—expressed as cohort size shrinkage index a population of more than 80 million people. Sichuan remains a (CSSI; see details in Materials and Methods)—varied widely – high PTB-transmission area within China (23), with an esti- across regions in the study area (Fig. 1A). Yaan, Meishan, and mated prevalence rate of active PTB of 598 cases per 100,000 – Leshan prefectures in central Sichuan exhibited the highest persons (95% confidence interval [CI]: 480 717), substantially famine intensity; these areas had high rural populations and higher than the national average of 442 (95% CI: 417–469) cases experienced high compulsory grain procurement during the per 100,000 persons, according to a cross-sectional survey con- famine period (21, 35). The prefectural CSSIs estimated for only ducted in 2010 (24). Furthermore, Sichuan had the highest total male, only female, and the whole population were highly con- fertility loss and excess mortality of all Chinese provinces during sistent (SI Appendix, Table S1). the Great Chinese Famine (25). As a leading producer of rice, – Sichuan transferred grain to other affected provinces while also Over the 2005 2018 study period, annual mean PTB incidence aggressively implementing a “communal dining” system in which rate was higher among men (123.4 per 100,000) than women food stocks and cookware were confiscated from rural residents, (54.1 per 100,000). The annual mean incidence rate was higher but free meals were provided (21). This led to an illusion of in less developed, western mountainous regions, and lower in the B abundance, resulting in overconsumption and waste of food, more affluent eastern plains regions (Fig.
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