COVID ‐19, crisis, and emotional stress: A biocultural perspective of their impact on growth and development for the next generation

«Paintings for Wuhan», Li Zhong (China) © Li Zhong through Tricontinental: Institute for Social Research. Li Zhong is president of the Artist Association of Fengxian District, Shanghai (China). An interview with Li Zhong and a series of paintings on the fight in China against the COVID-19 pandemic area is available in Painting and epidemic. This is a Commentary on the impact of the current COVID-19 pandemic on future human growth and development. Our focus is on birth weight, one measure of prenatal growth and development, and its association with later life health. We assess the possibilities from the broad biocultural sense of human growth and development, especially in relation to its social-economic-political-emotional (SEPE) correlates. The biocultural perspective includes all aspects of human ecology in terms of biology, behavior, thinking, and beliefs. Human ecology and human biology are directly influenced by SEPE factors. A case in point is that on April 2, 2020 in the U.S. a freight train driver purposefully derailed his train to destroy the hospital ship Mercy sent to help with the COVID-19 crisis. The train driver said he did it because he believed the Mercy was part of suspicious activities involving the coronavirus. In addition, during the first week of April, 5G cellular communication towers in Birmingham, Liverpool and Melling, UK were burned by people claiming that 5G technology is the cause of COVID-19. Such emotionally and ideologically driven behavior always happen during pandemics. In the year 1630, a Bubonic Plague epidemic erupted in Milan, which also was at war with Spain. Four Spaniards in Milan were arrested, convicted of spreading Plague, and sentenced to death by torture. During the Plague pandemic of 1349 the people of Strasbourg, Alsace accused Jews of poisoning the water wells. One thousand Jews were arrested, taken to the cemetery, and burned alive. These cases and others of paranoia and murder during pandemics are described by medical historian Frank M Snowden in his book, Epidemics and Society: From the Black Death to the Present (Snowden, 2019).1 Fear of pandemic disease spreads as fast and as deep as the disease itself. The fear plays-out in in many ways, from extremes of paranoia and violence, to xenophobia, closed borders, economic lockdowns, and social distancing. The fear pervades every level of society. The fear causes emotional stress. Chronic emotional stress—from insecurity that lasts for months or years—has biological impacts on people. Along with several colleagues, we have been investigating the impact of chronic emotional stress on human growth. In one series of studies, we analyzed changes in birth weight related to the 2008 financial crisis in Spain. We reported a decline in birth weight across virtually all maternal social-economic groups in Spain in the years leading up to, and especially, during the financial crisis (Terán, Juárez, Bernis, Bogin, & Varea, 2020; Terán, Varea, Juárez, Bernis, & Bogin, 2018; Varea, Terán, Bernis, Bogin, & González-González, 2016). Our findings are supported by studies reporting reduced birth weight in Portugal, Iceland, Japan, and Greece during the 2008 banking system crisis, which was a global financial pandemic (Kana, Correia, Peleteiro, Severo, & Barros, 2017; Olafsson, 2016; Ueda, Kondo, & Fujiwara, 2015; Zografaki, Papamichail, & Panagiotopoulos, 2018). Many factors influence human birth weight. A few well-studied variables are maternal age, maternal size (height) and body composition, maternal psychological stress, gestational age at delivery, mother's hemoglobin concentration, and per capita daily income of the mother or family (reviewed in Bisai, Mahalanabis, & Bose, 2007; Bisai, Sen, Mahalanabis, Datta, & Bose, 2006). Other known influences of birth weight are maternal or fetal genetic anomalies; maternal exposure to infectious disease; maternal parasite load; maternal systemic diseases such as diabetes, hypertension, periodontal disease; abnormal placental development, and function that impairs fetal nutrition and oxygenation; maternal use or exposure to tobacco smoking, use of alcohol or many prescribed or illicit drugs (Negrato & Gomes, 2013). Maternal exposure to ambient air pollution is known to lower birth weight and increase the risk of preterm birth (Stieb, Chen, Eshoul, & Judek, 2012; Woodward, Finch, & Morgan, 2015). While any or all these variables may influence birth weight, we interpreted the findings from our Spanish research in terms of SEPE factors. Our interpretation was guided by the fact that the entire Spanish population of births was similarly affected. This includes births to women of all household income levels, educational attainment, region of the country, urban or rural residence, body composition, health status, and exposure to air pollution. The Spanish National registry of births does not include most of these variables. However, given the population-wide changes in birth weight, the impact of the 2008 financial crisis on pregnant women and birth outcome may have come about as an emotional response by mothers to the interaction of social, economic, and political factors at individual, family, and community levels. At all three levels, there was a reduction in material resources, such as jobs, money, and housing, deteriorating environmental conditions due to the closure or curtailment of public and private sector services in health, education, sanitation, and so forth, and a widespread increase in psycho-social stress due to the insecurity of material resources, reliability of services, and uncertainty of the future. These SEPE sequelae of the 2008 financial crisis are tightly comingled, as the material, environmental, and psychosocial stress were caused by the political decisions of the Spanish government to impose harsh fiscal and social austerity policies on the entire population. The uncertainties and psychosocial stress caused by the 2008 financial crisis and the governmental reactions to it could explain the Spanish birth weight reductions at two levels: first, at a population level, the crisis might determine changes in the sociodemographic profile of women who become mothers, with an increasing predominance of older women, who may have been at higher gestational or obstetrical risk; and second, at an individual level, the crisis might affect fetal development and birth outcome through direct worsening of living conditions and increased maternal stress during pregnancy. We analyzed the impact of both levels using a join point regression analysis to identify the time periods of significant changes in the prevalence of LBW by parity (Terán et al., 2020). Adjusted relative risk (RR) of LBW by year of birth was calculated in order to confirm that the time trend differences in LBW by parity were independent of possible confounders. The prevalence of LBW among singleton live births to primipara increased from 5.12% in 1996 to 6.87% in 2008 and then stabilized at that maximum value. Among live births to multipara LBW increased from 3.96% in 1996 to a maximum of 5.20% in 2008 and then significantly reduced (Figure 1). Trends in adjusted RR of LBW by parity confirm that primipara and multipara were affected differently by the financial crisis. Older, nulliparous women may have felt more biosocial pressure to reproduce during the financial crisis, compared with women who were already mothers. That biosocial pressure may have increased the risks for LBW. For all women, the global SEPE stress imposed in the years up to the financial crisis associated with a statistically and biologically significant increase in LBW. There is a growing body of evidence in the literature for pathways from SEPE stress toward LBW. Several key articles were published in the American Journal of Human Biology. An evolutionary perspective on maternal stress and fetal responses was taken by Ivy Pike (2005). While she focused on preterm delivery, Pike did report that the stress of racial discrimination is associated with the consistently lower birth weights of African American neonates compared with European Americans. Countering claims that low birth weights for African Americans are due to genetic factors, Pike reviews the evidence published by David and Collins (1997) that recently immigrated women of African origin have higher birth weight babies than African Americans, but the risks for poor pregnancy outcomes increase with the duration of stay and exposure to racial discrimination of the immigrants in the United States. Discrimination and racism based on skin color, ethnicity, religion or any other characteristic of human groups is a powerful SEPE stress with measurable biological consequences. Building on Pike's review and analysis, Kuzawa and Sweet (2009) employed a social constructivist model to integrate the extensive literature showing how SEPE stresses become “embodied,” meaning in this case, how material and psychosocial discrimination are transduced into human biology, creating durable and transgenerational influences on health disparities in the United States (Figure 2). Kuzawa & Sweet's focus was on the social origin of prematurity and LBW in African Americans. They emphasized the biocultural pathways by which the effects of racial discrimination impact maternal stress physiology and lead to lower birth weight. In turn, lower birth weight babies are known to have higher risks for adult overweight and associated diseases. In this model, there are direct, “…links between early life environmental factors like maternal stress during pregnancy and adult race-based health disparities in diseases like hypertension, diabetes, stroke, and coronary heart disease” (p. 2). Empirical evidence for the transgenerational transmission of synergism between physiological stress and lower birth weight is provided in two studies by Zaneta Thayer and colleagues. They measured salivary cortisol, a widely used indicator of psychosocial and physiological stress. Both the absolute levels of salivary cortisol and its diurnal variation have been shown to be associated with reduced growth in body length (Nyberg et al., 2012). The first study (Thayer, Feranil, & Kuzawa, 2012), included a sample of 488 participants, mothers aged 20.8 to 22.3 years old, of the Cebu Longitudinal Health and Nutrition Survey, Philippines. Thayer and colleagues reported that mothers who were themselves born with lower birth weight had higher evening cortisol levels (P < .04) and that independently both lower maternal birth weight (P < .0001) and higher evening cortisol in adulthood (P = .003) predicted lower birth weight for male offspring. The associations for female offspring birth weight were not statistically significant (maternal birth weight, P = .07; bedtime cortisol, P = .3). The second study (Thayer & Kuzawa, 2014) was conducted in Auckland, New Zealand with a sample of 55 women at 34 to 36 weeks gestation. The socioeconomic status (SES) of the women was categorized using the locally validated NZ Deprivation Index for individuals (NZiDep). Maternal saliva samples were assessed for cortisol in the morning and at evening bedtime. Offspring salivary cortisol (N = 19) was assessed before and after a standard vaccination, a mild trauma, 6 weeks after birth. The authors reported that, “…after controlling for ethnicity and other covariates, women with higher NZiDep scores had significantly higher evening but similar morning cortisol, consistent with a pattern of chronic strain. Infants of women reporting greater material deprivation had elevated cortisol response to vaccination” (p. 723). Greater material deprivation and the chronic, daily stress this causes was associated with greater cortisol reactivity in both mothers and offspring. The authors review research showing that greater morning-to-evening reactivity and posttrauma reactivity are both predictive of poorer health now and in the future. Research in Yucatan, Mexico connects the studies just reviewed, and many others on maternal SEPE stress and birth weight, to later life physical growth. Hugo Azcorra, Samantha Sanchez-Escobedo and colleagues have been working with Maya families, all of whom are of low socioeconomic status (Azcorra, Dickinson, Bogin, Rodríguez, & Varela-Silva, 2015; Sanchez-Escobedo et al., 2020). One study included 109 families with measurements of a 6 to 8-year-old child, her/his mother, and the mother's mother (grandmother) living in Merida, the largest urban area of Yucatan. The researchers used total height and leg length as proxies for the quality of the material and SEPE environment. It was reported that maternal height and leg length were positively associated with child height and leg length. The association was relatively stronger for leg length, which is often a better index than total height of the quality of living conditions during infancy and childhood (Bogin & Varela-Silva, 2010). Better living conditions of the grandmother in terms of house quality and larger family size were significantly associated with higher values of leg length in the grandchildren. All the grandmothers grew-up in rural, agricultural areas where larger family size indicated more secure, less stressful living conditions. So, even in their current conditions of urban poverty, with daily insecurity from many material and SEPE stressors, early life conditions of rural-living grandmothers were shown to have transgenerational effects on the linear growth of the grandchildren. In another study the researchers worked with 260 dyads of Maya children aged 6 to 8 years and their mothers living in the city of Merida and the town of Motul, Yucatan, Mexico. The authors reported that child height-for-age was positively associated with the child's birth weight and with maternal height and mother's current age, but inversely associated with birth order and age of introduction of solid foods, that is, the age of termination of breastfeeding. These findings were interpreted to indicate that well-being of the children, as measured by their height-for-age, is influenced by both the quality of SEPE living conditions when the mother was growing-up and during her pregnancy, and by the child's own SEPE conditions. Taken together, these two Mexican studies and the others reviewed above, all support the life course, intergenerational model of SEPE stressors and their influence on birth weight and later growth, development, and health illustrated in Figure 2. 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