El Niño adversely affected childhood stature and lean mass in northern Peru

The El Niño phenomenon is an anomalous warming of sea surface temperatures (SST) in the equatorial Pacific that causes extreme weather variability every 2 to 7 years [1], leading to disaster and disease worldwide. During El Niño episodes, natural disasters such as severe drought and floods are estimated to affect 35 per 1,000 people, more than four times the rate affected by natural disasters during non-El Niño years [2]. El Niño episodes have been linked to increased incidences of malaria [3]-[6], dengue [7]-[10], cholera [11]-[10], and diarrhea [15],[16], all of which are highly prevalent in the developing world. Even small increases in any of these diseases translate into hundreds of thousands of deaths and millions affected.

While many studies have evaluated the short-term effects of El Niño episodes such as an increase in the burden of infectious diseases, the long-term consequences on human health have not been studied. Due to the recurrent and global nature of El Niño, it is important that we gain a better understanding of possible long-term adverse effects on the health of affected human populations. One such measure of poor health is failure to grow adequately in height, also known as stunting. Small stature for a given age and sex is a surrogate measure of chronic malnutrition [17]. Stunting occurs in early childhood as a result of undernutrition, a high burden of infectious diseases, or both [18]. In developing countries, height deficits incurred early in life generally persist through childhood and even adulthood [19],[20] and have been linked to other developmental problems including delayed motor [21] and locomotion skills [22], cognitive impairment [23], delayed school enrollment [24] and poor school performance [25], lower adult productivity [26], and higher risk pregnancies and deliveries.

El Niño impacts communities throughout the world; however, the northern coastline of Peru suffers the greatest effects of El Niño episodes through heavy rainfall and severe flooding. During the 1997–1998 El Niño episode, the most severe on record, the Peruvian government received an early forecast of its potential severity 6 months prior to the onset of heavy rains. The government developed a prevention strategy that centered on the preservation of infrastructure and construction and repair of irrigation and drainage systems [27]. Despite these efforts, overflowing riverbanks cut off access to bridges and roads and isolated many rural villages in northern Peru, some for months at a time. Food, clean water, and healthcare were largely inaccessible in these villages, and increased cases of malaria and diarrhea were reported throughout the region [5],[28]. Severe damage to crops and livestock limited food reserves and severed an important source of income for most rural residents. Due to severe food shortages and increased incidence of infectious diseases during El Niño, we hypothesized that children born in northern Peru during and after the 1997–1998 El Niño may be shorter for their age and sex than children born in other years. In 2008–2009, we visited a random sample of children born between 1991 and 2001 in a cluster of rural villages in Tumbes, Peru, and measured their height, weight, and bioelectrical impedance. As secondary objectives, we also examined 1) whether children born after the onset of El Niño had differences in later body composition (lean mass (LM) and fat mass (FM)) and 2) whether birth and death rates in Tumbes changed significantly in 1997–1998, the period of El Niño, using data collected by the Peruvian National Institute of Statistics and Information between 1994 and 2002.

Two important indicators used in public health to measure the well-being of children are mortality and nutritional status. This study demonstrates that El Niño may have had a marked effect on the long-term nutritional status of children, yet the effect on mortality was negligible. Although the negative effect in height and lean mass was not prevented, if the major effort to intervene by the Peruvian government had not occurred, this disaster might have produced a severe impact on mortality which has been seen in other similar disaster situations such as the 1999 flood in Venezuela [38], the 2000 flood [38] and 2002–2003 droughts in Mozambique [39], and more recently, the 2009 flood in the Philippines [40] and the 2010 flood in Pakistan [41].

Our original hypothesis anticipated that the 1997–1998 El Niño would have a negative effect on the age- and sex-adjusted heights of children born during El Niño. These data support this hypothesis and further show that children born both during and after the 1997–1998 El Niño have a lower HAZ than would be expected if the El Niño had not occurred. That is, the trend of improvement in HAZ over time in children born in the post-El Niño years (1999–2001) failed to recover to pre-El Niño levels. Thus, the disruption and destruction left by El Niño may not have been resolved during this time, particularly in those regions with the heaviest flooding, having a protracted effect on the nutritional status of children born even 3 years after the initial disaster.

The abating height attainment of children born during and after the 1997–1998 El Niño event may be the result of an increased incidence of infectious illnesses during the period of the El Niño disaster as well as food unavailability. Previous studies conducted in Peru have shown that the incidence of infectious illnesses in children, particularly bouts of diarrhea, spiked during and after El Niño likely due to the warmer and wet conditions that accompany El Niño events [15],[16]. In addition, El Niño has been linked to epidemics of malaria in northern Peru [5] and dengue in an Ecuadorian region neighboring Tumbes [5],[42]. During focus groups conducted in a subsample of Tumbes villages (villages that are also included in our analysis), village members reported an increase in illness and prolonged food shortages, particularly of animal protein foods, during the El Niño period and after [43]. In addition, there was a substantial loss of the chief crops of banana and rice in this region as a result of El Niño, affecting food availability and prices as well as the economic livelihood of these communities, which largely rely on the export of these crops. In conclusion, it is possible that children born during the disaster as well as during its aftermath may have been more likely to have an infectious illness and less likely to have a diet adequate for optimal growth, which may explain the negative association of El Niño and height attainment in these children found in our results.

El Niño had an impact on lean mass but not fat mass regardless of the amount of flood exposure. It is not surprising that El Niño may have adversely affected only lean mass given that later body composition is strongly influenced by the nutritional environment experienced in early life, during both the prenatal and postnatal periods [44]. Previous studies from diverse populations have shown relatively consistent findings, in that birth weight is positively associated with later lean mass but not fat mass, indicating that reduction in fetal growth diminishes later lean mass [44]. Findings for infant weight gain differ between industrialized and developing countries; in the latter, based on studies from Brazil, Guatemala, and India, infant weight gain is again positively associated with later lean mass but not fat mass, indicating that poor infant growth would constrain later lean mass [44]. Lean mass is an important predictor of physical work capacity in later life [45],[46], which may have important implications for productivity particularly in primarily agricultural and fishing communities such a Tumbes. Similar to height, El Niño’s effect on decreasing lean mass may have been the result of the unavailability of nutrient- or energy-dense foods to those children born during the disaster and the aftermath. More research is needed to further understand the mechanisms by which the El Niño disaster affects growth in young children.

Just as rings act as indicators of natural disasters experienced by a tree throughout its life [47], exposure to severe adverse weather events in utero or early life can leave a long-lasting mark on growth and development in young children. In low- and middle-income countries, a child who undergoes inadequate growth early in life is unlikely to achieve complete catch-up growth later on [19]. Early shortfalls generally persist into adult life. As noted, stunting is a marker for decreased mental and physical capacity [21]-[23],[27]. Early disruptions to lean mass appear to affect its constituent components unequally, protecting the brain at the expense of other organs and tissues such as the kidneys, liver, pancreas, and muscle mass [48],[49]. These effects also vary as to whether they occur in fetal life or infancy. In later life, such constraints on early growth are predicted to reduce the capacity for homeostasis, and increase the risk of chronic degenerative diseases, as shown extensively elsewhere [26].

Our study has some potential limitations. First, due to the nature of the cross-sectional study design, nutritional measurements (height, weight, and body composition) were taken at only one time point for each child, and therefore, inferences cannot be made regarding the change in height across time at the individual level. In addition, we do not have earlier information such as birth weight or any illness history prior to or during the 1997–1998 El Niño episode. Despite this, our data include nutritional measurements for children across several birth cohorts and therefore allow for comparisons of the mean average change in height, lean mass, and fat mass between birth year cohorts. Second, we define exposure to El Niño in early life as having a birth year that coincides with the onset (or after) of El Niño. It is possible that the effects on height attainment and lean mass may be due to other events that may have occurred during the same period as the onset and aftermath of the El Niño disaster; however, in focus groups conducted in a subsample of villages in Tumbes, community members did not cite other events occurring during the same period as El Niño that had such a destructive impact on their lives [43]. Third, we may have been underpowered to detect a possible effect on lean mass in households with higher flood likelihood. Fourth, our study may be less representative of older children in our cohort, as many of them were either hard to reach because they were working and difficult to find or were married and had moved to another household or another village. Lastly, the variables used to generate the SES index were based on self-report. As with any self-reported information, these variables are subject to reporting bias; however, if bias were present in our data, the results would be biased towards the null making our estimates conservative and not changing our final conclusions.

Despite these limitations, our study has several strengths. First, both villages and children within each birth cohort were randomly selected. Therefore, we are confident that our sample is representative of the study population. Second, we used standardized and consistent methods to measure height, weight, and body composition across all children, and therefore the measurements are reliable and can also be compared with other populations. Third, only children who had lived in Tumbes since 1 year of age were eligible for enrollment eliminating a possible risk of bias from migration. Finally, as shown in our analyses, our results are not likely to be affected by migration or a mortality difference.

If adverse weather events affect a significant portion of young children of a country, then they have the potential to adversely affect the future of a community as a whole. Some investigators hypothesize that global warming will translate into more frequent El Niño episodes [50],[51] heightening the urgency of the global health issues consequential to weather events accompanying El Niño. Because children and those in lower SES levels are most vulnerable to the health and economic impacts of disasters [52], including those induced by El Niño, it is imperative that we continue to explore the extent to which they are affected to design prevention strategies and target aid and relief during future El Niño episodes.