Climate has direct effects on the health of diverse populations across the globe [1
]. Changes in rainfall patterns and temperature patterns are resulting in far-reaching health effects [3
] Vector and food-borne diseases, food insecurity, heatwaves and the effects of other extreme weather events make millions sick annually [4
]. Heat is possibly the climate-related illness of greatest concern. In the United States, extreme heat events are causing more deaths than all weather-related fatalities combined [5
]. High temperatures adversely impact the human body by interfering with its ability to dissipate heat and thermoregulate, leading to heat exhaustion and possibly heat stroke, a condition characterized by a core temperature ≥40.6 °C and central nervous system dysfunction [6
Populations vulnerable to heat have most often been children under the age of five and adults over 65, individuals with pre-existing conditions, and those of low socioeconomic status who have limited ability to cope [7
]. Urban populations are of central concern since the urban heat island effect is created when limited greenspace and larger proportions of impenetrable surfaces reflect heat in the surrounding environment, resulting in localized microclimates 4.4–5.6 °C above average temperatures [9
]. However, there are other vulnerable populations who have not generally been of concern who deserve greater attention.
Despite research demonstrating the effects of heat on pregnant women, the effects of heat on them and their fetuses have often been left out of this discussion. The more recent assessment by the Intergovernmental Panel on Climate Change did explore the adverse effects of heat on maternal health outcomes [10
]. The World Health Organization has named improving maternal and child health a continued focus in their Sustainable Development Goals, as targets from the Millennium Development Goals for maternal and child health were met. Despite improvements in reducing under age five child mortality and the global maternal mortality ratio, both efforts failed to meet the respective 66% and 75% reduction goals [11
]. Up to 40.3% of deaths in children under five years of age occur in neonates [12
], and preterm births account for 35% of neonatal mortality worldwide [1
]. Preterm birth rates may reach 18% in some sub-Saharan African and South Asian countries, and only three countries globally successfully reduced preterm birth rates from 1990 to 2010 [1
Pregnant women are susceptible to increasing ambient temperatures and heat waves since their ability to thermoregulate is compromised [13
]. Furthermore, pregnancies are susceptible to complications at all stages of gestation. Such complications may affect maternal health, fetal health, perinatal health, or postnatal health of the mother and/or child [14
], and are complex in both etiology and outcome. The sequelae of heat exposure on developing fetuses are not yet completely understood since the epidemiology behind many adverse fetal outcomes, including preterm delivery, is diverse [1
]. Low birth weight was previously hypothesized as a consequence of sustained heat exposure and maternal heat stress [13
]. While there is not conclusive evidence at this point, there may be a connection between adverse birth events and extreme deviation in ambient temperature.
We conduct a systematic review to identify how extreme heat, specifically effects maternal, fetal, and neonatal health. There have been a handful of systematic reviews on the influences of climate change and variety of birth outcomes [14
]. This review is an update and focused assessment of preterm labor, birth weight, and stillbirth as a result of ambient temperature exposures in a rapidly developing field of research. Additionally, this review specifically addresses the failure of existing heat health recommendations to capture heat-related morbidity in fetuses and pregnant women. This allows us to advance recommendations for pregnant women in the face of climate change by addressing insufficient public health recommendations for those populations during extreme heat events.
2. Materials and Methods
In January, 2017, we conducted a systematic review of the literature, following the Populations of interest, Exposures, Comparators, and Outcomes (PECO) Statement model. We investigated impacts of climate change processes on maternal, fetal, and neonatal health by targeting publications in the PubMed database (6450 results) and Cochrane Review (0 results). As the original search in PubMed returned a comprehensive number of articles, no searches in additional database were deemed necessary. Our search included the following terms: human AND temperature (OR ambient temperature OR hot temperature OR heat wave OR climate change) AND pregnancy (OR pregnancy outcome OR birth weight OR preterm birth OR gestational age OR stillbirth). Papers were included on the basis of pertaining to maternal health, reproductive health, birth outcomes, child health, and climate change processes. We focused on maternal, fetal and child populations, with the given exposure of atypical climatic processes. The primary exposure and climate change topic of interest was heat and heat waves. The outcome of interest was a notable change in health outcome for any one of these populations. Papers were excluded if they did not examine human populations. Papers that focused on specific disease processes, such as the vertical transmission of viruses in pregnant women, the indoor ambient environment, or maternal and fetal outcomes unrelated to climate change or temperature were excluded.
We examined each research article for the following criteria: population of exposure, nature of exposure, measured outcome, study type, location, and possible sources of bias. In exposure, we noted data on temperature measurements, duration of heat events, and severity of temperature exposure. For each type of outcome, we collected statistical outcomes, confidence intervals, and risk estimates, when provided. Confounding or mitigating factors, such as air pollution and socioeconomic variables, were also collected. Each article was examined for the possibility of bias, including selection bias, misclassification bias, detection bias, internal validity. Definitions for preterm birth, early birth, lower birth weight, and still-birth were used according to established literature. The World Health Organization defines preterm birth as occurring at less than 37 weeks of gestational age, and low birth weight as birth weight of less than 2500 g [17
]. Early term birth is defined as 37–38 gestational weeks at birth.
The study selection proceeded according to Preferred Reporting Items for Systematic Reviews and Meta-Analyses (PRISMA) guidelines. Of 6450 initially screened studies, 28 met final selection criteria for this review. All search results were exported to RefWorks. The papers were screened initially by title, contents of abstract, and then by contents of full text by one reviewer. The search terms returned both reviews and original research articles; reviews were excluded from this literature review. As such, the final selection of articles is a combination of literature retrieved from the initial search terms, from reviewing reference lists of selected articles and linked citations from newly published literature, though only 1 source was returned via hand selection (see Figure 1
Studies were selected based on their adherence to these search criteria, and were evaluated based on the strength of their findings and the risk of bias present in each study. We examined each research article for the following criteria: population of exposure, nature of exposure, measured outcome, study type, location, and possible sources of bias. In exposure, we reviewed method of temperature measurement, duration of heat events, and nature of temperature exposure. For each type of outcome, we collected statistical findings where provided. Inclusion of air pollution and socioeconomic variables were included in the final analysis of the study. In the event that a study was deemed to have high risk of bias, it would be removed from the literature review; however, no studies were deemed to have inappropriate risk of bias.
Incidence or risk of preterm birth, early term birth or shortened gestation, birth weight, low birth weight, stillbirth, and neonatal heat-related distress all arose as relevant outcomes for temperature in this review. Furthermore, the intensity of the temperature exposure is wide-ranging. This review includes exposures measured over a variety of intervals, seasons, and extremes. Such variety in data collection necessitates a wide range of study designs.
This systematic review demonstrates that extreme heat exposure affects fetal outcomes, ranging from stillbirth rates to birth weight and gestational age. This trend is present in research regarding reduced gestational age and preterm birth. The specifics of this review represent some clear conclusions regarding actions that should be taken to prevent adverse effects of heat on pregnant women.
First, public health agencies should specify that their warnings apply to pregnant women. This is complicated by the lack of uniformity in defining a heat wave. The definition of a heatwave alters the amount of heat-related morbidity captured within an exposure period. Recent meta-analysis demonstrates that correlations between mortality and specific heat wave definitions vary by the temperature threshold and the duration of the event [47
]. The most important metric for determining both mortality and morbidity from heatwaves is intensity [20
]. The inclusion of humidity and other meteorological factors may not increase prediction of heat-related morbidities [24
] or may cause a direction of effect that was counterintuitive [49
]. The most important component of generating an appropriate definition of a heatwave is consideration of average local temperatures [24
] but in correlation with the specific health profile of the target population, focusing on the health risks posed by excess heat exposure [51
When attempting to reduce heat-related illness through public health warnings, the timing of the heat wave should be taken into consideration. Heat events occurring earlier in the warm season cause an increase in adverse outcomes relative to comparable events occurring later. As such, the relative acclimatization of the population should be considered as an additional factor when generating heat warnings. Furthermore, these results may not appear initially, but rather as a lagged effect, with adverse outcomes appearing from immediately after exposure to as late as one month post exposure [23
]. While some extreme heat exposures resulted in acute outcomes, exposures to moderate temperature spikes may results in an adverse birth outcome delayed by a longer time interval.
Second, urban planning may also become a necessary tool to prevent adverse birth outcomes. Urban heat is affected by albedo (reflectivity) and land use patterns. More specifically, as land use increases and reflectivity increases, the relative magnitude of UHI will also increase [52
]. Increasing greenspace may reduce the ambient temperature of a given area, particularly through increasing canopy cover [52
]. Without adequate urban planning and adaptation, cities will rely on air conditioning, an energy-intensive mitigation strategy, to reduce exposure [53
Yet, air pollution has been correlated with all-cause mortality [54
] and low birth weight [55
]. Levels of fine particulate matter (such as PM2.5) may increase in low and middle income countries (LMICs) as well as developing countries, serving to further exacerbate adverse fetal health risks [55
]. Increasing air pollution levels appear to cause increased maternal stress [56
] that is exacerbated in heat waves when pollutant concentrations rise [3
], further impacting fetal stress. While most studies accounted for air pollution as a potential confounder, air pollution coupled with heat may directly impact both maternal health and birth outcomes [37
]. Therefore, strategies to address heat exposure for pregnant women should also reduce both the impact of extreme heat and air pollution through urban design and implementation of heat warning systems [52
]. Greenspace should be expanded within urban areas, not only as it reduces the impacts of UHI, but since proximity to greenspace has additionally been linked to lower PM2.5 exposures in pregnant women [57
], and may reduce risk for adverse birth outcomes.
Finally, identifying the most effective strategies to prevent adverse outcomes would ideally rely on an improved understanding of the primary causes underlying adverse birth outcomes from heat. However, they are currently not well understood, as the etiologies of low birth weight and preterm birth are complex. There are a number of theories regarding this connection, such as increased maternal heat production [13
], increased weight gain, and the burden of the fetus overwhelming a pregnant woman's ability to tolerate heat stress, resulting in low birth weight. Increasing heat stress may cause uterine constriction, and dehydration may result in decreased uterine blood flow [58
]. Inflammation may also contribute to low birth weight or preterm birth [58
]. Díaz et al. [39
] argue that preterm birth and low birth weight outcomes must be considered separately due to the high correlation between preterm birth and low birthweight. Socioeconomic factors may further play a role, as psychological stress, social stress, and housing instability may further increase risk for preterm birth [58
While there has been significant progress on heat and birth research in the last five years, a number of limitations remain. We only included articles that are written in English. While this obviously offers an imbalanced representation of the literature, we do not believe it is a biased review since many studies in non-English speaking countries are still represented. Several studies report effect modification by socioeconomic factors, such as race, income, and profession [26
]; these factors are not included in analysis universally in the data sets. Furthermore, there is a widespread lack of information regarding home air conditioning access, or other resources that serve as mitigating factors in heat exposure [35
]. These factors may serve as confounders within studies, bias findings towards the null, or cause discord in results among studies. The protective effect of extreme heat (99th percentile) on preterm birth observed by Liang et al. [30
] demonstrates that socioeconomic data and air conditioner use may impact preterm birth in Shenzhen, China differently from other cities in ways not yet quantified. However, this review of the literature is not a meta-analysis, and therefore cannot draw further statistical significance of heat impacts on birth outcomes beyond the findings of the original studies.
The World Health Organization and the World Meteorological Association have suggested that the heat exposure should be taken into consideration in both clinical care and public health programming. Vulnerability will play an additional role in heat-stress susceptibility. Current literature largely refers to heat-susceptible individuals as poor, elderly, young children, minority groups, outdoor workers, individuals with chronic respiratory or cardiovascular disorders, socially isolated individuals, and living in an urban heat island [2
]; notably, pregnant women are not included. However, limited thermoregulatory abilities warrants, dependent on medical care access, the inclusion of pregnant women as a vulnerable class in the face of heat exposure [13
]. Therefore, when considering the exaggerated impacts of heat, pregnant women must also be included as an at-risk class. Vulnerability and warnings should be specified to local context. Heat tolerance and acclimatization may affect the heath of pregnant women and fetuses. The threshold temperature that results in significant effects varies by climate since women in each region have acclimatized to a relative threshold for extreme heat.
Due to climate change, increasing heat waves are likely unavoidable in the coming century. Heat exposure promises to affect population health, such as developing fetuses and pregnant women. We are likely to see an increase in preterm birth, a decrease in birth weight, and an increase in stillbirth rates. After birth, neonates may be susceptible to heat-related morbidity and mortality, though additional research is required. These findings indicate the importance of ongoing public health efforts to combat local effects of climate change.