Abstract
Extreme weather events and climate change have witnessed a substantial increase in recent years, leading to heightened concerns. The rise in abnormal ambient temperatures, both in intensity and frequency, directly and indirectly impacts cardiovascular health. While the impact of high ambient temperatures on cardiovascular response is a common concern in the context of global warming, the significance of low temperatures cannot be overlooked. The challenges posed by low temperatures contribute to increased cardiovascular morbidity and mortality, posing a significant threat to global public health. This review aims to provide an overview of the relationship between low ambient temperature and cardiovascular health, encompassing the burden of cardiovascular outcomes and underlying mechanisms. Additionally, the review explores strategies for cold adaptation and cardioprotection. We posit that to optimize cold adaptation strategies, future research should delve deeper into the underlying mechanisms of cardiovascular health in response to low ambient temperature exposure.
1 Introduction
While the detrimental impact of climate change on human health has been recognized for centuries, the escalating frequency of extreme weather events and the growing population exposed to their hazards have reignited our attention to these issues. The general public is now more aware than ever of the health consequences stemming from abnormal weather patterns[1,2,3]. With a global average temperature increase of 1.2°C since the pre-industrial period (1850–1900)[4], it is imperative that we exercise caution regarding the health implications of global warming. Extensive research in the field of climate change and health has primarily focused on the effects of high ambient temperatures[5–6]. However, the impact of low ambient temperature has been largely overlooked within the context of global warming. Paradoxically, global warming contributes to an increased occurrence of extreme cold ambient temperature events[7–8]. For instance, during a warm winter from December 1, 2020 to February 20, 2021, China experienced three cold spells that brought about record-breaking low temperatures in numerous cities across the country[8].
Abnormal ambient temperatures not only have ecological implications but also pose life-threatening risks to public and individual health, contributing to increased morbidity and mortality[9–10]. It is important to note that the elevated mortality or morbidity associated with climate change is often indirectly driven by factors other than direct hyperthermia or hypothermia, such as cardiovascular diseases (CVD)[11–12]. In recent years, mounting evidence has emerged linking exposure to abnormal ambient temperatures with a widespread epidemic of CVD[13,14,15,16,17,18]. Epidemiological studies have consistently demonstrated that abnormal ambient temperatures serve as a risk factor for CVD morbidity and mortality[19,20,21,22]. Moreover, the relationship between ambient temperature and CVD mortality exhibits a non-linear pattern, often characterized by a V-, U- or J-shaped curve[23,24,25,26,27]. Notably, cold ambient temperatures have a more pronounced impact on the burden of CVD morbidity and mortality compared to heat[25–26,28,29,30]. Consequently, our intention is to provide a comprehensive review of the cardiovascular effects of low ambient temperature and explore strategies for cold adaptation in cardioprotection.
2 Global burden of CVD attributable to low ambient temperature
A substantial body of epidemiological evidence has consistently shown a positive correlation between low ambient temperature and increased morbidity and mortality related to CVD[19,20,21,26,31]. Despite variations in the definition of low ambient temperature across different studies, the overall burden of CVD risks remained relatively constant[32,33,34]. Moreover, the burden of CVD mortality significantly varied significantly depending on the specific causes of CVD[20,36]. In a systematic review and meta-analysis conducted in China from 2001 to 2018, it was found that a temperature decrease of 1°C beyond the threshold led to a 6% increase in cardiovascular mortality (RR, 1.06; 95% CI: 1.04–1.07) during cold periods[35]. Another systematic review focused on temperate and tropical countries revealed a significant increase in the risk of cardiovascular hospitalization associated with cold exposure (RR, 1.028; 95% CI: 1.021–1.035)[37]. Additionally, the magnitude of the effect of low ambient temperature on the burden of CVD exhibits variability. Findings from several studies indicated that moderate cold had a higher attributable fraction of CVD mortality and hospitalization compared to extreme cold[23,29,37,38,39,40].
Furthermore, in order to capture the impact of ambient temperature-related premature deaths, studies have increasingly employed years of life lost (YLL) as a health indicator instead of mortality, taking into account life expectancy at the time of death[19,26,41–42]. Recent studies have shown that the population-adjusted YLL rate (YLL/100000 population) maybe a more suitable health indicator, considering the varying population sizes across different studies[43–44]. Cold temperatures have been found to significantly exacerbate premature deaths from CVD[44–45], with and the highest burden of CVD-related life loss attributed to moderate cold[26]. The effects of low ambient temperature on CVD mortality/mortality often exhibit lag patterns, lasting from 0 to 4 weeks[23,39–40,46,47,48,49], although one study did not identify any lag effect, possibly due to the use of heating installations[27]. Various potential effect modifiers, such as demographic characteristics, socioeconomic characteristics, climatic zones, and others, have been explored in the majority of the studies. The burdens of CVD mortality, morbidity, or YLL are more pronounced among the elderly[23,50,51,52], males[27,51,53–54], individuals aged ≤ 9 years[23], widowed adults[20], ever-smokers[55], alcohol drinkers[55–56], during the cold season[52,55], in temperate monsoon and subtropical monsoon zones[23,52], cities characterized by higher urbanization rates and shorter durations of central heating[23], and among individuals with chronic diseases[19,57–58]. However, some studies have indicated that the burden of CVD mortality and morbidity is more significant among those aged ≤ 65 years old[19, 53–54] and females[23, 52]. Nevertheless, certain studies did not find any effects when stratifying by sex, age, body mass index (BMI), and smoking status[56,59]. The differences in demographic, geographical, and climatic characteristics, socioeconomic status, climate change adaptation policies, physiological factors, and human behavioral factors could potentially explain the discrepancies among these studies. Moreover, it is important to note that while studies on the impact of air pollution on CVD risks have been extensively performed[60,61,62], only a few studies have adjusted for air pollutants, including nitrogen dioxide (NO2), ozone (O3), fine particulate matter (< 2.5 μm in aerodynamic diameter, PM2.5), and PM10 (< 10 μm in aerodynamic diameter)[29,39,63]. Selected investigations on low ambient temperature and the mortality and morbidity of CVD are summarized in Table 1 and Table 2, respectively.
Summary of selected studies on low ambient temperature and CVD mortality
| Authors (year of publication) | Study region | Study period | Population size | Outcome variables | Main outcome | Reference |
|---|---|---|---|---|---|---|
| Carder et al. (2005) | 3 large cities in Scottish | 1981–2001 | 1,652,000 | Cardiorespiratory mortality | For temperatures below 11°C, a 1°C drop in the daytime mean temperature on any day was associated with an increase in mortality of 3.4% (95% CI: 2.6, 4.1) over the following month for CVD disease. | [47] |
| Zeka et al. (2014) | Ireland | 1984–2007 | 1,057,046 | CVD mortality | CVD mortality showed the greatest increase associated with temperatures in the preceding week; the impact of cold temperature on mortality was slightly weakened, but lasted up to 4 weeks prior to death. | [49] |
| Wang et al. (2015) | Beijing and Shanghai, China | 2007–2009 | none | CVD mortality | People with hypertensive disease were particularly susceptible to extremely low temperature in Beijing. People with ischemic heart disease in Shanghai showed greater susceptibility to extremely cold temperature. | [48] |
| Yang et al. (2015) | 15 cities in China | 2007–2013 | 1,936,116 | CVD mortality | Cold weather was responsible for temperature-related CVD death burden with a fraction of 15.8% (95% CI: 13.1%, 17.9%), corresponding to 305902 deaths. | [34] |
| Zhang et al. (2016) | Wuhan, China | 2003–2010 | 32,721 | CVD mortality | For cold effects over lag 0–21 days, a 1°C decrease in mean temperature below the cold thresholds was associated with a 3.65% (95% CI: 2.62, 4.69) increase in CVD mortality. | [46] |
| Fu et al. (2018) | India | 2001–2013 | 40,003 | Ischemic heart disease death | Moderately cold temperature (13.8°C) was estimated to have higher attributable risks (9.7% [95% CI: 3.7, 15.3]) for ischemic heart disease death than extreme cold one. | [38] |
| Zhang et al. (2018) | Yinchuan, China | 2010–2015 | 26,097 | CVD mortality | Cold temperature was associated with significantly delayed CVD mortality. | [27] |
| Chen et al. (2018) | 272 main Chinese cities | 2013–2015 | 1,826,186 | CVD mortality | Compared to the minimum mortality temperatures, extreme cold temperature had larger relative risks (1.92 [95% CI: 1.75, 2.10]) than extreme hot temperature (RR: 1.22 [95% CI: 1.16, 1.28]) on CVD mortality. | [23] |
| Lv et al. (2020) | Hunan, China | 2013–2017 | none | YLL rate | Cold temperature was responsible for most of the YLL for cardiovascular death, with an overall estimate of 15.94% (8.82%, 23.05%). | [43] |
| Cheng et al. (2021) | Hong Kong, China | 2000–2016 | 67,157 | YLL | Cold was estimated to cause life expectancy loss of 0.9 years in total cardiovascular disease. | [41] |
| Hu et al. (2021) | 364 locations across China | 2006–2017 | none | YLL | An average of 1.07 (95% CI: 1.00, 1.15) years life loss per CVD death was associated with cold temperature. | [26] |
| Liu et al. (2021) | 364 locations across China | 2013–2017 | none | YLL rate | A mean of 1.1 (95% CI: 0.67, 1.37) YLL per CVD death was attributable to cold temperature. | [44] |
| Lv et al. (2022) | Hunan, China | 2013–2017 | 711,484 | YLL rates | Life loss per death of cardiovascular diseases attributable to cold temperature was 1.13 (95% CI: 0.89, 1.37), particularly moderate cold (1.00, 95% CI: 0.78, 1.23). | [19] |
| Xu et al. (2022) | Jiangsu, China | 2015–2019 | 1,000,014 | CVD mortality | Exposure to extreme cold (−0.6°C) was significantly associated with increased odds of mortality (1.79, 95% CI: 1.73, 1.85). | [20] |
CVD, cardiovascular disease; CI, confidence interval; eCI, empirical confidence interval; RR, relative risk; YLL, years of life lost.
Summary of selected studies on low ambient temperature and CVD morbidity
| Authors (year of publication) | Study region | Study period | Population size | Outcome variables | Main outcome | Reference |
|---|---|---|---|---|---|---|
| Sartini et al. (2016) | British | 1998–2012 | none | CVD morbidity | CVD risks were higher in winter. | [55] |
| Bai et al. (2016) | Ontario, Canada | 1996–2013 | 395,840 | Hospitalizations from hypertensive diseases and arrhythmia | Compared to the temperature with minimum risk of morbidity, cold temperatures (1st percentile) were associated with a 37% (95% CI: 5%, 78%) increase in hypertension-related hospitalizations. Arrhythmia was not linked to temperatures. | [32] |
| Hensel et al. (2017) | Hamburg, Germany | 2010–2014 | 510,389 | CVD emergencies | Coronary artery disease, cardiac pulmonary edema and hypertensive urgency were increased at low temperatures, particularly below 10°C. | [33] |
| Ponjoan et al. (2017) | Catalan | 2006–2013 | 22,611 | CVD emergency hospitalization | The overall incidence of CVD hospitalization was significantly increased during cold spells (IRR = 1.120; 95% CI: 1.10, 1.30) and the effect was even stronger in the 7 days subsequent to the cold spell (IRR = 1.29; 95% CI: 1.22, 1.36). | [59] |
| Bai et al. (2018) | Ontario, Canada | 1996–2013 | 1,389,057 | Coronary heart disease hospitalization | On cold days with temperature corresponding to the 1st percentile of temperature distribution, a 9% increase in daily hospitalizations for coronary heart disease (95% CI: 1%, 16%), 29% increase for myocardial infarction (95% CI: 15%, 45%) and 11% increase for stroke (95% CI: 1%, 22%) relative to the days with an optimal temperature. | [29] |
| Zhao et al. (2018) | Ningxia, China | 2012–2015 | 158,733 | Clinical visit | Cold effect on cardiovascular visits appeared at the lag 6th day and persisted until the 22nd day, resulting in a cumulative relative risk (RR) 1.55 (95% CI: 1.26, 1.92), compared to the minimum-clinical visit temperature. | [40] |
| Liu et al. (2018) | Beijing, China | 2013–2016 | 81,029 | Acute myocardial infarction (AMI) hospitalization | Compared to the 10th percentile temperature measured by daily mean temperature (T mean), daily minimum temperature (T min) and daily minimum apparent temperature (AT min), the cumulative RR at 1st percentile of T mean, T min and AT min for AMI hospitalization were 1.15 (95% CI: 1.02, 1.30), 1.24 (95% CI: 1.11, 1.38) and 1.41 (95% CI: 1.18, 1.68), respectively. | [51] |
| Mohammadi et al. (2018) | Tehran, Iran | 2013–2016 | 15,835 | AMI hospitalization | Cold temperatures increased the risk of AMI admissions. | [53] |
| Xu et al. (2019) | Suzhou, China | 2013–2016 | 100 | Blood pressure | The systolic blood pressure, diastolic blood pressure, pulse pressure, and mean arterial pressure decreased with hourly temperature decreased. | [56] |
| Cui et al. (2019) | Hefei, China | 2015–2017 | 35,096 | Hospital admission | Compared to the 25th percentile of temperature (10.3°C), the cumulative RR of extremely low temperature (1st percentile of temperature, 0.075°C) over lag 0–27 days was 0.616 (95% CI: 0.423, 0.891), and the cumulative RR of moderate low temperature (10th percentile of temperature, 5.16°C) was 1.081 (95% CI: 1.019, 1.147) over lag 0–7 days. | [54] |
| Tian et al. (2020) | Hong Kong, China | 2005–2012 | 521,575 | Emergency CVD hospitalization | Compared to the identified optimal temperature at 23.0°C, the cumulative relative risk during 0 to 21 lag days was 1.69 (95% CI:1.56, 1.82) for extreme cold (1st percentile) and 1.22 (95% CI:1.15, 1.29) for moderate cold temperature (10th percentile). | [39] |
| Kang et al. (2020) | 31 provinces in China | 2012–2015 | 451,770 | Blood pressure | An overall 10°C decrease in ambient temperature was statistically associated with 0.74 mmHg (95% CI: 0.69, 0.79) and 0.60 mmHg (95% CI: −0.63, −0.57) rise in systolic and diastolic blood pressure, respectively. | [52] |
| Lavigne et al. (2021) | Toronto, Canada | 2002–2010 | 292,666 | CVD morbidity | The effect of extreme cold temperatures (1st percentile of temperature distribution vs. 25th percentile) on CVD emergency room visits was stronger for individuals with comorbid cardiac (REM = 1.47; 95% CI: 1.06, 2.23) and kidney diseases (REM = 2.43; 95% CI: 1.59, 8.83). | [58] |
| Fonseca-Rodríguez et al. (2021) | Sweden | 1991–2014 | 1,630,189 | CVD hospitalization | Moist and very cold weather was related to a delayed increase in cardiovascular hospitalizations. | [21] |
CVD, cardiovascular disease; CI, confidence interval; RR, relative risk; YLL, years of life lost; IRR, Incidence rate ratios; REM, relative effect modification.
3 Mechanisms linking low ambient temperature and CVD
The pathophysiological mechanisms underlying the association between low ambient temperature and increased CVD morbidity and mortality are multifaceted. Firstly, studies in both humans and animals have provided evidence that that exposure to cold triggers increased activity of the sympathetic nervous system (SNS) and renin-angiotensin system (RAS). This results in elevated levels of norepinephrine, angiotensin-II, and catecholamines in the bloodstream, which subsequently induce peripheral vasoconstriction, reduces heart rate variability, and elevates heart rate and blood pressure[15–16,64,65,66,67,68]. These physiological responses can impact blood supply to the aorta media, deteriorate the aortic artery wall, and contribute to coronary plaque instability, arrhythmias, and coronary spasms, thereby increasing the risk of cardiovascular events[16,19,69]. Secondly, cold exposure can lead to dehydration by increasing urinary voiding and decreasing peripheral circulation, which further exacerbates blood viscosity, electrolyte imbalances, and acid-base imbalances. These factors contribute to the overall burden of CVD[12,70]. Thirdly, the elevation of circulating cardiac troponin I, muscle myoglobin, and endothefin-1 in response to cold exposure indicates potential damage to cardiomyocytes[65]. Furthermore, low ambient temperatures have been associated with abnormal plasma levels of fibrinogen, uric acid, matrix metalloproteinase-9, adiponectin, and lipid profiles[64,70,71,72], all of which can contribute to cardiovascular risks. Finally, cold-induced vascular dysfunction may also facilitate the development of CVD[73]. These various mechanisms highlight the complex interplay between low ambient temperature and cardiovascular health. Further research is needed to fully elucidate these mechanisms and their implications for clinical management and preventive strategies.
The molecular mechanisms underlying the link between low ambient temperature and CVD involve both cardiovascular and extra-cardiovascular effects. Firstly, cold exposure can induce an increase in macrophage infiltration and inflammation in the lung and pulmonary arterial (PA) system, leading to PA remodeling and right ventricle hypertrophy[74]. Secondly, cold-related epigenetic changes are a key factor in the development of CVD. For instance, cold exposure has been shown to up regulate hypertrophy-related miR-328 in the heart[75], while reducing the expression of the endothelial function-related miR-292-3p in the mouse aorta[73]. Thirdly, cold temperatures can alter the plasma lipid profile and enhance the growth and instability of atherosclerotic plaques in individuals with preexisting atherosclerotic lesions. This effect may be attributed to increased cholesterol synthesis and hydroxymethylglutaryl-coenzyme A reductase (HMG-CoA reductase) activity, leading to the accumulation of atherosclerosis-prone lipids. Additionally, cold exposure can activate adipose uncoupling protein 1 (UCP1), contributing to these lipid-related effects[76–77]. Furthermore, cold exposure can promote inflammatory responses[78], disrupt prooxidant-antioxidant imbalance[79–80], perturb Ca2+ homeostatic imbalance, affect mitochondrial function disarray, induce ferroptosis, and contribute to adverse cardiac hypertrophy, cardiac fibrosis, and cardiac remodeling[81,82,83,84,85]. These various mechanisms demonstrate the established link between low ambient temperature and CVD, although the precise biological mechanisms involved require further investigation. Fig. 1 provides a visual representation of the underlying mechanisms linking low ambient temperature to cardiovascular morbidity and mortality.
Potential mechanisms linking low ambient temperature to cardiovascular morbidity and mortality
PA, pulmonary arterial; BAT, brown adipose tissue; SNS, sympathetic nervous system; RAS, renin-angiotensin system.
4 Can cold adaptation be a viable strategy for cardioprotection?
Numerous studies have identified potential therapeutic targets for cold-related CVD. For example, inhibitingendothelin-1 has shown promise in ameliorating cold-induced cardiac hypertrophy and hypertension[86]. Oral supplementation of probiotics, such as A. muciniphila, has been found to mitigate the pro-atrial fibrillation properties induced by cold exposure by ameliorating gut microbiota dysbiosis[87]. In addition, natural bioactive compounds like ginsenoside Rc[78] and resveratrol[75], have demonstrated the ability to prevent acute and chronic cardiomyocyte injury caused by low ambient temperature exposure. However, these findings are primarily based on animal studies and have not been validated in human subjects. Notably, a time-stratified case-crossover study conducted in Queensland, Australia from 1995 to 2016 revealed a decreasing trend of cold temperatures on cardiovascular hospitalization[88]. Similarly, in Shanghai, China, a clear downward trend in daily CVD mortality associated with low ambient temperatures was observed between1981 and 2012[89]. Spain also experienced a decline in extreme cold-related mortality from 2004 to 2013 compared to the period of 1993 to 2002[90]. These epidemiological studies suggest that individuals may adapt to the impacts of cold temperatures, although the specific reasons for this adaptation remain unclear. While cold adaptation presents a potentially effective strategy for mitigating the adverse effects of cold, it is necessary to explore ways to enhance individuals' ability to adapt to low ambient temperature exposure in the context of climate change. An animal study found that chronic cold exposure-induced cold acclimation, reducing the ambient temperature by 1.5°C every other day until 4°C on day 25 and maintaining it for 4–6 days, attenuated impairment in cardiac function during subsequent acute cold exposure[91]. However, it is worth noting that prolonged cold acclimation (4°C for 4 weeks) could accelerate the development of atherosclerotic lesions[76]. Additionally, winter swimming, which combines cold exposure with physical activity, has shown to enhance cold adaptation and benefit cardiovascular health. However, individuals with pre-existing cardiovascular conditions or those unaccustomed to cold exposure may be more susceptible to adverse effects[92]. Therefore, achieving optimal cold adaptation depends on multiple factors, including the patterns of cold acclimation, duration of acclimation period, intensity and frequency of cold exposure, and the underlying mechanisms of adaptation. Special attention should be given to the impact on vulnerable populations.
5 Conclusions
In conclusion, this review has examined the epidemiological and laboratory evidence supporting the adverse health effects of low ambient temperature on cardiovascular system. We have discussed the underlying pathophysiological and molecular mechanisms that contribute to the increased burden of CVD in response to cold exposure. Additionally, we have explored the potential of cold adaptation strategies for cardioprotection. However, several important issues warrant further investigation. Firstly, there is a need to establish a clear definition of “low ambient temperature” to facilitate accurate and standardized research in this area. Secondly, it is crucial to determine whether the observed effects of low ambient temperature on CVD represent a causal relationship across the entire temperature range. Further studies are required to elucidate the dose-response relationship between temperature and cardiovascular health outcomes. Moreover, future epidemiological studies should carefully consider and account for major confounding factors associated with climate, such as wind speed, humidity, and barometric pressure. These factors can significantly influence the relationship between temperature and cardiovascular health, and their inclusion in analyses would enhance the accuracy and reliability of research findings. Ultimately, we hope that the solutions to the issues mentioned above will provide policymakers with direct evidence to inform decision-making regarding climate change and its impact on human health. By better understanding the mechanisms and implications of low ambient temperature on the cardiovascular system, we can develop effective strategies to mitigate the adverse health effects and protect vulnerable populations.
Author contributions
Zhang G Q, Liu C Q and Sun Q H drafted the manuscript; Liu C Q and Sun Q H provided the funding.
Conflicts of interests
The authors declare no competing financial interests.
Acknowledgments
This study was supported by the National Natural Science Foundation of China (grant # 81973001) and the Zhejiang Chinese Medical University Startup Fund.
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