Associations between extreme temperature exposure and hypertensive disorders in pregnancy: a systematic review and meta-analysis

Figures & data

Figure 1. PRISMA flow diagram: preferred reporting items for systematic reviews and meta-analyses.

Table 1. Characteristics of the included studies on ambient temperature and HDP.

Author	Country	Study design	Year(s) of study	Subgroup(s) of HDP	HDP (n)	Total women(n)	Definition of HDP	NOS score
2022 Chérie (30)	South Africa	Retrospective cohort	2017–2018	HDP excluding preeclampsia or eclampsia Preeclampsia or eclampsia	432 412	7,986	ACOG	9
2022 Zhao (31)	China	Retrospective cohort	2016–2017	Preeclampsia	1,213	1,213	The codes of ICD 10	9
2020 Xiong (22)	China	Retrospective cohort	2013–2016	Gestational hypertension	23,704		ACOG, without other recorded obstetric complications or medical complications	9
				Preeclampsia or eclampsia	38,166	2,043,182
				Superimposed eclampsia	1,940
2020 Shashar (25)	Israel	Retrospective cohort	2004–2013	Preeclampsia	2,617	64,566	The codes of ICD 9	9
2017 Auger (26)	Canada	Case control studies	1989–2012	Preeclampsia	65,273	1,890,711	ISSHP, ICD	9
2014 Nasiri (27)	Iran	Retrospective cohort	2002–2008	Preeclampsia	262	20,332	ACOG	7
2014 Morikawa (36)	Japan	Retrospective cohort	2005–2009	HDP	13,848	301,510	ACOG	7
2014 Melo (37)	Brazil	Retrospective cohort	2000–2006	HDP	5,051	20,125	ACOG	7
2014 Kausar (38)	Pakistan	Retrospective cohort	2008–2012	Eclampsia	579	31,331	ACOG	7
2008 Tam (39)	China	Retrospective cohort	1995–2002	Preeclampsia	245	15,402	ISSHP, singleton primiparous pregnancies with preeclampsia	9
2008 Imminki (40)	Netherlands	Retrospective cohort	2002–2003	Preeclampsia	1,329	11,585	ISSHP, The preeclampsia, eclampsia and HELLP syndrome patients together were called the pre-eclampsia group.	9
1999 Makhseed (41)	Kuwait	Retrospective cohort	1992–1994	HDP and Preeclampsia	1,457	28,262	ACOG	7
1993 Neela (42)	India	Retrospective cohort	1987–1988	Eclampsia	126	7,374	Unclear	7
1992 Bergström (43)	Mozambique	Retrospective cohort	1984	Eclampsia	70	37,469	Unclear	7
1988 Alderman (44)	USA	Case control studies	1980–1982	Eclampsia	153	840	Unclear, singleton pregnancies with eclampsia	9

Abbreviations: HDP: Hypertensive Disorders in Pregnancy; NOS: Newcastle-Ottawa Scale; ACOG: American College of Obstetricians and Gynecologists; ISSHP: International Society for the Study of Hypertension in Pregnancy; ICD: International Classification and Disease.

Table 2. Summary of temperature exposure data, statistical methods and results.

Author	Temperature Source	Measurement	Exposure time window	Method	Adjusted factors	Outcome				Conclusion
						HDP and subgroups	Category Extreme temperature		Mean temperature
2022 Chérie (30)*	Johannesburg, South Africa	Weekly mean temperature (cold and heat temperatures were defined as the 5th and 95th percentiles of daily mean temperature.	(1) early pregnancy (2–5 weeks’ gestation)(2) Late pregnancy(29 weeks after conception)	Cox proportional hazards regression analyses	season of conception, season of birth, maternal age, ethnicity (PEH model only), parity, gravidity, and HIV status.	HDP excluding preeclampsia or eclampsia	early pregnancy HR(95%CI) Heat 1.36 (0.84–2.19) Cold 1.01 (0.60–.69) Late pregnancy Heat 1.00 (0.77–1.29) Cold 1.86 (1.36–2.53)		None	Early pregnancy: Cold exposure had no association. Late pregnancy: Cold exposure increased risk. Heat exposure had no association at any time during gestation.
						Preeclampsia or eclampsia	early pregnancy HR(95%CI) Heat 1.79 (1.19–2.71) Cold 1.18 (0.70–1.95) Late pregnancy Heat 0.86 (0.70–1.04) Cold 1.52 (1.13–2.04)			Early pregnancy: Heat temperature increased risk, cold exposure had no association Late pregnancy: Heat exposure decreased risk and cold temperature increased risk.
2022 Zhao (31)*	Nanjing, China	(1) Daily minimum and maximum temperatures a. very cold(10th percentile) b. cold (25th percentile) c. hot(75th percentile) d. very heat (90th percentile) 2. Daily mean temperatures	after 20 w (time of delivery)	The distributed lag nonlinear model (DLNM)	relative humidity, SO2,NO2, CO, O3, PM10 and PM2.5	Preeclampsia	after 20 w RR(95%CI) Very cold 1.65 (1.07–2.54) Cold 1.55 (1.10–2.19) Heat 0.64 (0.48–0.87) Very heat 0.64 (0.44–0.94)		RR(95%CI) 1.73 (1.06–2.83) 1.62 (1.14–2.29) 0.68 (0.50–0.91) 0.64 (0.43–0.97)	after 20 w: Heat exposure decreased the risk, cold exposure increased the risk.
2020 Xiong (22)*	Chinese mainland, at the county level,	1.extreme temperatures a. very cold(<5th percentile) b. moderate cold (5th −10th percentile) c. moderate heat(90th − 95th percentile) d. very heat (>95th percentile)2. Weekly mean temperature (°C)a. very cold (−17.2°C)b. Very heat (29.5°C)	1.p12 (12 weeks before conception) 2.w1–20 (20 weeks after conception)	1.extreme temperatures: a logistic regression; 2.average temperature (weekly): pooled cumulative exposure–response curves	region, hospital level, number of antenatal visits, maternal education, marital status, maternal age, parity, number of fetuses, elevation, humidity, and air pollution exposure.	Gestational hypertension	p12 Very cold Moderate cold Moderate heat Very heat w1–20 Very cold Moderate cold Moderate heat Very heat	OR (95%CI) 1.28 (1.14–1.43) 1.06 (0.97–1.16) 0.88 (0.81–0.95) 0.91 (0.83–0.98) 0.87 (0.80–0.94) 0.80 (0.75–0.87) 1.19 (1.12–1.28) 1.10 (1.03–1.17)	aOR (95%CI) 1.86 (1.62–2.14)--0.79 (0.74–0.85) 0.53 (0.44–0.62)--1.29 (1.21–1.38)	p12: Heat exposure decreased the odds of gestational hypertension, cold exposure increased the odds of preeclampsia or eclampsia and gestational hypertension. w1–20: Heat exposure increased the risk of preeclampsia or eclampsia and gestational hypertension, and it was opposite in cold exposure. No significant association was observed between temperature and superimposed preeclampsia
						Preeclampsia or eclampsia	p12 Very cold Moderate cold Moderate heat Very heat w1–20 Very cold Moderate cold Moderate heat Very heat	OR (95%CI) 1.22 (1.12–1.32) 0.98 (0.91–1.05) 0.94 (0.88–1.01) 0.96 (0.89–1.02) 0.89 (0.84–0.94) 0.86 (0.81–0.92) 1.13 (1.07–1.19) 1.16 (1.11–1.22)	aOR (95%CI) 1.44 (1.29–1.61)--0.91 (0.86–0.96) 0.61 (0.54–0.69)--1.23 (1.16–1.30)
						Superimposed eclampsia	p12 Very cold Moderate cold Moderate heat Very heat w1–20 Very cold Moderate cold Moderate heat Very heat	OR (95%CI) 0.86 (0.62–1.20) 0.85 (0.60–1.21) 1.06 (0.83–1.37) 1.01 (0.78–1.32) 1.20 (0.89–1.60) 1.25 (0.95–1.65) 0.98 (0.80–1.25) 1.00 (0.77–1.31)	aOR (95%CI) 1.26 (0.68–2.33)--1.03 (0.77–1.37) 1.14 (0.56–2.32)--0.93 (0.68–1.28)
2020 Shashar (25)	Southern Israel	Daily mean temperature (°C) a. heat (>25°C) b. cold (≤25°C)	1.w1–12 (first trimester) 2.w13–24 (second trimester) 3.After 24 w (third trimester)	generalized estimating equation (GEE) Poisson multivariable regression models	maternal age, gravidity, multiple pregnancies and a history of preeclampsia in past deliveries	Preeclampsia, Bdouin-Arab ethnicity	w1–12 heat cold w13–24 heat cold after 24 w heat cold	RR (95%CI) 2.91 (1.98–4.28) 0.68 (0.49–0.94) 0.83 (0.60–1.15) 0.90 (0.73–1.13) 2.37 (1.75–3.20) 0.62 (0.44–0.87)	None	w1–12 and after 24 w: Heat exposure increased risk. w1–12 and after 24 w: Cold exposure decrease the risk. w13–24: No significant association was observed.
						Preeclampsia, Jewish ethnicity	w1–12 heat cold w13–24 heat cold after 24 w hot cold	RR (95%CI) 2.38 (1.50–3.80) 1.01 (0.69–1.47) 0.90 (0.61–1.33) 1.22 (0.96–1.57) 1.94(1.34–2.81) 0.89 (0.60–1.34)
2017 Auger (26)*	Quebec from Environment Canada.	Monthly mean temperature (°C) a.Heat (20°C) b.Cold (−15°C)	1.w1–4 (4-week exposure window after conception) 2.after 27 w (4-week exposure window before delivery)	log-binomial regression models	maternal age, preexisting diabetes, parity, socio-economic deprivation, place of residence, period and humidity	Preeclampsia	w1–4 Heat Cold After 27 w Heat Cold	RR (95%CI) 1.08 (1.06–1.11) 0.97 (0.93–1.01) 0.85 (0.82–0.88) 1.01 (0.96–1.03)	None	w1–4: Heat exposure increased the risk and and cold exposure decreased the risk. after 27 weeks: It was opposite.
2014 Nasiri (27)	Iran	Monthly mean temperature (°C)	1. w1–4 (time of conception) 2.after 20 w (time of delivery)	Duncan’s test, Multivariable logistic regression	unclear	Preeclampsia	w1–4	None	p=0.0001 (regression line inclination: 0.071 ± 0.01)	w1–4: Heat exposure increased the risk and cold expoure decreased the risk. after 20 w: No significant relationship.
2014 Morikawa (36)	Tokyo	Monthly mean temperature (°C)	1. w1–4 (time of conception) 2.after 22 w (time of delivery)	Bonferroni’s method., t-test	unclear	HDP	w1–4	No significant relationship	None	w1–4: No significant relationship. after 22 w: Heat exposure decreased the risk, cold exposure had no effect.
							after 22 w	the incidence of HDP was lowest in hot temperature (p<0.05)
2014 Melo (37)	Recife, Brazil	Monthly mean temperature (°C)	after 20 w (time of delivery)	Pearson’s correlation coefficient	unclear	HDP	after 20 w	None	p=0.046 (r = −0.26)	Heat exposure decreased the risk, cold exposure increased the risk.
2014 Kausar (38)	Pakistan	Monthly maximum temperature (°C)	after 20 w (time of delivery)	Pearson’s correlation coefficient	unclear	Eclampsia	after 20 w	p<0.05 (r = 0.516)s	None	Heat exposure increased the risk, cold exposure decreased the risk.
2008 Tam (39)	Eastern New Territories, Hong Kong	Mean heat index (°F): the daily maximum temperature; the lowest heat index: the temperature<57°F	w1–4 (time of conception)	The cross-correlation function	maternal age and fetal sex	Preeclampsia	w1–4	OR (95%CI): 2.80 (1.50–5.20)	None	Heat exposure increased the risk, cold exposure was an decreased risk.
2008 Imminki (40)	South African	Monthly minimum temperature (°C)	after 20 w (time of delivery)	logistic regressions, Wald-test statistic	maternal age, parity and fetal sex	Preeclampsia or eclampsia	after 20 w ≤8.5 8.5 to 10.5 10.5 to12.5 12.5to 14.5 14.5 to16.5	OR (95%CI) 1.00 (referent) 0.90 (0.76–1.07) 0.96 (0.81–1.14) 0.90 (0.71°C1.12) 0.62 (0.53–0.72)	None	Heat exposure decreased the risk, cold exposure increased the risk.
1999 Makhseed (41)	Kuwait	Monthly mean Temperature (°C)	after 20 w (time of delivery)	Pearson correlation and linear regression	unclear	HDP	after 20 w Hot Cold	None	Incidence (95%CI) 0.46% (0.43–0.49) 0.36% (0.34–0.39) Incidence (95%CI) 0.32% (0.29–0.36) 0.41% (0.37–0.45)	For HDP, heat exposure increased the risk, cold exposure decreased the risk. It was reverse for preeclampsia.
						Preeclampsia	after 20 w Hot Cold	None
1993 Neela (42)	India	Monthly mean temperature (°C)	after 20 w (time of delivery)	linear regression	unclear	Eclampsia	after 20 w	None	p<0.01 (r = −0.77)	Heat exposure decreased the risk, cold exposure increased the risk.
1992 Bergström (43)	Maputo	Monthly mean temperature (°C)	after 20 w (time of delivery)	Linear regression analysis, t-test	unclear	Eclampsia	after 20 w	None	p<0.005(r = −0.78)	Heat exposure decreased the risk, cold exposure increased the risk.
1988 Alderman (44)	Washington	Daily mean temperature (°C, cold temperature)	after 20 w (time of delivery)	Stratification and Mantel-Haenszel adjustment	maternal age, parity, race, and month antenatal care	Eclampsia	after 20 w ≤0 0 to 4.5 4.5 to 7.5 7.5 to 10 >10	None	OR (95%CI) 1.00(referent) 1.20(0.70–2.00) 0.80(0.50–1.50) 1.00 (0.50–1.70) 1.00 (0.50–1.70)	Cold exposure had no association with eclampsia.

Abbreviations: HDP: Hypertensive Disorders in Pregnancy; CI: confidence interval; OR, odds ratio; RR: risk ratio; HR: hazard ratio.

*means that the study made the adjustments for multiple comparisons.

Figure 2. Analysis of the associations between heat exposure and HDP by the gestational weeks of pregnancy. Green shading indicates the period of increased risk during pregnancy after heat exposure. Orange shading indicates the studies that showed a decreased risk. Yellow shading indicates that heat exposure and HDP have no association.

Figure 3. Meta-analysis of the associations between heat exposure and preeclampsia or eclampsia by the gestational weeks of pregnancy. (a) heat temperature during w1–20 vs. reference temperature; (b) 1°Cincrease during w1–20 vs. reference temperature; (c) heat temperature after 20 weeks of gestation vs. reference temperature; (d) 1°Cincrease during after 20 weeks of gestation vs. reference temperature.

Table 3. Meta-analysis results between extreme temperature exposure and preeclampsia or eclampsia during the gestational weeks.

	No of studies	Average effect size (OR (95% CI))	I^2 (%)	T^2	p value
Heat exposure during w1–20^a
Heat exposure vs. reference temperatures	4	1.54 (95% CI 1.10–2.15)	99.33	0.15	0.01
Every 1°C temperature increase	4	1.07 (95% CI 1.02–1.12)	97.20	0.00	0.00
Heat exposure after 20 weeks of gestation
Heat exposure vs. reference temperatures	4	1.05 (95% CI 0.67–1.64)	96.35	0.29	0.83
Every 1°C temperature increase	4	1.01(95% CI 0.96–1.06)	94.96	0.00	0.81
Cold exposure during w1–20
Cold exposure vs. reference temperatures	4	0.90 (95% CI 0.84–0.97)	66.34	0.00	0.01
Every 1°C temperature decrease	4	0.99 (95% CI 0.98–1.00)	86.32	0.00	0.09
Cold exposure after 20 weeks of gestation
Cold exposure vs. reference temperatures	4	1.13 (95% CI 0.84–1.53)	87.30	0.11	0.43
Every 1°C temperature decrease	4	1.02 (95% CI 0.98–1.05)	87.99	0.00	0.40

^aw-20 means the first half of pregnancy.

Figure 4. Analysis of the associations between cold exposure and HDP by the gestational weeks of pregnancy. Green shading indicates the period of increased risk during pregnancy after cold exposure. Orange shading indicates the studies that showed a decreased risk. Yellow shading indicates that the temperature and HDP have no association.

Figure 5. Meta-analysis of the associations between cold exposure and preeclampsia or eclampsia by the gestational weeks of pregnancy. (a) cold temperature during w1–20 vs. reference temperature; (b) 1°Cdecrease during w1–20 vs. reference temperature; (c) cold temperature after 20 weeks of gestation vs. reference temperature; (d) 1° decrease during after 20 weeks of gestation vs. reference temperature.

Part C, le Roux J, Chersich M, et al. Ambient temperature during pregnancy and risk of maternal hypertensive disorders: a time-to-event study in Johannesburg, South Africa. Environ Res. 2022;212(Pt D):113596.

 PubMedGoogle Scholar

Zhao T, Long W, Lu P. Short-term effects of ambient temperature on the risk of preeclampsia in Nanjing, China: a time-series analysis. Bmc Pregnancy Childbirth. 2022;22(1):539. doi: 10.1186/s12884-022-04859-w

 PubMed Web of Science ®Google Scholar

Xiong T, Chen PR, Mu Y, et al. Association between ambient temperature and hypertensive disorders in pregnancy in China. Nat Commun. 2020;11(1). doi: 10.1038/s41467-020-16775-8

 Web of Science ®Google Scholar

Shashar S, Kloog I, Erez O, et al. Temperature and preeclampsia: epidemiological evidence that perturbation in maternal heat homeostasis affects pregnancy outcome. PLoS One. 2020;15(5):e0232877.

 PubMed Web of Science ®Google Scholar

Auger N, Siemiatycki J, Bilodeau-Bertrand M, et al. Ambient temperature and risk of preeclampsia: biased association? Paediatr Perinat Epidem. 2017;31(4):267–271.

 PubMed Web of Science ®Google Scholar

Nasiri R, Shadmehri AA, Ghiassi PK, et al. Association of meteorological factors and seasonality with preeclampsia: a 5-year study in northeast of Iran. Ann Clin Exp Hypertens. 2014;36(8):586–589.

 Google Scholar

Morikawa M, Yamada T, Yamada T, et al. Seasonal variation in the prevalence of pregnancy-induced hypertension in Japanese women. J Obstetrics Gynaecol Res. 2014;40(4):926–931.

 PubMed Web of Science ®Google Scholar

Melo B, Amorim M, Katz L, et al. Hypertension, pregnancy and weather: is seasonality involved? Rev Assoc Med Bras. 2014;60(2):105–110. doi: 10.1590/1806-9282.60.02.006

 PubMed Web of Science ®Google Scholar

Malik A, Kausar S, Bashir A, et al. Seasonal trends in the occurrence of eclampsia. J SAFOG. 2014;6(2):83–87. doi: 10.5005/jp-journals-10006-1277

 Google Scholar

Tam WH, Sahota DS, Lau TK, et al. Seasonal variation in pre-eclamptic rate and its association with the ambient temperature and humidity in early pregnancy. Gynecol Obstet Invest. 2008;66(1):22–26. doi: 10.1159/000114252

 PubMed Web of Science ®Google Scholar

Immink A, Scherjon S, Wolterbeek R, et al. Seasonal influence on the admittance of pre-eclampsia patients in Tygerberg Hospital. Acta Obstet Gynecol Scand. 2008;87(1):36–42. doi: 10.1080/00016340701743066

 PubMed Web of Science ®Google Scholar

Makhseed M, Musini VM, Ahmed MA, et al. Influence of seasonal variation on pregnancy-induced hypertension and/or preeclampsia. Aust NZ J Obstetrics Gynaecol. 1999;39(2):196–199. doi: 10.1111/j.1479-828X.1999.tb03372.x

 PubMed Web of Science ®Google Scholar

Neela J, Raman L. Seasonal trends in the occurrence of eclampsia. Natl Med J India. 1993;6(1):17–18.

 PubMedGoogle Scholar

Bergström S, Povey G, Songane F, et al. Seasonal incidence of eclampsia and its relationship to meteorological data in mozambique. J Perinat Med. 1992;20(2):153–158. doi: 10.1515/jpme.1992.20.2.153

 PubMed Web of Science ®Google Scholar

Alderman BW, Boyko EJ, Loy GL, et al. Weather and occurrence of eclampsia. Int J Epidemiol. 1988;17(3):582–588.

 PubMed Web of Science ®Google Scholar

Data availability statement

Data sharing is not applicable to this article because there is no new data was created or analyzed.