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Obstetrics & Gynecology 2000;96:689-695
© 2000 by The American College of Obstetricians and Gynecologists
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ORIGINAL RESEARCH

Season and Outdoor Ambient Temperature: Effects on Birth Weight

L. J. MURRAY, MD, D. P. J. O’REILLY, MB, N. BETTS, PhD, C. C. PATTERSON, PhD, G. DAVEY SMITH, PhD and A. E. EVANS, MD

From the Departments of Epidemiology and Public Health, Health and Social Care Research Unit, Department of Geography, The Queens University of Belfast, Belfast, and the Department of Social Medicine, The University of Bristol, Bristol, United Kingdom.

Address reprint requests to: Liam J. Murray, MD Queen’s University Department of Epidemiology and Public Health Mulhouse Building, Royal Group of Hospitals Grosvenor Road Belfast, BT12 6BJ United Kingdom E-mail: l.murray{at}qub.ac.uk


   Abstract
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Abstract
Materials and Methods
 Results
 Discussion
 References
 
Objective: To determine the extent to which meteorologic factors explain seasonality in birth weight in a developed country.

Methods: Recorded birth weights were collected for all singleton live births after 36 weeks of pregnancy in Northern Ireland between 1971 and 1986. Data on daily maximum and minimum temperatures, rainfall, and hours of bright sunshine were obtained from a local climatologic station for the same period. For each birth, mean daily maximum and minimum temperatures, rainfall, and hours of bright sunshine were calculated for the trimesters of the pregnancy. Linear regression models were constructed with birth weight as the dependent variable and month of birth as a predictor variable. Months of birth were entered in the models as dummy variables. Adjustment was made for year of birth, duration of gestation, maternal age, number of previous pregnancies, sex, and social class of infants at birth and for meteorologic variables relating to each trimester.

Results: A clear seasonal pattern in birth weight was observed, with lowest mean birth weight in late spring and summer. Adjusted mean birth weights were 25.5 g, 29.6 g, and 31.6 g lower in May, June, and July, respectively, than in January. This seasonal variation occurred in both sexes, and in female births, it disappeared almost entirely after adjustment for mean daily maximum temperature during the second trimester of pregnancy.

Conclusion: Infants born during late spring and summer are lighter than those born in winter, which might be the result of exposure to low winter temperatures during midgestation. Pregnant women should keep themselves warm during midpregnancy.

With the advent of the "fetal origins hypothesis of adult cardiovascular disease,"1 the intrauterine period, previously the domain of obstetricians and embryologists, has been scrutinized in such disciplines as epidemiology, endocrinology, and adult medicine. Birth weight has become significant well beyond the perinatal period. There is renewed interest in determinants of birth weight, in the hope that unknown modifiable factors might be identified and prove useful for preventing heart disease and other chronic diseases.

In this context, we investigated the effect of season on birth weight. Seasonality in birth weight is recognized in populations in the underdeveloped world, where it is probably the product of seasonal variation in food availability and infections, such as malaria.2,3 Birth weight in developed populations has been inconsistently related to season; some4,5 but not all investigators6 have found seasonal patterns. Confirming seasonality in birth weight in a developed population and understanding any contributing factors might provide new insights into growth in utero that will be valuable to many disciplines. We investigated whether birth weight was seasonal in Northern Ireland and the nature of the relation between fetal growth and climate by estimating individual exposure to meteorologic factors during specific periods of gestation.


   Materials and Methods
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Abstract
 Materials and Methods
Results
 Discussion
 References
 
Computerized records of residents of Northern Ireland born between 1971 and 1986 were collected from the Department of Health and Social Sciences (Northern Ireland). After removing 156 duplicates, the data set contained information on 447,499 births to Northern Irish mothers. The birth register maintained by the Office of the Registrar General, Northern Ireland, contained 448,587 births for the same period. Information from the birth records included pregnancy outcome (live or stillbirth), sex of infant, gestational age, birth weight, mother’s age, number of previous pregnancies, and social class at birth (coded on the father’s occupation). Data on smoking during pregnancy were not available.

Singleton live births after 36 completed weeks of pregnancy (n = 418,817) were identified within the data set; all subsequent analyses were limited to that group. Data were complete for outcome of pregnancy, sex of infant, and gestational age. Birth weight, mother’s age, number of previous pregnancies, and social class at birth were missing for 0.3%, 0.2%, 7.2%, and 3.9% of records, respectively. Complete data were available for 386,494 births. Social class was categorized as armed forces, students, and unemployed; academics, professionals, and managers; clerical workers or skilled manual workers; and semi-skilled or unskilled manual workers.

Meteorologic data were collected from the climatologic station at Armagh, in the south of the province. Data on daily maximum and minimum temperatures (°C), rainfall (mm), and hours of bright sunshine were obtained for the period 1970–1986. Mean monthly climatic factors at this lowland station deviate little from the United Kingdom Meteorologic Office computed values for Northern Ireland as a whole.

Dates of the women’s last menstrual periods were estimated for each birth by using duration of gestation and date of birth. Mean daily maximum and minimum temperature, rainfall, and hours of bright sunshine were calculated for the first, second, and third trimesters of each pregnancy by using the estimated dates of the last menstrual periods, and meteorologic and birth weight files were merged.

Linear regression models were constructed with birth weights as dependent variables and months of birth (ie, January, February) as predictor variables. Months of birth were entered in the models as 11 dummy variables and the four social class categories as three dummy variables. In the initial models, variables that could plausibly be expected to affect birth weight for data available were included as independent variables. These were duration of gestation, maternal age, number of previous pregnancies, sex (in the models including both sexes), social class at birth, and date of birth (entered as month of birth from January 1971 to December 1986). Sex-specific models were constructed by adding, as independent variables, the meteorologic variables that related to each trimester. Separate models were constructed for each meteorologic variable.

The years between 1971 and 1986 were ranked according to mean highest daily maximum temperature during winter months (November, December, and January). Using data from the warmest 8 years and the coldest 8 years separately, the basic model was then constructed and adjusted for highest daily maximum temperature in the second trimester.


   Results
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Abstract
 Materials and Methods
 Results
Discussion
 References
 
The distributions of key variables are shown in Table 1Go. Mean birth weights increased from 1971 to 1986 (Figure 1Go) at a rate of 0.76 g per month (Table 2Go). The mean birth weight of males was higher than that of females. Birth weight increased with maternal age and number of previous pregnancies, and a social class gradient in birth weight was found; the highest mean birth weight was seen in infants whose fathers had professional or academic, or managerial occupations (Table 2Go). A clear seasonal pattern in birth weight was observed (Figure 2Go, Table 2Go): The lowest mean birth weight occurred in late spring and summer months. Adjusted mean birth weights were 25.5 g, 29.6 g, and 31.6 g lower in May, June, and July, respectively, compared with January. Pregnancies that corresponded to those births had their second trimesters in winter. A similar pattern was observed across all social class categories (data not shown).


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  		Table 1. Key Variables Included in the Linear Regression Models
 


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  		Figure 1. Monthly trend in mean birth weight in Northern Ireland from 1971 to 1986.

 

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  		Table 2. Initial Linear Regression Model (Sexes Combined): Dependent Variable Birth Weight, No Adjustment for Meteorologic Variables
 


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  		Figure 2. Mean birth weight (both sexes) by month of birth, before and after adjustment for mean daily maximum temperature and mean hours of bright sunshine in the second trimester.

 
Adding rainfall, hours of bright sunshine, or mean daily minimum temperature in any trimester, or mean daily maximum temperature in the first or third trimesters, to the model did not alter the seasonal pattern of birth weight. However, adjustment for mean daily maximum temperature in the second trimester substantially reduced it (Figure 2Go). This pattern was much more clear in females than males (Table 3Go). The mean birth weights of females born in March, April, May, June, and July were 22.4 g, 17.3 g, 27.3 g, 27.6 g, and 36.1 g lower, respectively, than those of females born in January. These differences were statistically significant (P <.001), but they did not remain so after adjustment for mean daily maximum temperature during the second trimester. Seasonal differences in birth weight were slightly less marked in males and remained, especially for the months of June and July, after adjustment for mean daily maximum temperature during the second trimester. In females, an increase of 1C in the mean daily maximum temperature during the second trimester was associated with an increase in mean birth weight of 3.5 g.


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  		Table 3. Sex-Specific Linear Regression Models With Birth Weight as the Dependent Variable, Unadjusted and Adjusted for Meteorologic Variables
 
The seasonal pattern and the effect of adjustment for mean daily maximum temperature in the second trimester were most marked in the years with the coldest winters (Figure 3Go), indicating that exposure to low winter temperature during midgestation might underlie the seasonal variation in fetal growth.



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  		Figure 3. Mean birth weight (both sexes) by month of birth in coldest and warmest winters, before and after adjustment for mean daily maximum temperature in the second trimester.

 

   Discussion
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Abstract
 Materials and Methods
 Results
 Discussion
References
 
We found a seasonal pattern in birth weight in a developed country; the lowest birth weights were seen in infants born in late spring and early summer. This pattern was not explained by seasonality in gestational age. Investigators in Denmark ( Wohlfahrt J, Meybye M, Christens P, Andersen AM, Hjalgrim H. Lancet 1998;352:1990[Medline]), New York,5 Finland,7, and Japan4,8 also found seasonality in birth weights, but with the exception of the Japanese study,8 the patterns might have resulted from seasonality in gestational age. As in our study, the Japanese investigators observed a decrease in mean birth weight in summer, although the pattern was bimodal, with a smaller decrease in mean birth weight during the winter. Other investigators did not find seasonality in birth weight in Canada,6 but their study was not large enough to detect a small effect. Some previous studies considered whether meteorologic factors might have contributed to seasonality in birth weight,7,8 but did not attempt to estimate temperature exposure individually. When we did so, we found that the seasonal distribution of birth weight in females was largely explained by the outdoor ambient temperature to which mothers might have been exposed during their second trimesters.

Our findings might be artifactual, as suggested by the apparent inconsistency between the sexes which, at present, defies explanation. Sex difference in sensitivity of prenatal growth to environmental insult, eg, nutritional deprivation or smoking, has been infrequently investigated, and no consistent evidence of a difference has been found.9,10 Our findings might be real because the association was specific for daily maximum temperature, which is likely to be a better proxy for actual temperature exposure than daily minimum temperature (which usually occurs at night). The association was seen in the second trimester, a period of rapid fetal weight gain. Animal experiments also seem to provide parallels. For example, high ambient temperature during gestation was associated with increase birth weight in pigs11; however the converse—that low temperature is associated with low birth weight—has not been directly shown.

Adults increase their total energy and carbohydrate intake in autumn,12 and Godfrey et al13 found that high energy intake, particularly of carbohydrates, in early pregnancy (first and early second trimesters) is associated with low birth weight. Other investigators did not replicate that finding,14 and did not show any relation between intake of macronutrients during pregnancy and subsequent fetal or placental weight. However, they observed a positive relation between intake of vitamin C in early pregnancy and birth weight.14 It is possible that the association we found is the product of seasonality in vitamin C intake. Any association between vitamin C intake and birth weight might be confounded by season and exposure to low temperature during pregnancy.

Several other processes might operate during winter and have detrimental effects of fetal growth, eg, exposure to infections, decreased physical activity, increased exposure to environmental smoke,15 or increased pregnancy-induced hypertension.16 Such factors might underlie the seasonal birth weight pattern, which cannot be excluded with any certainty because the necessary data are not available (which is a limitation of our study). However, if seasonal variation in such factors is important, then meteorologic data, which vary by season, would act as proxies for those factors. It might then be expected that the seasonal birth weight pattern would be attenuated when any of the meteorologic factors, not just daily maximum temperature, were included in the models. That might be particularly so for hours of sunlight, which in Northern Ireland varies more by season from mean annual rates than does daily maximum temperature.17

Exposure to low temperature in the second trimester might directly result in low birth weight. Fetal growth appears to be influenced predominantly by the rate of uteroplacental blood flow rather than by the concentration of nutrients in intervillous blood.18 Exposure to low temperature raises plasma levels of fibrinogen,19 increases blood viscosity,20 and might induce vascular constriction in the placenta, diminishing uteroplacental blood flow and reducing fetal growth. Similar mechanisms appear to underlie low birth weight at high altitude.21

We observed a modest effect of temperature on birth weight, but Northern Ireland, with its midlatitude oceanic position on the western edge of a land mass, benefits in winter from the moderating influence of the North Atlantic Drift and rarely experiences extremes in temperature. The effect of climate on birth weight might be greater in countries that have more severe winters. Outdoor ambient temperature is, at best, a poor proxy for actual individual exposure to low temperature. If it were possible to record individual exposure to temperature during the second trimester, a stronger relation with birth weight might be seen.

Our findings require replication in populations in other developed countries, and the modest reduction in birth weight that might result from exposure to low temperature during the second trimester might be of limited clinical significance in the perinatal period or later in life. However, it seems reasonable to recommend that pregnant women keep themselves warm during midpregnancy, especially if they are at risk of premature delivery or having a small-for-gestational-age infant.


   Footnotes
 
Acknowledgments: The authors thank the Department of Health and Social Services (Northern Ireland) for providing birth records and Mr. J. McFarland, Armagh Observatory, for providing meteorologic data. During this work, Dr. Murray was employed as a Specialist Registrar in Public Health Medicine by the Eastern Health and Social Services Board (Northern Ireland).

PII S0029-7844(00)01022-X

Received October 27, 1999. Received in revised form June 19, 2000. Accepted July 7, 2000.


   References
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Abstract
 Materials and Methods
 Results
 Discussion
 References
 
1. Barker DJP, ed. Mothers, babies, and disease in later life. London: British Medical Association, 1994.

2. Bantje H. Seasonality of births and birth weights in Tanzania. Soc Sci Med 1987;24:733–9.

3. Hort KP. Seasonal variation of birth weight in Bangladesh. Ann Trop Paediatr 1987;7:66–71.[Medline]

4. Matsuda S, Sone T, Doi T, Kahyo H. Seasonality of mean birthweight and mean gestational period in Japan. Hum Biol 1993;65: 481–501.[Medline]

5. Selvin S, Janerich WT. Four factors influencing birthweight. Br J Prev Soc Med 1971;25:12–6.[Medline]

6. Fallis G, Hilditch J. A comparison of seasonal variation in birthweights between rural Zaire and Ontario. Can J Public Health 1989;80:205–8.[Medline]

7. Rantakallio P. The effect of a northern climate on seasonality of births and the outcome of pregnancies. Acta Paediatr Scand 1971;218:S1–67.

8. Matsuda S, Hiroshige V, Furuta M, Doi T, Sone T, Kahyo H. Geographic differences in seasonal variation of mean birthweight in Japan. Hum Biol 1995;67:641–56.[Medline]

9. Antonov AN. Children born during the siege of Leningrad in 1942. J Pediatr 1947;30:250–9.

10. Davies DP, Gray OP, Elwood PC, Abernethy M. Cigarette smoking in pregnancy: Associations with maternal weight gain and fetal growth. Lancet 1976;385–7.

11. Prunier A, Dourmad JY, Etienne M. Effect of light regimen under various ambient temperatures on sow and litter performance. J Anim Sci 1994;72:1461–6.[Abstract]

12. de Castro JM. Seasonal rhythms of human nutrient intake and meal pattern. Physiol Behav 1991;50:243–8.[Medline]

13. Godfrey K, Robinson S, Barker DJP, Osmond C, Cox V. Maternal nutrition in early and late pregnancy in relation to placental and fetal growth. BMJ 1996;312:410–4.[Abstract/Free Full Text]

14. Mathews F, Yudkin P, Neil A. Influence of maternal nutrition on outcome of pregnancy: a prospective cohort study. BMJ 1999;319: 339–43.[Abstract/Free Full Text]

15. Ronchetti R, Bonci E, de Castro G, Signoretti F, Macri F, Ciofetta GC, et al. Relationship between cotinine levels, household and personal smoking habit and season in 9–14 year old children. Eur Respir J 1994;7:472–6.[Abstract]

16. Bider D, Sivan E, Seidman DS, Dulitzky M, Mashiach S, Serr DM, et al. Meteorological factors in hypertensive disorders, vaginal bleeding and premature rupture of membranes during pregnancy. Gynaecol Obstet Invest 1991;32:88–90.

17. Betts NL. 1997 climate. In: Cruickshank JG, ed. Soil and environment: Northern Ireland. Belfast: Agricultural and Environmental Science Division, DANI and the Agricultural Service Department, The Queen’s University of Belfast, 1997:63–84.

18. Vorherr H. Factors influencing fetal growth. Am J Obstet Gynaecol 1982;142:577–88.[Medline]

19. Neild PJ, Syndercombe-Court D, Keatinge WR, Donaldson GC, Mattock M, Caunce M. Cold-induced increases in erythrocyte count, plasma cholesterol and plasma fibrinogen of elderly people without a comparable rise in protein C or factor X. Clin Sci 1994;86:43–8.[Medline]

20. Keatinge WR, Coleshaw SRK, Cotter F, Mattock M, Murphy M, Chelliah R. Increases in platelet and red cell counts, blood viscosity and arterial pressure during mild surface cooling: Factors in mortality from coronary and cerebral thrombosis in winter. BMJ 1984;289:1405–8.

21. Jensen GM, Moore LG. The effect of high altitude and other risk factors on birthweight: Independent or interactive effects? Am J Public Health 1997;87:1003–7.[Abstract/Free Full Text]




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