(Hypertension. 2000;36:795.)
© 2000 American Heart Association, Inc.
Scientific Contributions |
Fetal Growth and Early Postnatal Growth Are Related to Blood Pressure in Adults
From the Department of Pediatrics (Y.B.C., L.L., J.K.) and the Clinical Trials Centre (Y.B.C., J.K.), University of Hong Kong, Queen Mary Hospital, Pokfulam, Hong Kong SAR, PR China; and MRC Environmental Epidemiology Unit (C.O., D.B.), Southampton General Hospital, Southampton, UK.
Correspondence to Prof Johan Karlberg, Department of Paediatrics, University of Hong Kong, Queen Mary Hospital, Pokfulam, Hong Kong SAR, PR China. E-mail jpekarl{at}hkucc.hku.hk
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Abstract |
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Abstract—It is commonly agreed that birth weight is associated with blood pressure in adults. However, not much is known about birth length, ponderal index, and early postnatal growth, whose effects on adult blood pressure, if any, can affect the interpretation of the birth weight–blood pressure association. This study examined the association between fetal growth, early postnatal growth, and blood pressure in Chinese adults. One hundred twenty-two subjects born in Hong Kong in 1967 were followed from birth to age 30 years. Multiple linear regression was used to analyze the association between size at birth, postnatal changes in body size, and systolic and diastolic blood pressure at age 30 years. Having adjusted for potential confounders and each other explanatory variable, it is found that birth length standard deviation score (regression coefficient or ß=-3.2), ponderal index at birth (ß=-1.8), and postnatal changes in ponderal index from age 6 months to 18 months (ß=-2.2) were inversely associated with systolic blood pressure (each P<0.05). Postnatal changes in length standard deviation score were not significantly associated with systolic blood pressure. Birth length standard deviation score was inversely associated with diastolic blood pressure at age 30 years (ß=-2.6; P<0.05). Other anthropometric variables were not associated with diastolic blood pressure. The results support the hypotheses that both fetal growth and early postnatal growth may have a long-term impact on blood pressure in adults. It also highlights the importance of differentiating length and weight for length.
Key Words: growth and development • body height • postnatal growth • thinness • blood pressure • Hong Kong
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Introduction |
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Studies in different populations have demonstrated an association between fetal growth and elevated blood pressure in adulthood.1 It has been suggested that fetal undernutrition at any stage of gestation can result in raised blood pressure in later life.2 Though evidence about an inverse association between birth weight and adult blood pressure is now abundant,3 there is only limited evidence about the association between birth length, ponderal index (PI), and adult blood pressure.4 Some recent studies have investigated whether postnatal growth also shows an association with blood pressure in children5 6 and with blood pressure or coronary heart disease in adults.7 8 9 This is a potentially important public health issue because appropriate postnatal care may be one way to minimize the adverse effect of disturbed fetal growth. Moreover, nutritional problems and growth faltering in the first 2 years of life are prevalent in developing countries.10 11 Any long-term consequence arising from a disturbed growth in this period can have a strong impact on population health. Catch-up growth during the first 6 months of life is often observed in babies born small.12 13 Growth faltering usually takes place from 6 to 18 months of life. Growth in the first 6 months after birth can be seen as an extension of fetal development, which is nutritionally dependent. Between the age of 6 and 12 months, the onset of the childhood phase of growth takes place, which is claimed to be growth hormone dependent.10 14 Because fetal growth and postnatal growth are related to each other, simultaneous analysis is needed to better understand their individual and combined effects.
Thinness (wasting) and shortness (stunting) at birth is usually seen as representing nutritional problems during different stages of gestation. A framework proposed by Barker15 is that thinness and shortness at birth could lead to interference in insulin and growth hormone sensitivity, respectively, in later life. Insulin resistance syndrome, which is characterized by hypertension, elevated plasma triglyceride level, and diabetes, is more specifically related to thinness than weight at birth.2 It was proposed that babies short at birth might have persisting growth hormone deficiency or growth hormone resistance.16 As such, it is desirable to differentiate the two phenomena in an empirical study. Weight is a crude measure of nutritional status that cannot differentiate between thinness and shortness.11 17
This article presents findings from a longitudinal study of 122 subjects born in Hong Kong in 1967. We investigated the associations between thinness and length at birth, changes in thinness and length between birth and 6 months of age and between 6 months and 18 months of age, and blood pressure at age 30 years. Although Hong Kong is an affluent society now, it was an overcrowded city with poor living and hygiene environment in the 1960s.18 Incidence of ill health and growth impairment in children was high.19 This background is similar to the rapid industrialization and urbanization taking place in less developed countries. The present study offers opportunities for investigating the long-term consequence of insults not only in fetal life but also during early childhood. The specific objectives were (1) to confirm the impact of length and thinness at birth on adult blood pressure and (2) to test the effects of (a) the changes in length and thinness from birth to 6 months of age and (b) the changes in length and thinness from 6 to 18 months of age on adult blood pressure.
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Methods |
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Subjects
Five hundred twenty-three ethnic Chinese babies born in two hospitals during the period from February 24 to April 1, 1967, were followed from birth to the age of 5 years by a team of pediatric researchers at the University of Hong Kong. Newborns with congenital abnormalities related to growth were excluded. Growth measurements were taken monthly during the first year, quarterly during the second and third years, and annually thereafter. In 1995, the study was reopened. Among 171 cohort members who could be located in Hong Kong, 133 agreed to participate in a follow-up assessment. Approval by the Ethics Committee, Faculty of Medicine, University of Hong Kong, as well as informed written consent from the subjects, were obtained. Detailed information was collected through interviews and clinical assessment was carried out at the university in 1997. None of the subjects were under hypertension medication at age 30 years.
Variables
Weight and length at birth, and weight and length within a
2-month interval from age 6 months and 18 months were taken for the
construction of independent variables. We converted each
measurement for weight and length at or close to 6 months and 18 months
to a gender- and age-specific standard deviation score (SDS), using a
World Health Organization (WHO)-recommended international
reference.11 20 We used a piecewise linear function to
interpolate the SDS values at 6 months and 18 months.7 The
interpolated SDS values were also back-transformed to the corresponding
weight and height values at these ages for the calculation of a weight
for height index. To reduce the problem of multicollinearity, it is
important to make measures of weight for height independent of height.
There is not a single index that can achieve this at all
ages.21 22 The PI
[PI=weight(kg)/length(m)3] was used for weight
for length at birth, at 6 months, and at 18 months. The independent
variables representing fetal growth included birth
length SDS and PI at birth. The independent variables
representing postnatal growth included change in length SDS
between birth and 6 months, change in length SDS between 6 and 18
months, change in PI between birth and 6 months, and change in PI
between 6 and 18 months. The changes were defined as values at the
recent age minus values at the previous age. For brevity, they were
referred to as 
length SDS 0 to 6 months, length SDS 6 to 18
months, PI 0 to 6 months, and PI 6 to 18 months. Birth weight and
birth length in metric form were not our focus. We provided some
information about them because we expected that some researchers would
be interested.
In the follow-up in 1997, the subjects were interviewed and examined by
a physician. The subjects had 
15 minutes of rest after arrival at the
clinic and were seated for 5 minutes before blood pressure measurement.
An automatic device (Dinamap, Critikon, Neuilly Plaisance) and a cuff
of the recommended size for the mid-upper arm circumference were used.
Three measurements were taken at 1-minute intervals. Arithmetic means
of the last 2 readings were taken for the systolic and
diastolic blood pressure outcomes.
Body mass index (BMI) was also measured at age 30 years and analyzed as a covariate. Other covariates included gender, mother’s education, mother’s health status during pregnancy, gestational age (GA, in completed weeks), and respondent’s education. Mother’s education was enumerated at birth and categorized as "no formal education/primary incomplete," "primary complete," or "secondary or above." Chronic diseases during pregnancy (eg, kidney disease, hypertension) and complications of pregnancy (toxemia) were recorded by physicians, and the mothers were classified as "healthy" versus "diseased" during pregnancy. GA was estimated according to last menstrual period. Respondent’s education level was reported in the follow-up interview and classified as "secondary" or "tertiary."
Statistical Analysis
A 
2 test and t test were
used to compare the characteristics of the cohort members included in
the analysis and the cohort members not included. Pearson
correlation (r) was used to examine the association among
independent variables. Initially, the associations between each
independent variable and adult systolic and
diastolic blood pressure were separately analyzed
by ordinary least-squares regression, adjusting for covariates. Then,
we proceeded to multiple regression models that
simultaneously analyzed fetal and postnatal growth
variables, controlling for GA and other covariates. In the
regression analysis, each gender was pooled. Interaction
between gender and the independent variables were tested.
Initially, mother’s education was analyzed as a categorical
variable. F tests showed that assuming linear effect did
not compromise goodness of fit (P>0.1), so the
analysis presented in this article treated mother’s
education as having a linear effect. Recently, there has been a
discussion on the dual effects of statistical adjustment for adult BMI.
It is well known that adjusting for adult BMI as a covariate can reduce
variation in blood pressure measures and therefore improved precision.
Lucas et al23 maintains that there is a second effect
on the interpretation of the regression coefficient of birth weight or
relative weight at birth. Briefly, birth weight (or relative weight)
adjusted for adult BMI refers to centile crossing in weight (relative
weight) from pediatric to adult age. As such, we included a
supplementary analysis without adjustment for adult BMI. To
provide a more clinical feel of the associations, we estimated the
differences in blood pressure between subjects at high (95 percentile)
and low (5 percentile) values of each significant anthropometric
variable. To check model robustness, we examined the leverage
statistics by using the criterion suggested by Hoaglin and
Welsch.24
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Results |
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Of the 133 subjects, 11 were excluded from the analysis because of missing anthropometric values. GA data were not available for 2 boys (birth weight 2.75 and 2.95 kg). A value of 39 weeks was assigned because their birth weight was within normal range. There was 1 obvious outlier (GA=47 weeks). This was replaced by a value of 42 weeks, which is the plausible upper limit. Table 1 summarizes the characteristics of the subjects. The mean birth weight was 3.1 and 3.0 kg for male and female subjects, respectively. The mean PI was 26.4 for boys and 27.0 for girls. The average birth length of either gender was 0.8 SDS shorter than that of the WHO international reference. Between the age of 6 and 18 months, a fall in the PI and height SDS was observed. There was no very early preterm birth; the lowest GA was 35 weeks. Figures 1 and 2 show the distribution of the gender-adjusted systolic and diastolic blood pressure against birth length, which is an important aspect in our study.
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The birth length and birth weight of the 400 cohort members not
included were 48.7 cm and 3.1 kg, each gender pooled. They were
virtually identical to those of the 122 participants (t
values=1.03 and 0.4, respectively; P>0.1). Mother’s
education level of the 2 groups (each gender pooled) was also similar
(2=1.43, df=2, P=0.5;
details not shown).
Birth weight was highly correlated with birth length SDS
(r=0.85; P<0.05), whereas PI at birth was
independent of birth length SDS (r=-0.08;
P>0.05). PI at birth was inversely associated with PI 0
to 6 months (r=-0.47; P<0.05) and, to a lesser
degree, with PI 6 to 18 months (r=-0.19;
P<0.05). Similarly, birth length SDS was inversely
associated with length SDS 0 to 6 months (r=-0.38;
P<0.05) and with length SDS 6 to 18 months
(r=-0.18; P<0.05).
Table 2 shows the bivariate regression coefficients of systolic and diastolic blood pressure on growth variables and GA, with adjustment for covariates. Birth weight had a significant, inverse association with systolic pressure: An increment of 1 kg in birth weight was associated with a reduction of 6.0 mm Hg (P<0.05). Birth length also had a significant, inverse association with systolic pressure. In terms of centimeters, the regression coefficient was -1.1 (P<0.05); in terms of SDS the coefficient was -2.6 (P<0.05). Other regression coefficients were not statistically significant at the 5% level. Birth length was inversely associated with diastolic pressure. The regression coefficients for birth length in centimeters and birth length SDS were -0.8 (P<0.05) and -1.9 (P<0.05), respectively. Birth weight and other variables were not significant in this regard.
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Table 3 shows the multiple
regression models for systolic and diastolic blood
pressure. Having adjusted for GA and other covariates, PI at birth
(regression coefficient or ß=-1.8), PI 6 to 18 months
(ß=-2.2), and birth length SDS (ß=-3.2), were significantly
related to systolic blood pressure (each P<0.05).
PI 0 to 6 months (ß=-1.4; P=0.05) was marginally
significant. Postnatal changes in length SDS were not associated with
systolic blood pressure at age 30. Birth length SDS had a
significant inverse association with diastolic blood
pressure (ß=-2.6; P<0.05). None of the other
anthropometric variables were significantly related to
diastolic pressure. Tests for interaction between gender
and anthropometric variables in both systolic and
diastolic blood pressure models did not show any
statistical significance (each P>0.1). According to the
criterion of Hoaglin and Welsch,24 3 subjects were
potentially influential on the multivariable regression as
indicated by a leverage value larger than 2xmean leverage value.
However, exclusion of the 3 subjects from the analysis would
give similar findings (details not shown), except that PI 0 to 6
months would be more significant in this restricted sample (ß=-1.9;
P=0.01).
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In a supplementary set of multiple regression, we omitted adult
BMI from the multiple regression models. Without adjustment for adult
BMI, the coefficients of PI at birth on systolic and
diastolic blood pressure reduced to -1.3
(P=0.14) and -0.4 (P=0.55), respectively
(details not shown). In another supplementary analyses, we
substituted BMI to PI (details not shown). The results were
similar to those reported in Table 3. The only difference that
may affect the interpretation was that the (multiple) regression
coefficient for BMI 0 to 6 months on systolic blood pressure
became insignificant (ß=-1.7; P=0.08).
Table 4 shows that the predicted differences in systolic and diastolic pressure between subjects at 95 percentile and 5 percentile of each significant anthropometric variable. It can be seen that the clinical importance of the fetal growth and early postnatal growth variable on blood pressure was roughly the same as that of adult BMI.
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Discussion |
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This is a longitudinal study of a Hong Kong Chinese cohort with detailed and accurate anthropometric measurements from birth through childhood into adult life. This study allows for simultaneous investigation on the long-term consequence of fetal and postnatal wasting and stunting. The choice of 6 and 18 months of age to indicate phases of postnatal growth was based on biological knowledge of human growth rather than data availability. Most previous studies lack information about birth length; therefore, they could only use birth weight for their analyses. Birth weight and other size-at-birth measures are only surrogate indicators of intrauterine growth and nutrition. In this study, both birth length and PI were used. They are more sensitive for the purpose and better characterize the dimensions of growth and nutrition. Potential socioeconomic confounders, maternal health, and GA were adjusted for. Confounding by congenital abnormalities was unlikely because of the exclusion criterion in recruitment.25 Model checking based on leverage statistics supported the robustness of the findings.
Nonetheless, there are several limitations in this study. Of the
original longitudinal study of 523 subjects, complete data were
available from 122 (23%) for the analysis. However, the
participants and nonparticipants were similar in birth length, birth
weight, and mother’s education. These 3 characteristics were chosen
for comparison before the analysis. There was no obvious
selection bias. The sample size was affected by the losses to
follow-up. There could be a problem of statistical power. Effect
estimates that were clinically important should be tentatively
interpreted with this problem in mind. Most historic data could not
offer data on GA. Our analyses involved imputation of GA values
for 3 subjects. However, the number was small and the imputation had
taken into account of birth weight. We use PI for its independence from
birth length; we then used PI for postnatal change in weight for
height for consistency. Using BMI instead of PI in
the multiple regression would provide similar results.
There was substantial correlation between the body size
variables at various ages. Birth weight itself was strongly
correlated with birth length. Any seemingly apparent association
between birth weight and blood pressure could be the result of birth
length. Birth length was associated with diastolic
pressure, but birth weight was not (Table 2). PI and length SDS
at birth were negatively correlated with PI and length SDS,
especially during the first 6 months of life. This reflected catch-up
growth in early infancy. Estimates of the impact of size at birth on
blood pressure could be affected by postnatal growth. Multiple
regression analyses (Table 3) suggested that length and
PI at birth and postnatal growth in weight for height from 6 to 18
months were inversely related to blood pressure in young adulthood. The
association between postnatal growth in weight for length 0 to 6 months
can only be taken tentatively because the significance level of PI 0
to 6 months was marginal (P=0.05) and using BMI 0 to 6
months as an alternative indicator would give an insignificant result
(P=0.08). Birth length was also inversely associated with
diastolic blood pressure. Blood pressure level mainly
varied within the normal range in the present sample. Only 1 male
participant was found to be hypertensive (145/95), with a birth length
of -2.3 SDS, a PI at birth of 25.3, and a PI 0 to 6 months of
-6.1. It has been suggested that hypertension is initiated by early
experience and that the effect will amplify throughout
life.9 Empiric findings have shown that the
association between birth weight and blood pressure is age-dependent;
the older the subject, the stronger the association.3 9
Furthermore, within a cohort, people’s relative positions of blood
pressure tend to maintain over time. The present cohort was only at
the age of 30 years. It is quite plausible that at older ages the early
growth failure may not only lead to a higher blood pressure but also a
higher risk of hypertension.
Lucas et al23 suggested comparing the regression coefficients of birth weight (or relative weight) with and without adjustment for adult BMI. In agreement with their hypothesis, without the adjustment, the coefficients of PI at birth slightly reduced toward the null value. This suggests the impact of centile crossing in weight for length from pediatric age to adulthood. Nevertheless, the point estimate on systolic blood pressure remained to be negative and strong. This may reflect an independent effect undetected as the result of insufficient statistical power.
At first glance, the inverse association between postnatal change in PI and systolic blood pressure seems to contradict findings from a Dutch study on blood pressure and a Finnish study on cardiovascular mortality, which suggested a positive association between postnatal weight gain and blood pressure and cardiovascular mortality.5 7 However, the present study and the previous studies in Europe are not comparable because of differences in the age of measurement of body size and in the outcome variables. For instance, in the Finnish study, the first postnatal growth measurement was taken at the age of 7 years. Moreover, there is an important difference in the situation of postnatal growth. In the Finnish study, postnatal accelerated growth was reportedly driven by improved nutrition. Though the Dutch study did not report, it is reasonable to assume that the Dutch infants born in 1980 had better nutrition and living environment than did the infants born in 1967 in Hong Kong. A previous report of the Hong Kong study has described the poor situation of the infants.19 The children had diarrheal and respiratory diseases related to environmental reasons. From the age of 6 months, there was a problem of inappropriate weaning and feeding practice; therefore, in this study, postnatal changes in body size should be interpreted as reflecting growth faltering, which is a more relevant worry in developing countries than childhood accelerated growth.
Postnatal height gain did not have any statistically significant relation with blood pressure in adulthood. Despite a lot of research since the 1970s, the causes and mechanisms of stunting in early ages are still largely unknown in nutritional and metabolic terms.26 Nevertheless, epidemiological studies suggested that stunting and wasting represent 2 different biological processes.11 It is then not very surprising to see changes in PI associated with blood pressure but not changes in length. It also highlights the importance of differentiating height/length and weight for length.
Recent research suggested that the association between blood
pressure and stroke was stronger in the Asian population than in the
Western population. It was estimated that a reduction of 3 mm Hg
in diastolic blood pressure should reduce the number of
strokes in eastern Asia by one third.27 If the regression
coefficients shown in Table 3 represent causal
relations, an improvement in birth length to the average level
described by the international reference (ie, an increase of 0.8 SDS)
will reduce diastolic blood pressure by 
2.1 mm Hg.
This would mean a substantial public health achievement. It was also
suggested that the effect on preventing coronary events of
controlling blood pressure among Indo-Asians in Britain had been
understated (Cruickshank, Letter to Editor, Br Med J
1996;312:376). Identification of the determinants of blood pressure in
Asian people has an important societal implication. Fetal growth and
early postnatal growth may make a difference in blood pressure as
important as that of adult BMI (Table 4) and therefore should
receive healthcare attention.
In summary, the present study of Hong Kong Chinese 30 years of age confirms that shortness at birth was inversely associated with both systolic and diastolic blood pressure in adulthood. There were some signs that thinness at birth and faltering in PI from birth to 6 months were also inversely associated with systolic blood pressure, but a larger sample size is needed for a firm conclusion. Growth faltering in PI from 6 to 18 months was inversely associated with systolic blood pressure in adult life. There was no statistically significant evidence for any association between postnatal changes in length and blood pressure at age 30 years. Future research is needed to simultaneously analyze the impact of fetal and postnatal growth. Healthcare interventions to prevent and remedy fetal growth restriction and postnatal faltering should be evaluated with longer follow-up.
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Acknowledgments |
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This study was supported by the United Kingdom/Hong Kong Joint Research Scheme of The British Council and the Hong Kong Research Grants Council; Health Services Research Fund No. 531037; the MRC Environmental Epidemiology Unit, University of Southampton; and the Faculty of Medicine, University of Hong Kong.
Received December 27, 1999; first decision January 26, 2000; accepted May 11, 2000.
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 A. D. Stein, A. Conlisk, B. Torun, D. G. Schroeder, R. Grajeda, and R. Martorell Cardiovascular Disease Risk Factors Are Related to Adult Adiposity but Not Birth Weight in Young Guatemalan Adults J. Nutr., August 1, 2002; 132(8): 2208 - 2214. [Abstract] [Full Text] [PDF]
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 O. Hafstrom, J. Milerad, and H. W. Sundell Altered Breathing Pattern after Prenatal Nicotine Exposure in the Young Lamb Am. J. Respir. Crit. Care Med., July 1, 2002; 166(1): 92 - 97. [Abstract] [Full Text] [PDF]
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M. W Gillman Epidemiological challenges in studying the fetal origins of adult chronic disease Int. J. Epidemiol., April 1, 2002; 31(2): 294 - 299. [Full Text] [PDF]
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C.M. Law, A.W. Shiell, C.A. Newsome, H.E. Syddall, E.A. Shinebourne, P.M. Fayers, C.N. Martyn, and M. de Swiet Fetal, Infant, and Childhood Growth and Adult Blood Pressure: A Longitudinal Study From Birth to 22 Years of Age Circulation, March 5, 2002; 105(9): 1088 - 1092. [Abstract] [Full Text] [PDF]
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