PEDIATRICS Vol. 116 No. 3 September 2005, pp. 725-731 (doi:10.1542/peds.2005-0309)
Is Blood Pressure Increased 19 Years After Intrauterine Growth Restriction and Preterm Birth? A Prospective Follow-up Study in the Netherlands
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* Department of Pediatric Nephrology, Erasmus MC–Sophia Children's Hospital, University Medical Center Rotterdam, Rotterdam, Netherlands
Department of Clinical Epidemiology
Department of Pediatrics
¶ Department of Clinical Laboratory, Leiden University Medical Center
|| Department of TNO Quality of Life, Leiden, Netherlands
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ABSTRACT |
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 TOP ABSTRACT METHODSRESULTSDISCUSSIONCONCLUSIONSREFERENCES |
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Objective. To determine whether intrauterine growth restriction (IUGR) is a predisposing factor for high blood pressure (BP) in 19-year-olds who were born (very) preterm.
Methods. A prospective follow-up study was conducted at age 19 in individuals who born preterm in the Netherlands in 1983. Systolic, diastolic, and mean BP values and plasma renin activity concentration were obtained in 422 young adults who were born with a gestational age (GA) <32 weeks. BP values were also measured in 174 individuals who born with a GA of 
32 weeks and a birth weight of <1500 g.
Results. An increased prevalence of hypertension and probably also of prehypertensive stage was found. IUGR, birth weight, GA, and plasma renin activity were not associated with BP. Current weight and BMI were the best predicting factors for systolic BP at the age of 19 years.
Conclusions. The prevalence of hypertension is high in individuals who were born preterm when compared with the general population. In the individuals who were born very preterm, no support to the hypothesis that low birth weight is associated with increased BP at young adult age can be given.
Key Words: adulthood • blood pressure • follow-up studies • intrauterine growth retardation • preterm infants
Abbreviations: IUGR, intrauterine growth restriction • BP, blood pressure • GA, gestational age • SBP, systolic blood pressure • SDS, SD score • DBP, diastolic blood pressure • PRA, plasma renin activity • MAP, mean arterial pressure • CI, confidence interval • NHANES III, Third National Health and Nutrition Examination Survey
The suggested association between birth weight and adult diseases was studied in many epidemiologic studies in the past decades ("fetal origins of adult diseases" hypothesis).1,2 In these studies, an inverse relation has been described between birth weight and hypertension, hyperlipidemia, type 2 diabetes, and cardiovascular diseases in adult life. Individuals born after intrauterine growth restriction (IUGR) are thought to be at risk for developing high blood pressure (BP) compared with individuals with the same birth weight but no IUGR.3,4
Besides low birth weight, 3 other early factors that are considered to be important risk factors for developing high BP in adult life have been identified in individuals with IUGR. First, accelerated postnatal growth in weight and length is suggested to increase the risk for developing hypertension and type 2 diabetes in later life, especially in low birth weight individuals.5–7
Second, it was postulated that altered angiotensin activity was an important factor underlying the "fetal origins of adult diseases" hypothesis.8,9 Also, hypoxia increased sympathetic nerve activity and catecholamine production and proliferation of juxtaglomerular cells (and thus renin-producing cells) are suggested as factors in the pathogenesis.
Finally, preterm infants are probably at even greater risk for developing adult diseases compared with individuals who were born at term. A large Swedish study showed an inverse association between gestational age (GA), ranging from 35 to 44 weeks, and systolic BP (SBP) in 165136 Swedish men.10 This correlation may be stronger in the lower range of gestation (GA 30–38 weeks), as demonstrated by Siewert-Delle et al.11 Very preterm infants who were born with a GA of <30 weeks were not included in this study. In contrast, other studies do not support these data. Singhal et al12 did not find an attributable risk to vascular disease at the age of 15 years in 216 preterm individuals (mean GA: 31 weeks) compared with individuals who were of the same age and born at term.
It is suggested that the underlying mechanism for prematurity's influencing BP and cardiovascular risk is related to an impaired (fetal) organ development. Many organ systems, such as kidneys and pancreas, develop until the third trimester of normal pregnancy. Preterm birth requires an increased energy of the neonate to grow and survive. Organ development, such as nephrogenesis and ß-cell development in the pancreas, is probably not or only partly completed after preterm birth.13 Large studies that include the lowest ranges of gestation are needed to explore the role of prematurity and growth restriction with respect to the "fetal origins of adult disease" hypothesis.
Also, several maternal factors, such as maternal hypertension, smoking during pregnancy, and perinatal and postnatal factors such as Apgar score and comorbidity after birth and drug use, are supposed to influence both neonatal and adult health. To our knowledge, no previous prospective studies were able to analyze these potential confounders in the relation to birth weight and BP.
In this article, we describe the results of a large, prospective, follow-up study in which BP was obtained in 19-year-olds who were born in 1983 with a GA of <32 weeks. Within this cohort, our objective was (1) to determine whether IUGR is associated with increased BP at age 19 after very preterm birth and whether this is amplified as a result of accelerated weight gain and growth postnatally and (2) to determine whether IUGR is associated with alterations in renin concentrations at age 19 after very preterm birth. In addition, the effects of potential maternal and perinatal and postnatal confounders on BP at young adult age were studied, as well as the relation between GA and BP.
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METHODS |
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Study Population
Participants were recruited from the POPS cohort (Project On Prematures and Small for gestational age infants). The POPS cohort comprises of 94% of all Dutch neonates (n = 1338) who were born alive in 1983 with a GA of <32 weeks (group 1) and/or a birth weight of <1500 g (group 2).14 All individuals who were alive at the age of 19 years (n = 959) and not lost to follow-up until the age of 14 y (n = 934) were invited to participate in a prospective follow-up study conducted from April 2002 until May 2003 in 10 outpatient clinics in the Netherlands.
Perinatal parameters (eg, birth weight, GA, Apgar score, congenital anomalies) and obstetric parameters (eg, maternal hypertension, medication during pregnancy, smoking during pregnancy) were known since birth. Follow-up data for growth (height, weight, and BMI) until the age of 10 years were also known in almost all participants.
Birth weight and birth length were converted to SD scores (SDSs), using Swedish reference standards.15 Birth weight SDS was considered as a measure of IUGR. At follow-up visits at the ages of 3, 6, and 12 months, weight and length (measured in supine position), and at the ages of 2, 5, 10, and 19 years, data on weight and height (measured in standing position) were recorded. All weight, length, and height values were recorded with standardized scales and were expressed as SDS using Dutch reference standards.16 BMI was calculated as weight (kg)/length or height (m)2 and converted to SDSs as well for all follow-up ages.
The main statistical analyses included only participants of group 1 (GA < 32 weeks). To study the relation between GA and BP, also participants of group 2 (GA > 32 weeks and birth weight < 1500 g) were included to increase the range of gestation until 40 weeks. Prevalence rates of hypertension were also calculated in both groups.
Data Obtainment
SBP and diastolic BP (DBP) were obtained with an automatic BP device (Dinamap, Critikon, Germany). Three measurements were performed at the nondominant arm in supine position after 30 minutes of rest in the same position. The cuff size was adjusted for arm length and circumference. Mean values were used in statistical analysis. Mean arterial pressure was calculated as [(SBP + 2 * DBP)/3]. Information about medical history and drug use was obtained by an interview.
Individuals were excluded from the analyses when antihypertensive medication was used, individuals were pregnant, or BP was not measured according protocol. Weight and height were recorded to the nearest 0.1 kg and 0.1 cm, respectively, using calibrated scales. Participants were categorized into normal BP (SBP <120 mm Hg and DBP <80 mm Hg), prehypertensive BP (SBP 120–139 mm Hg or DBP 80–89 mm Hg), hypertension stage 1 (SBP 140–159 mm Hg or DBP 90–99 mm Hg), or hypertension stage 2 (SBP >160 or DBP >100 mm Hg) according the Joint National Committee on Prevention, Detection, Evaluation, and Treatment of High Blood Pressure VII criteria.17
A blood sample was obtained after BP measurement, in which plasma renin activity (PRA) was measured by quantification of the generated angiotensin I with a radioimmunoassay (Incstar, Stillwater, MN). The sensitivity was 0.05 µg/L per hour, and the coefficients of variation ranged from 5.6% to 7.6% at different levels.
Informed Consent and Ethics Committee
Informed consent was obtained after oral and written information had been given. The ethics committees of all participating centers approved the study protocol.
Statistics
Student's unpaired t tests were performed to compare BP means. Because birth weight is positively associated with adult weight and adult weight influences BP (causal pathway),18 we used a multivariate regression model to analyze the effect of birth weight on BP and the effect of growing more in weight than would be expected from a given birth weight. Therefore, we first used linear regression to calculate the expected adult weight (or weight at 3, 6, 12, and 24 months and 5 or 10 years), on the basis of birth weight, and then subtracted the actual adult weight (or weight at the age of 3, 6, and 12 months and 2, 5, 10, or 19 years). This "residual" was entered in the final linear regression model.19 Recently, we explained the algebraic concept of this regression model.20 The coefficient of birth weight SDS shows the effect of birth weight SDS on adult BP, and the coefficient of the residual adult weight shows the effect of gaining more weight than expected on adult BP. Equally, multiple logistic regression analyses were applied to evaluate the effect of birth weight SDS and residual weight and height adjusted for gender on the prevalence of hypertension. The effect of GA and gender on BP and the prevalence of hypertension was analyzed separately with linear and logistic regression models. Statistical significance was defined at P < .05.
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RESULTS |
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Participant Characteristics
Of 934 eligible individuals, 596 participated in this study (response rate: 63.8%). Of the 338 nonresponders, 59 were lost to follow-up, 53 were not able, 177 did not feel like, and 27 did not have time to participate. Thirteen individuals could not be included within the research period, and in 9 individuals the reason for nonresponse is unknown.
Five individuals mentioned that they had had increased BP in the past, but none was treated for hypertension at the time of the study. Eight individuals were excluded from data analysis: 4 because of use of antihypertensive medication for other reasons than hypertension (eg, restless legs, nervousness), 2 because of protocol violation, 1 because of pregnancy, and 1 because of unreliable BP measurement. Therefore, SBP and DBP data of 588 individuals were analyzed, 264 of whom were male and 324 of whom female (Table 1). The mean age was 19.29 years (range: 18.63 –20.18). A total of 418 participants were born at a GA of <32 weeks (group 1); 170 were born with a GA of 32 weeks and with a birth weight of <1500 g (group 2). GA and birth weight of the participants in group 1 were 29.7 ± 1.53 weeks and 1314 ± 338 g and in group 2 were 33.9 ± 1.63 weeks and 1274 ± 177 g, respectively.
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Of all individuals who were alive at 19 years, birth weight and GA did not differ between the responders and nonresponders (mean difference for birth weight: 23 g [95% confidence interval (CI): –12 to 59 g]; mean difference for GA: 0.2 week [95% CI –0.1 to 0.5]). Baseline characteristics of the nonresponders are shown in Table 1. Compared with the individuals in the original cohort (including those who died and were lost to follow-up), the responders had a higher mean birth weight (101 g; 95% CI of mean difference: 67–134 g) and a longer duration of GA (1.2 weeks; 95% CI of mean difference: 0.9–1.5 weeks).
BP Values
Data of BP values are shown in Table 1. The mean (± SD) SBP, DBP, and arterial pressure (MAP) in participants in group 1 were 123 ± 13 mm Hg, 66 ± 8 mm Hg, and 85 ± 9 mm Hg, respectively. Participants in group 2 had a mean SBP, DBP, and MAP of 122 ± 12 mm Hg, 66 ± 8 mm Hg, and 85 ± 8 mm Hg, respectively. SBP was higher in men (126 ± 12) than in women (120 ± 12). DBP was lower in men (64 ± 8) than in women (68 ± 8). Prenatal (maternal hypertension and maternal smoking during pregnancy) and perinatal and postnatal parameters (alterations on cardiotocographic measurement, Apgar score, neonatal use of corticosteroids, sepsis, and infant respiratory distress syndrome status) all were related to birth weight SDS but not to SBP and DBP values (data not shown). Therefore, no adjustment for these parameters was required.
In a linear regression analysis of participants who were born with a GA of <32 weeks, BP was not associated with birth weight, birth weight SDS, birth length, and birth length SDS, all adjusted for gender. Regression coefficients (ß values) are given in Tables 2 and 3. Increased postnatal weight gain and BMI after the age of 5 years both were predictors for SBP at the age of 19 years. The strength of this relation increased with age. Height at 5 years of age predicted SBP, DBP, and MAP at age 19. However, the actual effect on both SBP and DBP was very small (0.3-mm Hg increase in SBP per 1 SD more increase in height than expected at age 5). Current weight (SDS) and current BMI (SDS) were the strongest predictors for SBP (ß = 2.3 mm Hg/1 residual weight SDS and 2.4 mm Hg/1 residual BMI SDS, respectively). Early postnatal weight gain (0–2 y) and increase in length were not related to BP at the age of 19 years.
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BP was also not related to GA, both when only participants in group 1 were included (ß for SBP: –0.251-mm Hg/week increase in GA; 95% CI: –1.016 to 0.514) and when all participants were included (ß for SBP: –0.149-mm Hg/week increase in GA; 95% CI: –0.542 to 0.245) or when only participants with a birth weight of <1500 g were included (ß for SBP: –0.150-mm Hg/week increase in GA; 95% CI: –0.553 to 0.254).
PRA was inversely related to BP adjusted for gender (ß for SBP: –0.02 mm Hg/1 µg per L/hour [95% CI: –0.032 to –0.011; P = .001]; ß for DBP: –0.0133 mm Hg/1 µg per L/hour [95% CI: –0.037 to –0.005; P = .011]; ß for MAP: –0.024 mm Hg/1 µg per L/hour [95% CI: –0.039 to –0.009; P = .002). Regression coefficients were not different between participants with low and high birth weight SDS. PRA was not related to birth weight SDS or GA (Table 4 for mean values within birth weight SDS tertiles).
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The prevalence of hypertension (SBP >140 mm Hg or DBP >90 mm Hg) was 10.5% and of prehypertensive stage was 45.9% (SBP 120–139 mm Hg or DBP 80–89 mm Hg) within group 1 and 8.8% and 37.6%, respectively within group 2 (Table 5). The crude risk for hypertension was higher in men (odds ratio: 2.7; 95% CI: 1.4–5.3) compared with women (logistic regression). Birth weight SDS and GA both did not affect the risk for hypertension. Increased postnatal weight gain and BMI after 5 years were predictors for the risk for hypertension at the age of 19 years, but current weight (19 years) affected the risk the most.
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DISCUSSION |
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TOPABSTRACTMETHODSRESULTSDISCUSSIONCONCLUSIONSREFERENCES |
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This article describes the results of the first large-scale prospective study on the suggested association between IUGR and BP at the age of 19 years in individuals who were born with a GA of <32 weeks and/or birth weight of <1500 g. Our main finding was that we were not able to show a relation between birth weight SDS, birth length SDS, or GA and adult BP. Adjustment for height, a common procedure in pediatric BP interpretation, did not reveal a relation between birth weight SDS and BP either. Also, accelerated postnatal growth or weight gain during the first months in life (postnatal hypothesis) did not influence BP at the age of 19 years. Current weight and BMI were the best predictors of BP at age 19.
A remarkable finding was that in our 19-year-old cohort (group 1), the mean SBP was high. In our cohort (mainly white), the SBP in men was 126 mm Hg and in women was 120 mm Hg. In comparison, the SBP of individuals of the same age (18–19 years) participating in the Bogalusa heart study was 115 mm Hg in white men and 109 mm Hg in white women.21 The Third National Health and Nutrition Examination Survey (NHANES III) study reported a mean SBP in 17-year-olds of 117 mm Hg in white boys and 107 mm Hg in white girls.22 So, in both men and women, SBP was higher in our cohort. Other studies, such as NHANES and Framingham heart studies, reported mean BP values in larger age categories (29–37 and 18–39 years), making comparison with our results difficult.23
The prevalence of hypertension in our study was 10.5%. The overall prevalence of hypertension in individuals between 18 and 39 years of age was 7.2% in the NHANES III survey.23 Moreover, as it has been reported that the prevalence of hypertension increases by 1.3% with a 1-year increase of age,23 the prevalence of hypertension in the general population between ages 18 and 39 would be higher than the prevalence in 19-year-olds. The prevalence of prehypertension in our cohort was 45.9%. Such individuals are suggested to have a 2-fold risk for progression toward hypertension in later life.17 Therefore, monitoring of BP in these individuals is recommended. However, whether the prevalence of prehypertensive stage (45.9% in our cohort) was also high compared with the general population and/or with a random 19-year-old reference group is not known. Population-based reports on BP prevalences according to the most recent criteria are needed. To compare our data with the Muscatine study, we needed to categorize our data according the Joint National Committee on Prevention, Detection, Evaluation, and Treatment of High Blood Pressure V criteria.24 Then, the prevalence of normal BP (SBP <130 mm Hg and DBP <85 mm Hg) in our cohort was lower compared with the subjects in the Muscatine study (62.4% vs 72%) and the prevalence of high BP (SBP 130–139 mm Hg or DBP 85–89) and hypertension stage I (SBP 140–159 mm Hg or DBP 90–99) was higher (22.2% and 15.5% in our cohort vs 18% and 9% in the Muscatine, respectively) in both men and women.25 Again, the mean age of the participants in our cohort was much lower (19 years in our study versus 29–37 years in the Muscatine study).
Several factors may have influenced our results. First, our protocol of BP measurements to minimize variability deviated from other studies. We measured BP 3 times in rest, in supine position, and at the nondominant arm. BP values are suggested to be lower when measured in supine position, but when the arm is supported at the heart level (which is the case in supine position), no significant error is expected.26
Second, our BP values may have been influenced because of the use of an automatic oscillometric device (Dinamap). Two studies that compared manometric and Dinamap BP measurements reported an underestimation of the DBP values between 2.4 and 8.2 mm Hg when this automatic device was used.27,28 However, inconsistency on the SBP values exists. Coppieters et al reported that SBP was systematically 3.6 mm Hg lower in Dinamap measurements, but Pavlik et al reported a systematic overestimation of SBP between 1.0 and 6.7 mm Hg when the Dinamap was used.27,28 When we adjusted for the systematic error as reported by Coppieters et al, the prevalence of hypertension increased to 18.9% and the prevalence of prehypertensive stage to 48.5%. When the Dinamap systematically overestimated the SBP with 6.7 mm Hg and underestimated DBP with 2.4 mm Hg,27,28 the mean BP in our cohort decreased to 120 ± 12 for SBP and 67 ± 8 for DBP in men and 114 ± 12 for SBP and 70 ± 8 for DBP in women (data not shown). The prevalence of hypertension within group 1 dropped to 4.3% and of prehypertensive stage to 31.8%. Still, mean SBP and DBP were higher compared with the subjects in the NHANES III and Bogalusa heart study.22,29
Third, it is recommended that BP be measured at least 2 times independently before mean SBP and DBP are calculated and a person is defined as hypertensive. Our 3 BP measurements were performed on 1 day and are evidently not independent. However, the reference data that we used to compare prevalence rates and mean BP values were also based on one initial screening and the mean of at least 3 measurements.22,23 Therefore, our data are comparable, showing both high prevalence and high mean BP.
Our study indicates that individuals who were born very preterm have elevated mean BP values and that the prevalence of hypertension is increased at the age of 19 years. This is not related to the extent of IUGR (birth weight SDS), birth weight (g), or GA. In our cohort, the range of birth weight is 560 to 2580 g. Most studies in which the relation between birth weight and adult BP was found included subjects with a birth weight ranging between 2000 and 5000 g.30–32 This suggests that the relation among birth weight, prematurity, and BP may be diminished in the lower birth weight ranges or GAs and is not a continuously linear but a curved dose-response relationship. This would explain the increased mean BP values, increased prevalence of hypertension, and the absence of the relation between birth weight and BP in the participants of group 1 in our cohort. This trend has not been described in other studies that included preterm individuals who were born at GA of 30 weeks. Future studies may help to confirm our findings.
A few other reasons can account for the absence of the association between IUGR and BP. First, at 19 years of age, our cohort may have been too young to detect a relation. Possibly, the differences were not present at this age yet, or differences were too small to detect with our tools (which measure BP 1–2 mm Hg accurate). However, changes in BP as a result of IUGR have been shown in other studies at even younger age.33 Law et al34,35 described that the effect of low birth weight on BP may be obscured during adolescence. Follow-up of our subjects therefore is recommended.
Second, a selection bias could have been introduced because of a response of 64%. Of all participants who were alive at age 19, no differences in baseline characteristics were present. However, compared with the original cohort, the responders had a slightly higher birth weight and were born after a longer duration of gestation compared with the nonresponders. So those with the suggested highest risk for increased BP were less included in the study, possibly leading to negative results. Even if this bias were introduced and a relation between IUGR and BP were concealed, our results concerning mean BP values and prevalence rates are probably underestimated, and conclusions would not change much.
Finally, it is possible that the relation between birth weight and BP does not exist at all and therefore was not found in our cohort. Indeed, authors have debated on contradictory results in several studies. Huxley et al36 stated that most studies that found a relation between birth weight and adult BP included small numbers of subjects. With increasing study size, the relation diminished, suggesting a publication bias.37 Furthermore, most studies failed to account for possible appropriate adjustment for potential confounders, such as current weight.36 As birth weight is positively correlated with current weight and current weight with BP, also in our cohort, current weight cannot be designated as a potential confounder (causal pathway).36,38,39 Therefore, we studied the effect of birth weight and current weight separately, using a multivariate regression model using "unexplained residuals" for current weight as adjusting variable.19 Using this model, no relation could be found.
Several authors suggested that other prenatal, perinatal, and postnatal parameters could influence the association of birth weight and BP.36,39 In our study, we were able to show that maternal hypertension, smoking during pregnancy, neonatal corticosteroids use, presence of infant respiratory distress syndrome, and alterations on cardiotocographic measurement were associated with birth weight SDS. All of these factors were not associated with BP at 19 years. We therefore conclude that these parameters are not confounders in our study.
As expected, PRA was negatively correlated to BP. Individuals with high levels of active renin will have lower BP values. However, neither birth weight SDS nor GA was associated with PRA. These data are not in agreement with the findings of Martyn et al,9 who showed increased plasma concentrations of (in)active renin at adult age in individuals who were large at birth. Konje et al8 found that active renin concentrations in the umbilical vein in neonates after delivery was higher in individuals who were small for gestational age. Both authors concluded that the renin-angiotensin system is altered in individuals with IUGR. Possibly, the relation between birth weight and PRA in our cohort is not found because the relation between birth weight and BP is not present. Contribution to the pathophysiologic mechanism of the renin-angiotensin system therefore can not be given.
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CONCLUSIONS |
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TOPABSTRACTMETHODSRESULTSDISCUSSIONCONCLUSIONSREFERENCES |
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In this large ex-preterm cohort, the mean SBP and the prevalence of hypertension were high. No relation with IUGR was found. Therefore, in individuals who were born prematurely, no support for the "fetal origins of adult diseases" hypothesis can be given. Whether the relation between birth weight and BP is a curved dose-response curve needs to be studied, using subjects in all birth weight ranges and GAs and sophisticated BP tools.
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ACKNOWLEDGMENTS |
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The POPS study at 19 years of age was supported by grants from the Netherlands Organization for Health Research and Development (ZonMw), Edgar Doncker Foundation, Foundation for Public Health Fundraising Campaigns, Phelps Foundation, Swart-van Essen Foundation, Foundation for Children's Welfare Stamps, TNO Prevention and Health, Netherlands Organization for Scientific Research (NWO), Dutch Kidney Foundation, Sophia Foundation for Medical Research, Stichting Astmabestrijding, and Royal Effatha Guyot group.
Participants of the Dutch POPS-19 Collaborative Study Group included the following: TNO Prevention and Health, Leiden (E.T.M. Hille, C.H. de Groot, H. Kloosterboer-Boerrigter, A.L. den Ouden, A. Rijpstra, S.P. Verloove-Vanhorick, and J.A. Vogelaar); Emma Children's Hospital AMC, Amsterdam (J.H. Kok, A. Ilsen, M. van der Lans, W.J.C. Boelen-van der Loo, T. Lundqvist, and H.S.A. Heymans); University Hospital Groningen, Beatrix Children's Hospital, Groningen (E.J. Duiverman, W.B. Geven, M.L. Duiverman, L.I. Geven, and E.J.L.E. Vrijlandt); University Hospital Maastricht, Maastricht (A.L.M. Mulder and A. Gerver); University Medical Center Radboud, Nijmegen (L.A.A. Kollée, L. Reijmers, and R. Sonnemans); Leiden University Medical Center, Leiden (J.M. Wit, F.W. Dekker, and M.J.J. Finken); Erasmus MC–Sophia Children's Hospital, University Medical Center Rotterdam (N. Weisglas-Kuperus, M.G. Keijzer-Veen, A.J. van der Heijden, and J.B. van Goudoever); VU University Medical Center, Amsterdam (M.M. van Weissenbruch, A. Cranendonk, L. de Groot, and J.F. Samsom); Wilhelmina Children's Hospital, UMC, Utrecht (L.S. de Vries, K.J. Rademaker, E. Moerman, and M. Voogsgeerd); Máxima Medical Centrum, Veldhoven (M.J.K. de Kleine, P. Andriessen, C. Dielissen, and I. Mohamed); Isala Clinics, Zwolle (H.L.M. van Straaten, W. Baerts, G. Veneklaas Slots-Kloosterboer, and E. Tuller-Pikkemaat); Royal Effatha Guyot Group, Zoetermeer (M.H. Ens-Dokkum); and Association of Parents of Premature Babies (G.J. van Steenbrugge).
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FOOTNOTES |
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Accepted May 12, 2005.
Address correspondence to A. J. van der Heijden, MD, PhD, Erasmus MC–Sophia Children's Hospital, University Medical Center Rotterdam, Department of Pediatric Nephrology, Room SP 2469, PO Box 2060, 3000 CB Rotterdam, Netherlands. E-mail: a.j.vanderheijden{at}erasmusmc.nl
No conflict of interest declared.
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