Published online March 26, 2007
PEDIATRICS Vol. 119 No. 4 April 2007, pp. e976-e982 (doi:10.1542/10.1542/peds.2006-2742)
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ARTICLE

Association Between Congenital Heart Defects and Small for Gestational Age

Sadia Malik, MD, MPHa,b,c, Mario A. Cleves, PhDa,b,c, Weizhi Zhao, MSa,b,c, Adolfo Correa, MD, MPH, PhDd, Charlotte A. Hobbs, MD, PhDa,b,c and the National Birth Defects Prevention Study

a Arkansas Center for Birth Defects Research and Prevention
b Department of Pediatrics, College of Medicine, University of Arkansas for Medical Sciences, Little Rock, Arkansas
c Arkansas Children's Hospital Research Institute, Little Rock, Arkansas
d National Center on Birth Defects and Developmental Disabilities, Centers for Disease Control and Prevention, Atlanta, Georgia


   ABSTRACT
TOP
 ABSTRACT
METHODS
 RESULTS
 DISCUSSION
 REFERENCES
 
OBJECTIVES. Infants with congenital heart defects may experience inhibited growth during fetal life. In a large case-control study, we addressed the hypothesis that infants with congenital heart defects are more likely to be small for gestational age than infants without congenital heart defects after controlling for selected maternal and infant characteristics.

METHODS. Using data from population-based birth defect registries, the National Birth Defects Prevention Study enrolled infants with nonsyndromic congenital heart defects (case subjects) and infants without congenital heart defects or any other birth defect (control subjects). Small for gestational age was defined as birth weight below the 10th percentile for gestational age and gender. Association between congenital heart defects and small for gestational age was examined by conditional logistic regression adjusting for maternal covariates related to fetal growth.

RESULTS. Live-born singleton infants with congenital heart defects (case subjects, n = 3395) and live-born singleton infants with no birth defect (control subjects, n = 3924) were included in this study. Case subjects had lower birth weights compared with control subjects. Small for gestational age was observed among 15.2% of case subjects and among only 7.8% of control subjects. Congenital heart defect infants were significantly more likely to be small for gestational age than control infants.

CONCLUSIONS. Infants with congenital heart defects are approximately twice as likely to be small for gestational age as control subjects. Small for gestational age status may affect clinical management decisions, therapeutic response, and prognosis of neonates with congenital heart defects. Although the etiology of growth retardation among infants with congenital heart defects is uncertain, further exploration may uncover a common pathogenesis or causal relationship between congenital heart defects and small for gestational age.

Key Words: small for gestational age • cardiac disease • congenital anomalies

Abbreviations: CHD—congenital heart defect • NBDPS—National Birth Defects Prevention Study • OR—odds ratio • CI—confidence interval

Congenital heart defects (CHDs) are the most prevalent birth defects and frequently require multiple hospitalizations and surgical procedures. Prevalence estimates range from 8 to 11 per 1000 live births.1,2 Thus, in the United States, ~32000 to 44000 infants are born with a cardiac defect each year.1 Many infants will require corrective or palliative surgery and extensive hospitalizations during the first year of life.3,4 Medical and surgical outcomes are dependent on the complexity of the cardiac lesion, and other infant characteristics, such as lung development, prematurity, and birth weight.5,6 After corrective or palliative surgery, multiple studies have documented failure to grow in infants with CHDs because of increased metabolic demands and decreased caloric intake.6 The degree of preoperative growth failure has been associated with longer time on the ventilator, difficulty feeding postoperatively, a higher risk of infection, longer hospitalizations, and poor postoperative catch-up growth.5–9

Although the association between CHDs and low birth weight or small for gestational age has been described in clinical and pathologic case series and in case-control studies, few studies have been population based and/or controlled for maternal and fetal determinants of growth.10–15 The estimated risk of small for gestational age in large population-based studies has varied by the type of cardiac defects. Published reports indicate that infants with CHDs are ~1.8 to 3.6 times more likely to be small for gestational age than infants without CHDs.11,16

The etiology of most nonsyndromic CHDs is unknown but likely involves a complex interaction between multiple environmental exposures and genetic susceptibilities. Similarly, the etiology of small for gestational age is complex. The temporal relationship between CHDs and small for gestational age cannot be discerned from case series or case-control studies. It is possible that both CHDs and small for gestational age occur independently but share common risk factors. For example, maternal periconceptional smoking is the leading cause of small for gestational age in developed countries.17–21 Similarly, some case-control studies provide evidence indicating that maternal periconceptional smoking increases the occurrence of CHDs.16,22–25 Elevated total maternal homocysteine levels have been shown to be associated with an increased risk of small for gestational age26 in infants. Our group has also reported a higher incidence of CHDs associated with high maternal homocysteine levels, suggesting a common pathway25,27 related to maternal nutrition. Alternatively, it is possible that small for gestational age in infants with CHDs may be attributed to abnormal fetal hemodynamics.28,29 The objective of our study was to investigate the association between CHDs and small for gestational age in a large population-based sample while controlling for multiple maternal and fetal covariates.


   METHODS
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 ABSTRACT
 METHODS
RESULTS
 DISCUSSION
 REFERENCES
 
Case and Control Selection
Eligible case and control subjects were born between October 1997 through December 2002 and enrolled in the National Birth Defects Prevention Study (NBDPS). Details regarding the methods of NBDPS have been published previously.30 Briefly, the NBDPS is a multicenter ongoing population-based case-control study intended to identify the etiology of >30 nonsyndromic birth defects, including septal, conotruncal, and obstructive heart defects. Case subjects were identified by birth defect surveillance registries in 8 states using uniform diagnostic criteria.

For the investigation reported herein, infants born with CHDs were included if they met the following criteria: (1) the infant had no known single gene disorder or chromosomal abnormality; (2) the diagnosis of a CHD occurred before the child was 1 year of age and was based on an echocardiogram, heart catheterization, surgical or autopsy report; (3) the mother spoke English or Spanish; (4) the infant was not placed for adoption or in foster care; (5) they were singleton births; and (6) they had no extracardiac anomalies. Control subjects were infants with no birth defects randomly selected from birth certificates or hospital discharge listings in the same states as case subjects. During the study period, the birth population covered by the 8 states was ~482000 births per year. Approximately 18% of eligible case mothers and 21% of control mothers refused to participate in the NBDPS study during this time period.

Classification of Cardiac Defects
Each CHD case was reviewed by 1 of 4 NBDPS case classifiers31 and described as "simple" or "associated" based on the complexity of the lesion. Cardiac defects were classified into 4 categories based on the anatomic lesion: (1) conotruncal, including transposition of the great arteries, tetralogy of Fallot, truncus arteriosus, double outlet right ventricle, malaligned ventricular septal defect, and interrupted aortic arch type B; (2) septal, including atrial, ventricular, and atrioventricular septal defects; (3) right-sided obstructive, including pulmonary valve stenosis, pulmonary atresia, and tricuspid atresia; and (4) left-sided obstructive, including aortic valve stenosis, hypoplastic left heart syndrome and variants, coarctation of the aorta, and interrupted aortic arch types A and C lesions. Complex CHD lesions, which included total and partial pulmonary venous connection, double inlet left ventricle, and other lesions with ≥3 cardiac defects, were excluded from this analysis.

Maternal and Infant Covariates
As part of the NBDPS, mothers of case and control subjects completed an extensive interview regarding multiple preconceptional, periconceptional, and pregnancy exposures. A detailed list of exposures included in these interviews has been published previously.30 Maternal factors collected for the NBDPS and known to be associated with small for gestational age included maternal socioeconomic status, age, race/ethnicity,32 gestational weight gain, prepregnancy BMI, parity, preexisting diabetes, hypertension, infections such as cytomegalovirus or rubella smoking, alcohol consumption, and use of marijuana or cocaine.31–34 Infant variables studied included infant gender33 and race/ethnicity.35

Growth Parameters
Birth weight was obtained from the birth certificate and added to the NBDPS clinical database. Small for gestational age was defined as a birth weight less than the 10th percentile for a given gestational age and gender based on a standardized birth weight distribution of US live births.36,37 Gestational age was obtained from the clinical database; if this was missing, we used a calculated variable using expected date of delivery.

Statistical Methods
Maternal and infant characteristics measured on an interval scale were compared between CHD case and control subjects using the Mann-Whitney/Wilcoxon rank sum test. The frequency of small for gestational age was computed for normal control subjects, CHD case subjects, and each CHD subtype independently. Multiple linear regression was used to model birth weight as a function of case-control status and maternal and infant covariates. Adjusted means were computed from the fitted model. Adjusted odds ratios (ORs) and 95% confidence intervals (CIs) for the association between small for gestational age and CHDs were estimated using conditional logistic regression adjusting for infant and maternal factors and grouping on mother's state of residence. Covariates for inclusion were determined based on results of the bivariate analyses and evidence published previously.


   RESULTS
TOP
 ABSTRACT
 METHODS
 RESULTS
DISCUSSION
 REFERENCES
 
From October 1997 through December 2002, 3501 women who had live-born singleton infants with CHDs and no other congenital abnormality (case subjects) and 3953 women who had live-born singleton infants without any birth defects (control subjects) were enrolled in the NBDPS. Of these participants, 100 case subjects and 21 control subjects who had preconceptional type 1 or type 2 diabetes were excluded from the analyses. Six case and 8 control subjects were excluded from the analysis secondary to inconsistent and erroneous birth weight and gestational age measurements. The final sample consisted of 3395 case and 3924 control subjects.

In this NBDPS cohort, the vast majority 2796 (82.4%) had a simple cardiac lesion. Septal heart defects were the most common malformation (44.4%), followed by conotruncal (22.4%), right-sided obstructive (16.8%), and left-sided obstructive (16.3%) defects.

Selected infant and maternal characteristics of case and control subjects are presented in Table 1. There were no significant differences between case and control subjects for maternal education, total household income, parity, or cocaine or alcohol use. Maternal hypertension during the index pregnancy was more frequent among case subjects than control subjects (OR: 1.24; 95% CI: 1.06–1.45). Case subjects were also more likely to smoke during the pregnancy than control subjects (OR: 1.22; 95% CI: 1.04–1.43). Mean prepregnancy weight is shown in Table 1 to be higher for case subjects than control subjects (68.0 vs 66.4 kg; P = .014), and case subjects gained significantly less weight during pregnancy than control subjects (13.7 vs 14.5 kg; P = .002). Infants with CHDs were >3 times more likely to be premature than control subjects (OR: 3.16; 95% CI: 2.69–3.70) and less likely to be female (OR: 0.85; 95% CI: 0.78–0.94). The mean gestational age for case subjects was 38 weeks, and the mean gestational age for control subjects was 39 weeks. After controlling for gestational age and infant and maternal risk factors, CHD case subjects had lower mean birth weights (3039.56 g; SE: 35.8) compared with control subjects (3128.42 g; SE: 35.5; P < .0001).


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  		TABLE 1 Selected Characteristics of CHD Case and Control Subjects

 
As shown in Table 2, 15.2% of case subjects compared with 7.8% of control subjects were small for gestational age (OR: 2.09; 95% CI: 1.78–2.46). The strength and direction of this association remained among those with simple or associated heart lesions. The risk of small for gestational age was also significantly higher for each heart defect subtype group compared with control subjects. The ORs ranged from 1.83 (95% CI: 1.36–2.47) for left-sided obstructive defects to 2.41 (95% CI: 1.89–3.08) for conotruncal defects.


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  		TABLE 2 CHD Case Subjects and Subtypes With Small for Gestational Age

 
In the general population, more premature infants are small for gestational age than term or postterm infants.38 Thus, we conducted a stratified analysis to determine whether the association between CHDs and small for gestational age would be similar in preterm and term/postterm infants. The adjusted ORs for small for gestational age among individual cardiac subtypes for preterm and term/postterm infants are displayed in Fig 1. Among both preterm and term infants, after controlling for maternal and infant covariates, case subjects were more likely to be small for gestational age than control subjects. Among preterm infants, those with conotruncal and septal heart defects had the highest odds ratio for small for gestational age (OR: 3.24; 95% CI: 1.65–6.37 and OR: 2.29; 95% CI: 1.39–3.79, respectively).


Figure 1
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  		FIGURE 1 ORs and 95% CIs according to CHD class and term status.

 

   DISCUSSION
TOP
 ABSTRACT
 METHODS
 RESULTS
 DISCUSSION
REFERENCES
 
The findings of this population-based case-control study demonstrate that infants with CHDs are more likely to be small for gestational age and premature than control infants. Our findings are consistent with recent reports from other developed countries. In a British study, including participants born between 1987 and 2001, 16% of infants with CHDs, were premature compared with 17.3% in our study.39

Being small for gestational age is usually defined as <10% for a given gestational age, and, thus, one may expect more control infants to be small for gestational age than found in our study sample. However, we excluded twins and higher-order multiples and infants with syndromes, which may explain why only 7.8% of the control subjects were small for gestational age.

The nature of the etiologic and temporal relationships between CHDs and fetal growth remains elusive, but 2 competing hypotheses seem plausible. Some risk factors for small for gestational age may also be associated with CHDs. It remains unclear whether small for gestational age and CHDs coexist because of common underlying etiologic pathways, such as maternal smoking, or because CHDs independently affect the growth of the fetus.

The critical period for CHD development is between the third and ninth weeks of gestation. Snijders et al40 showed that erythropoietin levels were increased significantly in small for gestational age infants secondary to fetal hypoxia. Although it is possible that altered fetal circulation because of CHDs might result in low birth weight, no consistent hemodynamic pattern with respect to oxygen saturations or hemoperfusion can explain our findings.

Clinical knowledge about the association that we found between CHDs and small for gestational age may have significant implications in both prenatal and postnatal care. Closer monitoring of fetal growth may be warranted after a prenatal diagnosis of CHD. Nutritional programs in pregnant women at risk of small for gestational age have been shown to improve infant outcomes,41 and mothers diagnosed with CHDs by fetal echocardiography may benefit from nutritional interventions. Postnatal clinical management of the infant with CHD and fetal growth restriction is dependant on cardiac pathology. The most common subtype of CHD is septal heart defects, which often require anticongestive medications if there are signs of congestive heart failure. These children are typically more prone to be placed on medications if the child has concomitant growth failure. They are also more likely to be referred for surgical repair of their underlying lesion if they continue to have growth retardation in the face of adequate medical and nutritional therapy. In contrast, infants with cyanotic heart lesions require multiple palliative surgeries in infancy. If this high-risk group of infants is nutritionally deficient secondary to fetal growth restriction, this can lead to prolonged postoperative hospital stays, as well as invasive surgeries, such as gastrostomy tube placement for nutritional rehabilitation before hospital discharge.

Our findings were based on participants in the NBDPS, which is the largest population-based case-control sample of all major cardiovascular malformations ever conducted in the United States.30 This study uses a structured maternal questionnaire to provide detailed information to confirm gestational age and exposure to environmental and behavioral factors. Uniform criteria for clinical confirmation of the cardiac defect and a rigorous review of abstracted medical chart data by an expert panel of clinicians also maximizes homogeneity between cases.

Limitations of our study must be considered. Sample sizes when stratified by prematurity were limited, reducing our ability to detect statistically significant differences in small for gestational age among specific cardiac phenotypes. Echocardiograms were not performed on control subjects, and thus some may have undiagnosed CHDs. We were not able to obtain length and head circumference data on the majority of NBDPS centers; this information would be relevant in future studies, because it would provide "symmetry" data regarding the timing of intrauterine growth retardation. Symmetrical growth retardation is associated with in utero injury early in pregnancy.

Further study of the association between CHD and small for gestational age will hopefully provide insights into basic mechanisms that may lead to both outcomes. Identifying risk factors for both CHDs and small for gestational age will contribute to the evidence base required for the planning and implementation of primary prevention programs to prevent heart defects and optimize pregnancy outcomes. A greater clinical understanding of the association between CHDs and small for gestational age may have significant implications for prenatal care. Closer monitoring of fetal growth and maternal nutrition is warranted after prenatal diagnosis of CHD. These women may be candidates for nutritional monitoring and more frequent and detailed ultrasounds to determine serial fetal weights.42,43 In addition, infants with CHDs who are small for gestational age require substantial nutritional intervention postnatally to curtail growth-related problems and improve clinical outcomes in infancy and early childhood.44–47


   ACKNOWLEDGMENTS
 
This project was supported by cooperative agreement U50/CCU613236 from the Centers for Disease Control and Prevention.

We thank all staff members of the Centers for Birth Defects Research and Prevention and all of the centers’ abstractors. Most of all, we thank all of the families of children who have participated in the National Birth Defects Prevention Study.


   FOOTNOTES
 
Accepted Oct 23, 2006.

Address correspondence to Charlotte A. Hobbs, MD, PhD, University of Arkansas for Medical Sciences, College of Medicine, Department of Pediatrics, 1120 Marshall St, Mail Slot 512-40, Little Rock, AR 72201. E-mail: hobbscharlotte{at}uams.edu

The contents of this article are solely the responsibility of the authors and do not necessarily represent the official views of the Centers for Disease Control and Prevention.

The authors have indicated they have no financial relationships relevant to this article to disclose.


   REFERENCES
TOP
 ABSTRACT
 METHODS
 RESULTS
 DISCUSSION
 REFERENCES
 

  1. Boneva RS, Botto LD, Moore CA, Yang Q, Correa A, Erickson JD. Mortality associated with congenital heart defects in the United States: trends and racial disparities, 1979–1997. Circulation. 2001;103 :2376 –2381[Abstract/Free Full Text]
  2. Cleves MA, Ghaffar S, Zhao W, Mosley BS, Hobbs CA. First-year survival of infants born with congenital heart defects in Arkansas (1993–1998): a survival analysis using registry data. Birth Defects Res. Part A Clin Mol Teratol. 2003;67 :662 –668[CrossRef]
  3. Tilford JM, Robbins JM, Hobbs CA. Improving estimates of caregiver time cost and family impact associated with birth defects. Teratology. 2001;64(suppl 1) :S37 –S41
  4. Waitzman NJ, Romano PS, Scheffler RM. Estimates of the economic costs of birth defects. Inquiry. 1994;31 :188 –205[Web of Science][Medline]
  5. Ades A, Johnson BA, Berger S. Management of low birth weight infants with congenital heart disease. Clin Perinatol. 2005;32 :999 –xi[CrossRef][Web of Science][Medline]
  6. Peterson RE, Wetzel GT. Growth failure in congenital heart disease: where are we now? Curr Opin Cardiol. 2004;19 :81 –83[CrossRef][Web of Science][Medline]
  7. Castaneda AR, Jonas RA, Mayer JE Jr, Hanley FL. Cardiac Surgery of the Neonate and Infant. Philadelphia, PA: Elsevier; 2004
  8. Bove T, Francois K, DeGroote K, et al. Outcome analysis of major cardiac operations in low weight neonates. Ann Thorac Surg. 2004;78 :181 –187[Abstract/Free Full Text]
  9. Rossi AF, Seiden HS, Sadeghi AM, et al. The outcome of cardiac operations in infants weighing two kilograms or less. J Thorac Cardiovasc Surg. 1998;116 :28 –35[Abstract/Free Full Text]
  10. Rosenthal GL, Wilson PD, Permutt T, Boughman JA, Ferencz C. Birth weight and cardiovascular malformations: a population-based study. The Baltimore-Washington Infant Study. Am J Epidemiol. 1991;133 :1273 –1281[Abstract/Free Full Text]
  11. Khoury MJ, Erickson JD, Cordero JF, McCarthy BJ. Congenital malformations and intrauterine growth retardation: a population study. Pediatrics. 1988;82 :83 –90[Abstract/Free Full Text]
  12. Kramer HH, Trampisch HJ, Rammos S, Giese A. Birth weight of children with congenital heart disease. Eur J Pediatr. 1990;149 :752 –757[CrossRef][Web of Science][Medline]
  13. Levin DL, Stranger P, Kitterman JA, Heymann MA. Congenital heart disease in low birth weight infants. Circulation. 1975;52 :500 –503[Abstract/Free Full Text]
  14. Cedergren MI, Kallen BA. Obstetric outcome of 6346 pregnancies with infants affected by congenital heart defects. Eur J Obstet Gynecol Reprod Biol. 2006;125 :211 –216[CrossRef][Web of Science][Medline]
  15. Jacobs EG, Leung MP, Karlberg J. Birthweight distribution in southern Chinese infants with symptomatic congenital heart disease. J Paediatr Child Health. 2003;39 :191 –196[Web of Science][Medline]
  16. Ferencz C, Loffredo CA, Correa A, Wilson PD. Genetic and Environmental Risk Factors of Major Cardiovascular Malformations: The Baltimore-Washington Infant Study 1981–1989. Armonk, NY: Futura Publishing Co, Inc; 1997
  17. Dejin-Karlsson E, Hanson BS, Ostegren PO, Sjoberg WO, Marsal K. Does passive smoking in early pregnancy increase the risk of small-for-gestational-age infants? Am J Public Health. 1998;88 :1523 –1527[Abstract/Free Full Text]
  18. Infante-Rivard C, Weinberg CR, Guiguet M. Xenobiotic-metabolizing genes and small-for-gestational-age births: interaction with maternal smoking. Epidemiology. 2006;17 :38 –46[CrossRef][Web of Science][Medline]
  19. Salihu HM, Shumpert MN, Aliyu MH, Kirby RS, Alexander GR. Smoking-associated fetal morbidity among older gravidas: a population study. Acta Obstet Gynecol Scand. 2005;84 :329 –334[CrossRef][Web of Science][Medline]
  20. Mitchell EA, Thompson JA, Robinson E, et al. Smoking, nicotine and tar and risk of small for gestational age babies. Acta Paediatr. 2002;91 :323 –328[CrossRef][Web of Science][Medline]
  21. Chiolero A, Bovet P, Paccaud F. Association between maternal smoking and low birth weight in Switzerland: the EDEN study. Swiss Med Wkly. 2005;135 :525 –530[Medline]
  22. Hobbs CA, James SJ, Jernigan S, et al. Congenital heart defects, maternal homocysteine, smoking, and the 677 C>T polymorphism in the methylenetetrahydrofolate reductase gene: evaluating gene-environment interactions. Am J Obstet Gynecol. 2006;194 :218 –224[CrossRef][Web of Science][Medline]
  23. Woods SE, Raju U. Maternal smoking and the risk of congenital birth defects: a cohort study. J Am Board Fam Pract. 2001;14 :330 –334[Medline]
  24. Kallen K. Maternal smoking and congenital heart defects. Eur J Epidemiol. 1999;15 :731 –737[CrossRef][Web of Science][Medline]
  25. Hobbs CA, Malik S, Zhao, W, James SJ, Melnyk S, Cleves MA. Maternal homocysteine and congenital heart defects. J Am Coll Cardiol. 2006;47 :683 –685[Free Full Text]
  26. Yajnik CS, Deshpande SS, Panchanadiker AV, et al. Maternal total homocysteine concentration and neonatal size in India. Asia Pac J Clin Nutr. 2005;14 :179 –181[Web of Science][Medline]
  27. Hobbs CA, Cleves MA, Melnyk S, Zhao W, James SJ. Congenital heart defects and abnormal maternal biomarkers of methionine and homocysteine metabolism. Am J Clin Nutr. 2005;81 :147 –153[Abstract/Free Full Text]
  28. Leiva MC, Tolosa JE, Binotto CN, et al. Fetal cardiac development and hemodynamics in the first trimester. Ultrasound Obstet Gynecol. 1999;14 :169 –174[CrossRef][Web of Science][Medline]
  29. Clapp JF, III. The clinical significance of asymmetric intrauterine growth retardation. Pediatr Ann. 1996;25 :223 –227[Web of Science][Medline]
  30. Yoon PW, Rasmussen SA, Lynberg MC, et al. The National Birth Defects Prevention Study. Public Health Rep. 2001;116(suppl 1) :32 –40
  31. Lin A, Botto L, Ghaffar S, Cosper C, Correa A. The National Birth Defects Prevention Study. Classification of cardiovascular malformations in the National Birth Defects Prevention Study [abstract]. Am J Hum Genet. 2003;73 :165
  32. Cogswell ME, Yip R. The influence of fetal and maternal factors on the distribution of birth weight. Semin Perinatol. 1995;19 :222 –240[CrossRef][Web of Science][Medline]
  33. Martikainen MA. Effects of intrauterine growth retardation and its subtypes on the development of the preterm infant. Early Hum Dev. 1992;28 :7 –17[CrossRef][Web of Science][Medline]
  34. Ashworth A. Effects of intrauterine growth retardation on mortality and morbidity in infants and young children. Eur J Clin Nutr. 1998;52(suppl 1) :S34– S41
  35. Alexander GR, Kogan M, Bader D, Carlo W, Allen M, Mor J. US birth weight/gestational age-specific neonatal mortality: 1995–1997 rates for whites, Hispanics, and blacks. Pediatrics. 2003;111 (1). Available at: www.pediatrics.org/cgi/content/full/111/1/e61
  36. Zhang J, Bowes WA Jr. Birth-weight-for-gestational-age patterns by race, sex, and parity in the United States population. Obstet Gynecol. 1995;86 :200 –208[CrossRef][Web of Science][Medline]
  37. Alexander GR, Himes JH, Kaufman RB, Mor J, Kogan M. A United States national reference for fetal growth. Obstet Gynecol. 1996;87 :163 –168[CrossRef][Web of Science][Medline]
  38. Clausson B, Cnattingius S, Axelsson O. Preterm and term births of small for gestational age infants: a population-based study of risk factors among nulliparous women. Br J Obstet Gynaecol. 1998;105 :1011 –1017[Web of Science][Medline]
  39. Tanner K, Sabrine N, Wren C. Cardiovascular malformations among preterm infants. Pediatrics. 2005;116 (6). Available at: www.pediatrics.org/cgi/content/full/116/6/e833
  40. Snijders RJ, Abbas A, Melby O, Ireland RM, Nicolaides KH. Fetal plasma erythropoietin concentration in severe growth retardation. Am J Obstet Gynecol. 1993;168 :615 –619[Web of Science][Medline]
  41. Villar J, Merialdi M, Gulmezoglu AM, et al. Characteristics of randomized controlled trials included in systematic reviews of nutritional interventions reporting maternal morbidity, mortality, preterm delivery, intrauterine growth restriction and small for gestational age and birth weight outcomes. J Nutr. 2003;133 :1632S –1639S[Free Full Text]
  42. Hobbins J. Morphometry of fetal growth. Acta Paediatr. 1997;423(suppl) :165 –168
  43. Soothill PW, Bobrow CS, Holmes R. Small for gestational age is not a diagnosis. Ultrasound Obstet Gynecol. 1999;13 :225 –228[CrossRef][Web of Science][Medline]
  44. Schuurmans FM, Pulles-Heintzberger CF, Gerver WJ, Kester AD, Forget PP. Long-term growth of children with congenital heart disease: a retrospective study. Acta Paediatr. 1998;87 :1250 –1255[CrossRef][Web of Science][Medline]
  45. Chatelain P. Children born with intra-uterine growth retardation (IUGR) or small for gestational age (SGA): long term growth and metabolic consequences. Endocr Regul. 2000;34 :33 –36[Medline]
  46. Strauss RS, Dietz WH. Effects of intrauterine growth retardation in premature infants on early childhood growth. J Pediatr. 1997;130 :95 –102[CrossRef][Web of Science][Medline]
  47. Albertsson-Wikland K, Karlberg J. Postnatal growth of children born small for gestational age. Acta Paediatr. 1997;423(suppl) :193 –195
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