European Journal of Pediatrics

, Volume 175, Issue 8, pp 1047–1057 | Cite as

Defining small-for-gestational-age: prescriptive versus descriptive birthweight standards

  • Liset HoftiezerEmail author
  • Chantal W. P. M. Hukkelhoven
  • Marije Hogeveen
  • Huub M. P. M. Straatman
  • Richard A. van Lingen
Original Article


Descriptive population-based birthweight standards possess low sensitivity in detecting infants with growth impairment. A prescriptive birthweight standard based on a ‘healthy’ subpopulation without risk factors for intrauterine growth restriction might be superior. We created two birthweight standards based on live born, singleton infants with gestational age 24–42 weeks and born in The Netherlands between 2000 and 2007. Inclusion criteria for the prescriptive birthweight standard were restricted to infants without congenital malformations, born to healthy mothers after uncomplicated pregnancies. We defined small-for-gestational-age (SGA) as birthweight <10th percentile and assessed the ability of both standards to predict adverse neonatal outcomes. The prescriptive birthweight standard identified significantly more infants as SGA, up to 38.0 % at 29 weeks gestation. SGA infants classified according to both standards as well as those classified according to the prescriptive birthweight standard only, were at increased risk of both major and minor adverse neonatal outcomes. The prescriptive birthweight standard was both more sensitive and less specific, with a maximum increase in sensitivity predicting bronchopulmonary dysplasia (+42.6 %) and a maximum decrease in specificity predicting intraventricular haemorrhage (−26.9 %) in infants aged 28–31 weeks.

Conclusion: Prescriptive birthweight standards could improve identification of infants born SGA and at risk of adverse neonatal outcomes.

What is Known:

Descriptive birthweight standards possess low sensitivity in detecting growth restricted infants at risk of adverse neonatal outcomes.

Prescriptive standards could improve identification of very preterm small-for-gestational-age (SGA) infants at risk of intraventricular haemorrhage.

What is New:

Prescriptive standards identify more preterm and term SGA infants at risk of major adverse neonatal outcomes.

Late preterm and term SGA infants classified according to the prescriptive standard are at increased risk of minor adverse neonatal outcomes with potentially harmful implications.


Small for gestational age Intrauterine growth restriction Reference standards Sensitivity and specificity Perinatal mortality and morbidity 



Adjusted odds ratio


Bronchopulmonary dysplasia


Cystic periventricular leukomalacia


Gestational age


Hypoxic ischemic encephalopathy


Infant respiratory distress syndrome


Intrauterine growth restriction


Intraventricular haemorrhage


Necrotising enterocolitis


The Netherlands Perinatal Registry


Retinopathy of prematurity





We would like to thank The Netherlands Perinatal Registry (PRN) for granting us unlimited access to the required data.

Authors’ contributions

RvL and MH conceived the idea of the manuscript. LH, CH, MH, and RvL were responsible for the study concept and design. LH, CH, and HS analysed the data. LH wrote the initial draft of the manuscript, which was revised by LH, CH, MH, HS, and RvL. All authors approved the final manuscript as submitted and agree to be accountable for all aspects of the work.

Compliance with ethical standards

Ethical standards

The manuscript does not contain clinical studies or patient data.

Conflict of interest

The authors declare that they have no conflicts of interest.


No funding was secured for this study.

Supplementary material

431_2016_2740_MOESM1_ESM.pdf (516 kb)
Appendix 1 (PDF 272 kb)
431_2016_2740_MOESM2_ESM.pdf (134 kb)
Figure S1 Smoothed versus empirical descriptive and prescriptive percentiles for boys (A resp. B) and girls (C resp. D) (PDF 197 kb)
431_2016_2740_MOESM3_ESM.pdf (99 kb)
Figure S2 Test characteristics for infants aged 24+0-25+6 and 37+0-39+0 weeks. BW birthweight (PDF 38 kb)
431_2016_2740_MOESM4_ESM.docx (23 kb)
Table S1 (DOCX 23 kb)
431_2016_2740_MOESM5_ESM.docx (22 kb)
Table S2 (DOCX 22 kb)
431_2016_2740_MOESM6_ESM.docx (21 kb)
Table S3 (DOCX 21 kb)
431_2016_2740_MOESM7_ESM.docx (42 kb)
Table S4 (DOCX 20 kb)
431_2016_2740_MOESM8_ESM.docx (40 kb)
Table S5 (DOCX 20 kb)


  1. 1.
    Barker DJ (2006) Adult consequences of fetal growth restriction. Clin Obstet Gynecol 49:270–283CrossRefPubMedGoogle Scholar
  2. 2.
    Battaglia FC, Lubchenco LO (1967) A practical classification of newborn infants by weight and gestational age. J Pediatr 71:159–163CrossRefPubMedGoogle Scholar
  3. 3.
    Bell MJ, Ternberg JL, Feigin RD, Keating JP, Marshall R, Barton L, Brotherton T (1978) Neonatal necrotizing enterocolitis. Therapeutic decisions based upon clinical staging. Ann Surg 187:1–7CrossRefPubMedPubMedCentralGoogle Scholar
  4. 4.
    Bertino E, Milani S, Fabris C, De Curtis M (2007) Neonatal anthropometric charts: what they are, what they are not. Arch Dis Child Fetal Neonatal Ed 92:F7–F10CrossRefPubMedPubMedCentralGoogle Scholar
  5. 5.
    Burkhardt T, Schäffer L, Zimmermann R, Kurmanavicius J (2008) Newborn weight charts underestimate the incidence of low birthweight in preterm infants. Am J Obstet Gynecol 199:139.e1–139.e6CrossRefGoogle Scholar
  6. 6.
    Campbell MK, Cartier S, Xie B, Kouniakis G, Huang W, Han V (2012) Determinants of small for gestational age birth at term. Paediatr Perinat Epidemiol 26:525–533CrossRefPubMedGoogle Scholar
  7. 7.
    Clausson B, Gardosi J, Francis A, Cnattingius S (2001) Perinatal outcome in SGA births defined by customised versus population-based birthweight standards. BJOG 108:830–834PubMedGoogle Scholar
  8. 8.
    Cole TJ (1990) The LMS method for constructing normalized growth standards. Eur J Clin Nutr 44:45–60PubMedGoogle Scholar
  9. 9.
    Committee on Obstetric Practice, ACOG; American Academy of Pediatrcis; Committee on Fetus and Newborn, ACOG (2006) ACOG Committee Opinion Number 333, May 2006 (replaces No. 174, July 1996): the Apgar score. Obstet Gynecol 107:1209–1212CrossRefGoogle Scholar
  10. 10.
    Damodaram M, Story L, Kulinskaya E, Rutherford M, Kumar S (2011) Early adverse perinatal complications in preterm growth-restricted fetuses. Aust N Z J Obstet Gynaecol 51:204–209CrossRefPubMedGoogle Scholar
  11. 11.
    De Vries LS, Eken P, Dubowitz LM (1992) The spectrum of leukomalacia using cranial ultrasound. Behav Brain Res 49:1–6CrossRefPubMedGoogle Scholar
  12. 12.
    Ferdynus C, Quantin C, Abrahamowicz M, Burguet A, Sagot P, Gouyon JB (2013) Comparison of the ability of alternative birthweight and fetal weight standards to identify preterm newborns at increased risk of perinatal death. BJOG 120:1456–1464CrossRefPubMedGoogle Scholar
  13. 13.
    Ferdynus C, Quantin C, Abrahamowicz M, Platt R, Burguet A, Sagot P, Binquet C, Gouyon JB (2009) Can birth weight standards based on healthy populations improve the identification of small-for-gestational-age newborns at risk of adverse neonatal outcomes? Pediatrics 123:723–730CrossRefPubMedGoogle Scholar
  14. 14.
    Gardosi J, Chang A, Kalyan B, Sahota D, Symonds EM (1992) Customised antenatal growth charts. Lancet 339:283–287CrossRefPubMedGoogle Scholar
  15. 15.
    Giedion A, Haefliger H, Dangel P (1973) Acute pulmonary X-ray changes in hyaline membrane disease treated with artificial ventilation and positive end-expiratory pressure (PEP). Pediatr Radiol 1:145–152CrossRefPubMedGoogle Scholar
  16. 16.
    Gilbert WM, Danielsen B (2003) Pregnancy outcomes associated with intrauterine growth restriction. Am J Obstet Gynecol 188:1596–1599, discussion 1599–1601CrossRefPubMedGoogle Scholar
  17. 17.
    Hawass NE (1997) Comparing the sensitivities and specificities of two diagnostic procedures performed on the same group of patients. Br J Radiol 70:360–366CrossRefPubMedGoogle Scholar
  18. 18.
    Hemming K, Bonellie S, Hutton JL (2011) Fetal growth and birthweight standards as screening tools: methods for evaluating performance. BJOG 118:1477–1483CrossRefPubMedGoogle Scholar
  19. 19.
    Hendrix N, Berghella V (2008) Non-placental causes of intrauterine growth restriction. Semin Perinatol 32:161–165CrossRefPubMedGoogle Scholar
  20. 20.
    Hutcheon JA, Zhang X, Platt RW, Cnattingius S, Kramer MS (2011) The case against customised birthweight standards. Paediatr Perinat Epidemiol 25:11–16CrossRefPubMedGoogle Scholar
  21. 21.
    International Committee for the Classification of Retinopathy of Prematurity (2005) The international classification of retinopathy of prematurity revisited. Arch Ophthalmol 123:991–999CrossRefGoogle Scholar
  22. 22.
    Joseph KS, Kramer MS, Allen AC, Mery LS, Platt RW, Wen SW (2001) Implausible birth weight for gestational age. Am J Epidemiol 153:110–113CrossRefPubMedGoogle Scholar
  23. 23.
    Karlberg J, Albertsson-Wikland K (1995) Growth in full-term small-for-gestational-age infants: from birth to final height. Pediatr Res 38:733–739CrossRefPubMedGoogle Scholar
  24. 24.
    Kramer MS (1987) Determinants of low birth weight: methodological assessment and meta-analysis. Bull World Health Organ 65:663–737PubMedPubMedCentralGoogle Scholar
  25. 25.
    Lackman F, Capewell V, Richardson B, daSilva O, Gagnon R (2001) The risks of spontaneous preterm delivery and perinatal mortality in relation to size at birth according to fetal versus neonatal growth standards. Am J Obstet Gynecol 184:946–953CrossRefPubMedGoogle Scholar
  26. 26.
    Lawrence C, Fryer JG, Karlberg P, Niklasson A, Ericson A (1989) Modelling of reference values for size at birth. Acta Paediatr Scand Suppl 350:55–69CrossRefPubMedGoogle Scholar
  27. 27.
    Leitner Y, Fattal-Valevski A, Geva R, Eshel R, Toledano-Alhadef H, Rotstein M, Bassan H, Radianu B, Bitchonsky O, Jaffa AJ, Harel S (2007) Neurodevelopmental outcome of children with intrauterine growth retardation: a longitudinal, 10-year prospective study. J Child Neurol 22:580–587CrossRefPubMedGoogle Scholar
  28. 28.
    Løhaugen GC, Østgård HF, Andreassen S, Jacobsen GW, Vik T, Brubakk AM, Skranes J, Martinussen M (2013) Small for gestational age and intrauterine growth restriction decreases cognitive function in young adults. J Pediatr 163:447–453CrossRefPubMedGoogle Scholar
  29. 29.
    Marconi AM, Ronzoni S, Bozzetti P, Vailati S, Morabito A, Battaglia FC (2008) Comparison of fetal and neonatal growth curves in detecting growth restriction. Obstet Gynecol 112:1227–1234CrossRefPubMedPubMedCentralGoogle Scholar
  30. 30.
    Maulik D (2006) Fetal growth restriction: the etiology. Clin Obstet Gynecol 49:228–235CrossRefPubMedGoogle Scholar
  31. 31.
    McCowan L, Horgan RP (2009) Risk factors for small for gestational age infants. Best Pract Res Clin Obstet Gynaecol 23:779–793CrossRefPubMedGoogle Scholar
  32. 32.
    McIntire DD, Bloom SL, Casey BM, Leveno KJ (1999) Birth weight in relation to morbidity and mortality among newborn infants. N Engl J Med 340:1234–1238CrossRefPubMedGoogle Scholar
  33. 33.
    Niklasson A, Ericson A, Fryer JG, Karlberg J, Lawrence C, Karlberg P (1991) An update of the Swedish reference standards for weight, length and head circumference at birth for given gestational age (1977–1981). Acta Paediatr Scand 80:756–762CrossRefPubMedGoogle Scholar
  34. 34.
    Pallotto EK, Kilbride HW (2006) Perinatal outcome and later implications of intrauterine growth restriction. Clin Obstet Gynecol 49:257–269CrossRefPubMedGoogle Scholar
  35. 35.
    Papile LA, Burstein J, Burstein R, Koffler H (1978) Incidence and evolution of subependymal and intraventricular hemorrhage: a study of infants with birth weight less than 1,500 gm. J Pediatr 92:529–534CrossRefPubMedGoogle Scholar
  36. 36.
    Rooth G, Meirik O, Karlberg P (1985) Estimation of the “normal” growth of Swedish infants at term. Preliminary report. Acta Paediatr Scand Suppl 319:76–79CrossRefPubMedGoogle Scholar
  37. 37.
    Sarnat HB, Sarnat MS (1976) Neonatal encephalopathy following fetal distress. A clinical and electroencephalographic study. Arch Neurol 33:696–705CrossRefPubMedGoogle Scholar
  38. 38.
    Brouwers HAA, Bruinse HW, Dijs-Elsinga J, van Huis AM, de Miranda E, Ravelli ACJ, Tamminga P, de Winter GA (2013) Stichting Perinatale Registratie Nederland Grote Lijnen 1999–2012 (The Netherlands Perinatal Registry Trends 1999–2012). The Netherlands Perinatal Registry, UtrechtGoogle Scholar
  39. 39.
    Tsai LY, Chen YL, Tsou KL, Mu SC, Taiwan Premature Infant Developmental Collaborative Study Group (2015) The impact of small-for-gestational-age on neonatal outcome among very-low-birth-weight infants. Pediatr Neonatol 56:101–107CrossRefPubMedGoogle Scholar
  40. 40.
    Visser GH, Eilers PH, Elferink-Stinkens PM, Merkus HM, Wit JM (2009) New Dutch reference curves for birthweight by gestational age. Early Hum Dev 85:737–744CrossRefPubMedGoogle Scholar
  41. 41.
    Yu VY, Upadhyay A (2004) Neonatal management of the growth-restricted infant. Semin Fetal Neonatal Med 9:403–409CrossRefPubMedGoogle Scholar
  42. 42.
    Zaw W, Gagnon R, da Silva O (2003) The risks of adverse neonatal outcome among preterm small for gestational age infants according to neonatal versus fetal growth standards. Pediatrics 111:1273–1277CrossRefPubMedGoogle Scholar
  43. 43.
    Zhang J, Merialdi M, Platt LD, Kramer MS (2010) Defining normal and abnormal fetal growth: promises and challenges. Am J Obstet Gynecol 202:522–528CrossRefPubMedPubMedCentralGoogle Scholar
  44. 44.
    Zhang X, Mumford SL, Cnattingius S, Schisterman EF, Kramer MS (2010) Reduced birthweight in short or primiparous mothers: physiological or pathological? BJOG 117:1248–1254CrossRefPubMedPubMedCentralGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2016

Authors and Affiliations

  • Liset Hoftiezer
    • 1
    Email author
  • Chantal W. P. M. Hukkelhoven
    • 2
  • Marije Hogeveen
    • 3
  • Huub M. P. M. Straatman
    • 4
  • Richard A. van Lingen
    • 1
  1. 1.Princess Amalia Department of Paediatrics, Department of NeonatologyIsalaThe Netherlands
  2. 2.PerinedUtrechtThe Netherlands
  3. 3.Amalia Children’s Hospital, Department of NeonatologyRadboud University Medical CentreNijmegenThe Netherlands
  4. 4.PHARMO Institute for Drug Outcomes ResearchUtrechtThe Netherlands

Personalised recommendations