CoChat
Sign Up
Cited by 582Child Nutrition and Water AccessBirth, Development, and HealthPublic Health and Nutrition

Risk of childhood undernutrition related to small-for-gestational age and preterm birth in low- and middle-income countries

Open access
Christian, Parul, Lee, Sun Eun, Donahue Angel, Moira, Adair, Linda S, Arifeen, Shams E, Ashorn, Per, Barros, Fernando C, Fall, Caroline HD +24 more·2013·International Journal of Epidemiology
DOI 10.1093/ije/dyt109PMC PMC3816349
Open this paper in CoChat — free accountOpen PDF

Abstract

BACKGROUND: Low- and middle-income countries continue to experience a large burden of stunting; 148 million children were estimated to be stunted, around 30-40% of all children in 2011. In many of these countries, foetal growth restriction (FGR) is common, as is subsequent growth faltering in the first 2 years. Although there is agreement that stunting involves both prenatal and postnatal growth failure, the extent to which FGR contributes to stunting and other indicators of nutritional status is uncertain. METHODS: Using extant longitudinal birth cohorts (n=19) with data on birthweight, gestational age and child anthropometry (12-60 months), we estimated study-specific and pooled risk estimates of stunting, wasting and underweight by small-for-gestational age (SGA) and preterm birth. RESULTS: We grouped children according to four combinations of SGA and gestational age: adequate size-for-gestational age (AGA) and preterm; SGA and term; SGA and preterm; and AGA and term (the reference group). Relative to AGA and term, the OR (95% confidence interval) for stunting associated with AGA and preterm, SGA and term, and SGA and preterm was 1.93 (1.71, 2.18), 2.43 (2.22, 2.66) and 4.51 (3.42, 5.93), respectively. A similar magnitude of risk was also observed for wasting and underweight. Low birthweight was associated with 2.5-3.5-fold higher odds of wasting, stunting and underweight. The population attributable risk for overall SGA for outcomes of childhood stunting and wasting was 20% and 30%, respectively. CONCLUSIONS: This analysis estimates that childhood undernutrition may have its origins in the foetal period, suggesting a need to intervene early, ideally during pregnancy, with interventions known to reduce FGR and preterm birth.

The claims and statistics of this paper haven’t been checked yet.

Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.

A few free checks a day · papers already verified open instantly · results are public

Integrity signals

Registry

Crossref · 10.1093/ije/dyt109

Cites

1 of 1 references verified0 citation errors · 0 not checkable

Statistics

Claims the paper makes

The claims and statistics of this paper haven’t been checked yet.

Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.

A few free checks a day · papers already verified open instantly · results are public

Claims other papers make about this one

Each is checked against this paper’s own text: does it say what the citing paper says it does?

  • Breastmilk alone may be insufficient to meet the nutritional needs of MLBW infants.

    “Further, breastmilk alone may be insufficient to meet the nutritional needs of MLBW infants [42, 44–46]; most facilities did not have alternatives readily available.”

    From Facility-based care for moderately low birthweight infants in India, Malawi, and Tanzania (2023) · cites this paper as [46]

    The Introduction and Discussion address low birthweight, growth faltering, inadequate exclusive breastfeeding, and complementary feeding, but do not say that breastmilk alone may be insufficient for MLBW infants. Searches for breastmilk sufficiency and the nutritional needs of low-birthweight infants found no passage addressing that claim. Page numbers were not available in our copy. (LLM, conf=0.75)

    Experimental — accuracy not yet measured

  • When appropriate and safely administered, donor human milk and formula can provide a bridge to breastfeeding.

    “When appropriate and safely administered, DHM and formula can provide a bridge to breastfeeding [46–48].”

    From Facility-based care for moderately low birthweight infants in India, Malawi, and Tanzania (2023) · cites this paper as [46]

    The Discussion mentions inadequate exclusive breastfeeding as a contributor to growth faltering and recommends improving breastfeeding practices. Neither it nor the additional passages retrieved for donor milk, formula, and a bridge to breastfeeding address whether donor human milk or formula can serve as such a bridge. The indexed passages provide no page numbers. (LLM, conf=0.76)

    Experimental — accuracy not yet measured

Self-check

Percentages, sums and reported differences re-computed from the paper’s own numbers.

The self-check needs the paper’s full text.

Cites

Flagged first, then by citations

Research works printed but not linked: 49

  1. [2]Black RE Allen LH Bhutta ZA Maternal and child undernutrition: global and regional exposures and health consequences Lancet 2008 371 243 60 18207566
  2. [3]Pelletier DL The relationship between child anthropometry and mortality in developing countries: implications for policy, programs and future research J Nutr 1994 124 10 Suppl 2047S 2081S 7931716
  3. [4]Victora CG Adair L Fall C Maternal and child undernutrition: consequences for adult health and human capital Lancet 2008 371 340 57 18206223 PMC2258311
  4. [5]Victora CG de Onis M Hallal PC Blossner M Shrimpton R Worldwide timing of growth faltering: revisiting implications for interventions Pediatrics 2010 125 e473 80 20156903
  5. [6]Christian P Kalhan SC Prentice AM Yajnik CS Prenatal origins of malnutrition Emerging Societies—Coexistence of Childhood Malnutrition and Obesity 2009 Vol 63 S Karger Ag Vevey, Switzerland
  6. [7]Blencowe H Cousens S Oestergaard MZ National, regional, and worldwide estimates of preterm birth rates in the year 2010 with time trends since 1990 for selected countries: a systematic analysis and implications Lancet 2012 379 2162 72 22682464
  7. [8]Lee ACC Katz J Blencowe J Born too small: national and regional estimates of term and preterm small-for-gestational-age in 138 low-middle income countries in 2010 Lancet Global Health 2013 (in press) PMC4221634 25103583
  8. [10]Fall CH Fisher DJ Osmond C Margetts BM Multiple micronutrient supplementation during pregnancy in low-income countries: a meta-analysis of effects on birth size and length of gestation Food Nutr Bull 2009 30 S533 46 20120795 PMC3541502
  9. [11]Richter LM Victora CG Hallal PC Cohort profile: the consortium of health-orientated research in transitioning societies Int J Epidemiol 2012 41 621 26 21224276 PMC3378468
  10. [12]Alexander GR Himes JH Kaufman RB Mor J Kogan M A United States national reference for fetal growth Obstet Gynecol 1996 87 163 68 8559516
  11. [15]Zhang J Yu KF What’s the relative risk? A method of correcting the odds ratio in cohort studies of common outcomes JAMA 1998 280 1690 91 9832001
  12. [16]Levin ML The occurrence of lung cancer in man Acta Unio Int Contra Cancrum 1953 9 531 41 13124110
  13. [17]Rao CR Linear statistical inference and its application 1965 John Wiley New York
  14. [18]Vaidya A Saville N Shrestha BP Costello AM Manandhar DS Osrin D Effects of antenatal multiple micronutrient supplementation on children’s weight and size at 2 years of age in Nepal: follow up of a double-blind randomised controlled trial Lancet 2008 371 492 99 18262041 PMC2241662
  15. [19]Tielsch JM Darmstadt GL Mullany LC Impact of newborn skin-cleansing with chlorhexidine on neonatal mortality in southern Nepal: a community-based, cluster-randomized trial Pediatrics 2007 119 e330 e340 17210728 PMC2364722
  16. [20]Persson L-Å Arifeen S Ekstrom E-C Effects of prenatal micronutrient and early food supplementation on maternal hemoglobin, birthweight, and infant mortality among children in Bangladesh: the MINIMat randomized trial JAMA 2012 307 2050 59 22665104
  17. [21]Joglekar CV Fall CHD Deshpande VU Newborn size, infant and childhood growth, and body composition and cardiovascular disease risk factors at the age of 6 years: the Pune Maternal Nutrition Study Int J Obes (Lond) 2007 31 1534 1544 17653070 PMC2358952
  18. [22]Krishnaveni GV Hill JC Veena SR Truncal adiposity is present at birth and in early childhood in South Indian children Indian Pediatr 2005 42 527 38 15995269
  19. [23]Zeng L Dibley MJ Cheng Y Impact of micronutrient supplementation during pregnancy on birthweight, duration of gestation, and perinatal mortality in rural western China: double blind cluster randomised controlled trial BMJ 2008 337 a2001 18996930 PMC2577799
  20. [24]Zhang X Liu E Tian Z High birthweight and over-weight or obesity among Chinese children 3–6 years old Prev Me 2009 49 172 178 19632265
  21. [25]Adair LS Guilkey DK Age-specific determinants of stunting in Filipino children J Nutr 1997 127 314 20 9039833
  22. [26]Richter L Norris S Pettifor J Yach D Cameron N Cohort Profile: Mandela’s children: the 1990 Birth to Twenty study in South Africa Int J Epidemiol 2007 36 504 11 17355979 PMC2702039
  23. [27]Huybregts L Roberfroid D Lanou H Prenatal food supplementation fortified with multiple micronutrients increases birth length: a randomized controlled trial in rural Burkina Faso Am J Clin Nutr 2009 90 1593 600 19812173
  24. [28]Roberfroid D Huybregts L Lanou H Effects of maternal multiple micronutrient supplementation on fetal growth: a double-blind randomized controlled trial in rural Burkina Faso Am J Clin Nutr 2008 88 1330 40 18996870
  25. [29]Roberfroid D Huybregts L Lanou H Impact of prenatal multiple micronutrients on survival and growth during infancy: a randomized controlled trial Am J Clin Nutr 2012 95 916 24 22378724
  26. [30]Malaba LC Iliff PJ Nathoo KJ Effect of postpartum maternal or neonatal vitamin A supplementation on infant mortality among infants born to HIV-negative mothers in Zimbabwe Am J Clin Nutr 2005 81 454 60 15699235
  27. [31]Maleta K Virtanen SM Espo M Kulmala T Ashorn P Childhood malnutrition and its predictors in rural Malawi Paediatr Perinat Epidemiol 2003 17 384 90 14629321
  28. [32]Fawzi WW Msamanga GI Urassa W Vitamins and perinatal outcomes among HIV-negative women in Tanzania N Engl J Med 2007 356 1423 31 17409323
  29. [33]ter Kuile FO Terlouw DJ Kariuki SK Impact of permethrin-treated bed nets on malaria, anemia, and growth in infants in an area of intense perennial malaria transmission in western Kenya Am J Trop Med Hyg 2003 68 68 77 12749488
  30. [34]Victora CG Barros FC Cohort Profile: the 1982 Pelotas (Brazil) birth cohort study Int J Epidemiol 2006 35 237 42 16373375
  31. [35]Victora CG Hallal PC Araujo CL Menezes AM Wells JC Barros FC Cohort Profile: the 1993 Pelotas (Brazil) birth cohort study Int J Epidemiol 2008 37 704 09 17846051
  32. [36]Santos IS Barros AJ Matijasevich A Dominques MR Barros FC Victora CG Cohort Profile: the 2004 Pelotas (Brazil) birth cohort study Int J Epidemiol 2011 40 1461 1468 20702597 PMC3235016
  33. [37]Stein AD Melgar P Hoddinott J Martorell R Cohort Profile: the Institute of Nutrition of Central America and Panama (INCAP) Nutrition Trial Cohort Study Int J Epidemiol 2008 37 716 20 18285366 PMC4439516
  34. [38]Ramakrishnan U Stein AD Parra-Cabrera S Effects of docosahexaenoic acid supplementation during pregnancy on gestational age and size at birth: randomized, double-blind, placebo-controlled trial in Mexico Food Nutr Bull 2010 31 S108 16 20715595
  35. [39]Katz J Lee ACC Kozuki N Born too small or too soon: a pooled analysis of mortality risk among preterm and small-for-gestational-age infants in low- and middle-income countries Lancet 2013 (In press) PMC3796350 23746775
  36. [40]Lawn JE Cousens S Zupan J 4 million neonatal deaths: When? Where? Why? Lancet 2005 365 891 900 15752534
  37. [41]Schroeder DG Semba RD Bloem M Malnutrition Nutrition and Health in Developing Countries 2008 Springer Totowa, NJ 2nd edn
  38. [42]Schmidt MK Muslimatun S West CE Schultink W Gross R Haitvast JG Nutritional status and linear growth of Indonesian infants in West Java are determined more by prenatal environment than by postnatal factors J Nutr 2002 132 2202 07 12163663
  39. [43]Chaffee BW King JC Effect of zinc supplementation on pregnancy and infant outcomes: a systematic review Paediatr Perinat Epidemiol 2012 26 118 37 22742606 PMC3787719
  40. [44]Imdad A Bhutta ZA Maternal nutrition and birth outcomes. Effect of balanced protein-energy supplementation Paediatr Perinat Epidemiol 2012 26 178 90 22742610
  41. [45]Ramakrishnan U Grant FK Goldenberg T Bui V Imdad A Bhutta ZA Effect of multiple micronutrient supplementation on pregnancy and infant outcomes: a systematic review Paediatr Perinat Epidemiol 2012 26 153 67 22742608
  42. [46]Jiang T Christian P Khatry SK Wu L West KP Jr Micronutrient deficiencies in early pregnancy are common, concurrent, and vary by season among rural Nepali pregnant women J Nutr 2005 135 1106 12 15867289
  43. [47]Khan AI Kabir I Ekstrom E-C Effects of prenatal food and micronutrient supplementation on child growth from birth to 54 months of age: a randomized trial in Bangladesh Nutr J 2011 10 134 22152147 PMC3274449
  44. [48]Kinra S Rameshwar Sarma KV Ghafoorunissa Effect of integration of supplemental nutrition with public health programmes in pregnancy and early childhood on cardiovascular risk in rural Indian adolescents: long term follow up of Hyderabad nutrition trial BMJ 2008 337 a605 18658189 PMC2500199
  45. [49]Kramer MS The epidemiology of adverse pregnancy outcomes: an overview J Nutr 2003 133 1592S 96S 12730473
  46. [50]Ozaltin E Hill K Subramanian SV Association of maternal stature with offspring mortality, underweight, and stunting in low- to middle-income countries JAMA 2010 303 1507 16 20407060 PMC3100588
  47. [51]Christian P Maternal height and risk of child mortality and undernutrition. Editorial JAMA 2010 303 1539 49 20407066
  48. [52]Christian P Lammi-Keefe CJ Couch SC Philipson EH Nutrition and maternal mortality in developing countries Handbook of Nutrition and Pregnancy 2008 Humana Press Totowa, NJ
  49. [53]Demerath EW Choh AC Czerwinski SA Genetic and environmental influences on infant weight and weight change: the Fels Longitudinal Study Am J Hum Biol 2007 19 692 702 17639582 PMC2801417

Cited by

Sorted by citations

Authors
Christian, P., Lee, S. E., Donahue Angel, M., Adair, L. S., Arifeen, S. E., Ashorn, P., Barros, F. C., Fall, C. H., Fawzi, W. W., Hao, W., Hu, G., Humphrey, J. H., Huybregts, L., Joglekar, C. V., Kariuki, S. K., Kolsteren, P., Krishnaveni, G. V., Liu, E., Martorell, R., Osrin, D., Persson, L.-A., Ramakrishnan, U., Richter, L., Roberfroid, D., Sania, A., Ter Kuile, F. O., Tielsch, J., Victora, C. G., Yajnik, C. S., Yan, H., Zeng, L., & Black, R. E.
Affiliations
  • Universidade Católica de Pelotas (BR)
  • Johns Hopkins University (US)
  • University of North Carolina at Chapel Hill (US)
  • International Centre for Diarrhoeal Disease Research (BD)
  • Tampere University (FI)
  • Southampton General Hospital (GB)
  • Harvard University (US)
  • Emory University (US)
  • Pennington Biomedical Research Center (US)
  • Ghent University (BE)
  • King Edward Memorial Hospital Research Centre (IN)
  • Kenya Medical Research Institute (KE)
  • CSI Holdsworth Memorial Hospital (IN)
  • Tianjin Women's and Children's Health Center (CN)
  • Centers for Disease Control and Prevention (US)
  • Human Sciences Research Council (ZA)
  • U.S. President's Malaria Initiative (US)
  • George Washington University (US)
  • Universidade Federal de Pelotas (BR)
  • Xi'an Jiaotong University (CN)
Corresponding author
Christian, Parul
ORCID
Venue
International Journal of Epidemiology
Publisher
Oxford University Press (OUP)
Published
2013-08-06
Volume
42
Issue
5
Pages
1340-1355
ISSN
  • 0300-5771 (ISSN-L)
  • 1464-3685
DOI
10.1093/ije/dyt109
PMC
PMC3816349
OpenAlex
W2168268121
Cited by
582
References
1
Citations by year
2026: 35 · 2025: 36 · 2024: 44 · 2023: 74 · 2022: 51 · 2021: 81 · 2020: 59 · 2019: 35 · 2018: 43 · 2017: 42 · 2016: 38 · 2015: 29 · 2014: 9 · 2013: 6
FWCI
3.09
Type
journal article
Language
en
Open access
Locations
  • International Journal of Epidemiology (publishedVersion)
  • Europe PMC (PubMed Central) (publishedVersion)
  • PubMed Central (publishedVersion)
  • PubMed (publishedVersion)
  • Carolina Digital Repository (University of North Carolina at Chapel Hill) (submittedVersion)
  • Data Archiving and Networked Services (DANS) (submittedVersion)
  • LSTM Online Archive (Liverpool School of Tropical Medicine) (submittedVersion)
  • Ghent University Academic Bibliography (Ghent University) (submittedVersion)
  • ePrints Soton (University of Southampton) (submittedVersion)
  • UCL Discovery (University College London) (submittedVersion)
  • HighWire Press Open Archive (submittedVersion)
  • UNC Libraries
Funders
  • Bill and Melinda Gates Foundation (810–2054)
  • UNICEF
  • Johns Hopkins University
  • Wellcome Trust (083460, 098575, 091561, 100714, 079877, 059609)
  • Tampereen Yliopisto
  • National Institutes of Health (2r24hd050924-06)
  • Centers for Disease Control and Prevention
  • Johns Hopkins Bloomberg School of Public Health
  • Medical Research Council (MC_UU_12011/3)
  • Eunice Kennedy Shriver National Institute of Child Health and Human Development (R24 HD-050924)
Topics
  • Health Sciences › Nursing › Nutrition and Dietetics › Child Nutrition and Water Access
  • Health Sciences › Medicine › Pediatrics, Perinatology and Child Health › Birth, Development, and Health
  • Health Sciences › Medicine › Pediatrics, Perinatology and Child Health › Public Health and Nutrition
Keywords
child undernutrition, stunting, small for gestational age, preterm birth, fetal growth restriction, low birth weight, wasting, underweight, child anthropometry, population attributable risk, low- and middle-income countries
MeSH terms
Child, Preschool, Developing Countries, Female, Fetal Growth Retardation, Gestational Age, Humans, Infant, Infant, Low Birth Weight, Infant, Premature, Infant, Small for Gestational Age, Longitudinal Studies, Male, Pregnancy, Risk Factors, Cohort Studies, Malnutrition, Premature Birth

About these checks

Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.

Statistics and arithmetic are recomputed, not judged.

Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.

What counts as a claim ›How we measure confidence ›How we check this ›

Are you an author, or do you see a problem with this page? Request a review