COMMENTARY
Should We Use Customized Fetal Growth Percentiles in Urban Canada? Nir Melamed, MD, MSc,1 Joel G. Ray, MD, MSc,2 Prakesh S. Shah, MD,3 Howard Berger, MD,2 John C. Kingdom, MD, FRCSC1 Maternal-Fetal Medicine Division (Placenta Clinic), Department of Obstetrics and Gynaecology, Mount Sinai Hospital, University of Toronto, Toronto ON
1
Department of Obstetrics and Gynaecology, St. Michael’s Hospital, University of Toronto, Toronto ON
2
Department of Pediatrics, Mount Sinai Hospital, University of Toronto, Toronto ON
3
Abstract An increasingly common challenge in antenatal care of the small for gestational age (SGA) fetus is the distinction between the constitutionally (physiologically) small fetus and the fetus affected by pathological intrauterine growth restriction (IUGR). We discuss here the rationale and the evidence for the use of customized growth percentiles for the purpose of distinguishing between the fetus with true IUGR and the fetus with constitutional SGA. We also provide estimates of the potential effects of adopting ethnicity-specific birth weight curves on the rates of SGA and large for gestational age status in multi-ethnic metropolitan cities in North America and Europe, such as the City of Toronto. Using customized growth percentiles would result in a considerable decline in the rate of a false-positive diagnosis of SGA among visible minorities, and improve the detection rate of true large for gestational age fetuses among these groups.
Résumé La distinction entre les fœtus constitutionnellement (physiologiquement) petits et les fœtus affectés par un retard de croissance intra-utérin pathologique (RCIU) constitue un défi de plus en plus commun dans le cadre des soins prénataux prodigués aux fœtus présentant une hypotrophie fœtale (HF). Nous discutons ici de la logique et des données soutenant l’utilisation de percentiles de croissance adaptés aux fins de la distinction entre les fœtus présentant un réel RCIU et les fœtus présentant une HF constitutionnelle. Nous offrons également des estimations des effets potentiels de l’adoption de courbes de poids de naissance propres à une origine ethnique particulière sur les taux de fœtus présentant une HF et les taux de fœtus présentant une hypertrophie fœtale au sein de villes métropolitaines multiethniques d’Amérique du Nord et d’Europe (comme la ville de Toronto). L’utilisation de percentiles de croissance adaptés se traduirait en une baisse considérable du taux de diagnostic faux positif d’HF chez les minorités visibles, ainsi qu’en une amélioration du taux de détection des fœtus présentant une réelle hypertrophie fœtale chez ces groupes. Key Words: Customized, growth, percentiles Competing Interests: None declared.
THE NATURE OF THE PROBLEM
A
32-year-old nulliparous woman of South Asian origin is seen by her obstetrician at 33 weeks of gestation. Her pregnancy has been uncomplicated to date, but her physician is concerned that the fetus is small, on the basis of a symphysis-fundal height equivalent to a pregnancy of 31 weeks’ GA. An ultrasound examination is performed, and the EFW is at the fifth percentile for GA. The woman’s height is 152 cm and her weight is 60 kg. The current pregnancy was accurately dated by a first trimester ultrasound. One week later, a repeat ultrasound examination reveals a normal biophysical profile score, a normal amniotic fluid index, and normal umbilical artery Doppler waveforms. Her obstetrician feels that this is most likely a healthy, constitutionally SGA fetus, but agrees to continue weekly fetal monitoring thereafter as a precaution. At 37 weeks, the EFW is at the third percentile for GA, while the biophysical score, amniotic fluid index, and Doppler waveforms remain normal. However, her obstetrician expresses discomfort with further expectant management, and recommends delivery. Two days later, after failed induction of labour, the woman undergoes Caesarean section. Although the Apgar scores are normal, the newborn is admitted to the NICU for five days following respiratory difficulties attributed to transient tachypnea of the newborn and delayed adaptation to extrauterine life. This case illustrates that a diagnosis of SGA in the fetus may result in cautionary behaviour on the part of the clinician (which may inadvertently heighten maternal
Received on September 7, 2013 Accepted on October 11, 2013
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Should We Use Customized Fetal Growth Percentiles in Urban Canada?
and infant surveillance) and interventions that may in turn result in “iatrogenic” morbidity. This case also suggests that better tools are needed to aid the clinician in distinguishing between two forms of fetal SGA.1 The first is the constitutionally small fetus, defined as a fetus with an estimated weight or birth weight below the 10th percentile for gestational age, but whose “smallness” is merely attributed to genetic growth potential, without related negative effects on health. The second form of SGA arises from fetal IUGR, wherein physiologically regulated growth is impeded by one or more pathologic factors, such as placental dysfunction.2 Although pathological IUGR is commonly suspected when the estimated fetal weight is below the 10th percentile for gestational age, IUGR can be present even when the fetal weight is above the 10th percentile for gestational age.3,4 In contrast to constitutional SGA, pathological IUGR is associated with an increased risk of adverse outcomes, including stillbirth, neonatal mortality and morbidity, and long-term adverse outcomes.5–7 Current tools used to distinguish between constitutional SGA and pathological IUGR include the biophysical profile score, amniotic fluid volume, and umbilical artery Doppler studies.8 However, the sensitivity of these standard tools may be limited, especially in cases of lateonset IUGR.9 Doppler studies of the fetal middle cerebral artery9 and uterine artery10 may identify the at-risk SGA fetus near term, in whom induction of labour or Caesarean section might be justified to avoid stillbirth. However, these methods require ultrasound expertise, adding further to the costs of antenatal care, with no proven high-level evidence of benefit. Another approach to distinguish between pathological IUGR and constitutional SGA is through the use of customized fetal growth percentiles. Such customized measures account for factors that affect normal physiologic variation in fetal growth and weight, and therefore may be of special importance in Canadian communities with high ethnic diversity among whom there may be differences in normal fetal growth.
ABBREVIATIONS EFW
estimated fetal weight
GA
gestational age
IUGR
intrauterine growth restriction
LGA
large for gestational age
SGA
small for gestational age
CUSTOMIZED PERCENTILES: THE CONCEPT
The concept of customized growth percentiles was articulated by Gardosi et al. in 1992.11 These authors suggested that intrauterine fetal growth (i.e., fetal growth potential) is affected by multiple physiological (rather than pathological) factors that contribute to normal variation in birth weight. Thus, it is unreasonable to judge the growth of all fetuses according to uniform population-based curves, although this practice is all too common in most clinical settings, including in Canada. Customization (i.e., personalization) allows the clinician to better evaluate each pregnancy for the presence of reduced fetal growth by judging each fetus against its own predicted growth potential. Using multivariate analysis of birth weight data from uncomplicated pregnancies, Gardosi and colleagues identified several factors that consistently predicted fetal growth, including maternal ethnicity, parity, pre-pregnancy height and weight, and fetal sex.12,13 They calculated adjustment coefficients for each of these factors (per population studied) and then developed a software tool to determine the individual customized optimal birth weight at 40 weeks’ gestation for an individual fetus on the basis of the aforementioned variables. Next, Gardosi developed a “proportionality equation,” derived from the work of Hadlock et al.,14 and determined the proportion of the fetal weight at 40 weeks’ gestation that is achieved at any given prior gestational age, assuming that these proportions are constant for all fetuses. By combining the individual term optimal weight at 40 weeks with the proportionality equation, Gardosi generated fetal growth curves specifically reflecting the growth potential of the individual non-pathologically affected fetus throughout pregnancy.12 Nevertheless, it should be emphasized that this approach was based on several assumptions that remain to be proven, including: 1. all fetuses grow in utero according to the same pattern (i.e., meeting the proportionality equation); 2. the effects of the various maternal and fetal predictors of fetal weight on the optimal weight, as well as the variation in optimal weight, are similar at different gestational ages; and 3. most of the variation in optimal weight is explained by gestational age and fetal sex. CUSTOMIZED PERCENTILES: THE EVIDENCE
Since the introduction by Gardosi et al.12 of the customized fetal growth concept, other researchers have generated population-specific adjustment coefficients and validated FEBRUARY JOGC FÉVRIER 2014 l 165
Commentary
Effect of adaptation of ethnicity-specific birth weight percentile curves on the rate of SGA and LGA in the population of Toronto
The graph presents the distribution of birth weight at 40 weeks based on the current national (Kramer et al.37) and South Asian-specific36 birth weight curves. The actual current SGA rate (18.3%) is demonstrated by the proportion of newborns below the current national 10th percentile threshold (Kramer et al.37: males [40 weeks]—3079 g, females [40 weeks]—2955 g) in the ethnicity-specific birth weight curves.35,36 The proportion is denoted by the areas under the graph: A (light blue, 8.3%) + B (orange, 10.0%). The new SGA rate (10.0%) in the case of adaptation of the ethnicity-specific birth weight curves is demonstrated by the proportion of newborns below the new ethnicity-specific 10th percentile threshold in the ethnicity-specific birth weight curves (2906 g).35,36 The proportion is denoted by the area under the graph: B (orange, 10.0%). The actual current LGA rate (3.7%) is demonstrated by the proportion of newborns above the current national 90th percentile threshold (Kramer et al.37: males [40 weeks]—4200 g, females [40 weeks]—4034 g) in the ethnicity-specific birth weight curves (Ray et al.36). The proportion is denoted by the area under the graph: C (light blue, 3.7%). The new LGA rate (10.0%) in the case of adaptation of the ethnicity-specific BW curves is demonstrated by the proportion of newborns above the new ethnicity-specific 90th percentile threshold in the ethnicity-specific birth weight curves (4018g) (Ray et al.36). The proportion is denoted by the areas under the graph: C (light blue, 3.7%) + D (orange, 6.3%).
the benefits of using customized growth percentiles in multiple populations in countries including the United Kingdom, Sweden, Australia, New Zealand, Ireland, Spain, and the United States.11,15–19 Use of customized growth percentiles decreases both the false-positive and falsenegative rates of SGA below the 10th percentile, reflected by the observation that fetuses with a diagnosis of SGA below their customized 10th percentile are at considerably higher risk for adverse outcomes (stillbirth, neonatal death, neonatal morbidity, cerebral palsy, and longterm neurodevelopmental and metabolic abnormalities) compared with using the 10th percentile cut-point on a uniform population-based curve.20–26 Indeed, in the case of “unexplained” stillbirth, using customized growth curves introduces unrecognized IUGR as a contributing factor in as many as 40% of cases.27 More recent studies have observed, at the other end of the spectrum, that identifying an LGA fetus above the 90th percentile using customized growth 166 l FEBRUARY JOGC FÉVRIER 2014
percentiles better predicts LGA-related complications than does using uniform population-based curves.26 An online web-based software program has improved access to the calculation of customized percentiles.28 The Royal College of Obstetricians and Gynaecologists endorsed the use of customized growth percentiles in its recent Green Top Guideline “The investigation and management of the small for gestational age fetus.”29 Alternative methods for the customization of growth percentiles have been explored during recent years. In a recent study,30 Mikolajczyk et al. explored a simplified customization approach in which the fetal growth curve published by Hadlock et al.14 is adjusted to a local population by multiplying the calculated weight at each gestational age by a constant factor, namely, the ratio between the observed mean birth weight in the local population at 40 weeks’ gestation and the estimated weight at 40 weeks according to the fetal growth curve published by Hadlock et al. Following validation, using data from a large WHO global survey from 24 countries in Africa, Asia, and Latin America, the authors concluded that the performance of this simplified method is comparable to the full customization approach developed by Gardosi.12 Several investigators have challenged the concept of customized growth percentiles. Hutcheon et al.31 suggested that the main reason for the better performance of the customized growth percentiles is that they use ultrasoundbased fetal growth curves, rather than birth weight-based curves, yet the latter form the basis for most national population-based curves. The authors also found that the variables used in Gardosi’s model12 accounted for only 25% of the birth weight variability.31 In another recent study, Hutcheon et al. ran a simulation analysis of a hypothetic cohort using a database from the Royal Victoria Hospital in Montreal and, again, suggested that the customized approach adds little predictive ability.32,33 However, the interpretation of this sophisticated analysis depends to a large extent on the validity of the multiple assumptions that formed the basis for this analysis, which remains to be proven. SHOULD CUSTOMIZED PERCENTILES BE USED IN URBAN CANADA?
A considerable amount of evidence has accumulated during recent years to support the adoption of customization methods for fetal growth and the detection of IUGR, even when used with sonographic fetal weight estimation rather than birth weight.34 We suggest that the benefits of customization are likely to be substantial, especially within the multi-ethnic communities found in large urban centres across Canada.
12.3
12.6
8.5
3.1
5.1
2.8
Ethnic group
South Asian
Southeast and East Asian
African and Caribbean
Middle Eastern and North African
Filipino
Latin American
3514
3398
3501
3462
3432
3389
Median
3005
2928
3018
2958
2963
2906
10th percentile
15.6 (15.0 to 16.3)
11.7 (11.0 to 12.4)
17.6 (16.2 to 19.0)
11.7 (11.0 to 12.3)
14.9 (14.4 to 15.5)
14.6 (14.3 to 14.9)
18.3 (17.6 to 19.0)
SGA rate according to current thresholds, % (95% CI)‡
10.0
10.0
10.0
10.0
10.0
10.0
10.0
New rate (%)
–5.6 (–6.3 to –5.0)
–1.7 (–2.4 to –1.0)
–7.6 (–9.0 to –6.2)
–1.7 (–2.3 to –1.0)
–4.9 (–5.5 to –4.4)
–4.6 (–4.9 to –4.3)
–8.3 (–9.0 to –7.6)
Absolute change, % (95% CI)
–36.0 (–38.6 to –33.3)
–14.2 (–19.1 to –9.0)
–43.0 (–47.4 to –38.1)
–14.2 (–18.9 to –9.2)
–33.0 (–35.5 to –30.4)
–31.5 (–32.9 to –30.1)
–45.2 (–47.3 to –43.1)
Relative change, % (95% CI)
‡The proportion of newborns in each ethnic group who might be currently classified as SGA using the 10th percentile threshold within the Canadian growth curves published by Kramer et al.37 For males and females at 40 weeks’ gestation the thresholds are 3079 g and 2955 g, respectively.
56 (50 to 63)
17 (10 to 24)
76 (62 to 90)
17 (10 to 23)
49 (44 to 55)
46 (43 to 49)
83 (76 to 90)
Fetuses that would no longer be “incorrectly” identified as SGA (per 1000 fetuses), n (95% CI)
Proposed effect of adopting ethnicity-specific birth weight curves on the rate of SGA
†Based on recently published population-based birth weight percentile curves (Ray et al.35,36). Values represent the median and 10th percentile of birth weight at 40 weeks of gestation.
*Based on the 2011 National Household Survey.39
Overall
Prevalence of that ethnic group in Toronto*
Ethnicity-specific birth weight curve values at 40 weeks, grams†
Table 1. Effect of the use of ethnicity-specific birth weight percentile curves on the rate of SGA diagnoses in the population of Toronto
Should We Use Customized Fetal Growth Percentiles in Urban Canada?
FEBRUARY JOGC FÉVRIER 2014 l 167
168 l FEBRUARY JOGC FÉVRIER 2014
12.3
12.6
8.5
3.1
5.1
2.8
Ethnic group
South Asian
Southeast and East Asian
African and Caribbean
Middle Eastern and North African
Filipino
Latin American
3514
3398
3501
3462
3432
3389
Median
4138
4025
4139
4120
4039
4018
10th percentile
4.7 (4.4 to 4.9)
7.3 (6.8 to 7.8)
3.8 (3.4 to 4.3)
6.3 (5.9 to 6.8)
6.2 (5.9 to 6.5)
4.0 (3.9 to 4.1)
3.7 (3.5 to 3.9)
LGA rate according to current thresholds, % (95% CI)‡
10.0
10.0
10.0
10.0
10.0
10.0
10.0
New rate (%)
5.3 (5.1 to 5.6)
2.7 (2.2 to 3.2)
6.2 (5.7 to 6.6)
3.7 (3.2 to 4.1)
3.8 (3.5 to 4.1)
6.0 (5.9 to 6.1)
6.3 (6.1 to 6.5)
Absolute change, % (95% CI)
113.8 (102.2 to 126.1)
37.6 (28.8 to 47.1)
161.4 (132.1 to 195.2)
57.7 (47.8 to 68.5)
62.4 (54.7 to 70.5)
152.0 (145.1 to 159.0)
168.5 (153.3 to 184.9)
Relative change, % (95% CI)
‡The proportion of newborns in each ethnic group who might be currently classified as LGA using the 90th percentile threshold within the Canadian growth curves published by Kramer et al.37 For males and females at 40 weeks gestation the thresholds are 4200 g and 4034 g, respectively.
53 (51 to 56)
27 (22 to 32)
62 (57 to 66)
37 (32 to 41)
38 (35 to 41)
60 (59 to 61)
63 (61 to 65)
Fetuses that would no longer be “incorrectly” identified as LGA (per 1000 fetuses), n (95% CI)
Proposed effect of adopting ethnicity-specific birth weight curves on the rate of LGA
†Based on recently published population-based birth weight percentile curves (Ray et al.35,36). Values represent the median and 90th percentile of birth weight at 40 weeks of gestation.
*Based on the 2011 National Household Survey.39
Overall
Prevalence of that ethnic group in Toronto*
Ethnicity-specific birth weight curve values at 40 weeks, grams†
Table 2. Effect of the use of ethnicity-specific birth weight percentile curves on the rate of LGA diagnoses in the population of Toronto
Commentary
Should We Use Customized Fetal Growth Percentiles in Urban Canada?
To illustrate this, we analyzed the effects of an adjustment for only a single factor—maternal ethnicity—on the rates of SGA and LGA in the diverse population of the city of Toronto as a representative of urban Canada, based on the recently published Ontario ethnicity-specific birth weight curves.35,36 The ethnic distribution of the population of Toronto, 49.1% of which are visible minorities, is presented in Table 1. We initially calculated the proportion of newborns in each ethnic group who might be currently classified as SGA using the 10th percentile threshold within the Canadian growth curves published by Kramer et al.37 (Figure and Table 1). Overall, 15.6% of pregnancies among the visible minority groups are currently classified as SGA, with rates varying by ethnic group (Table 1). Adoption of the ethnicity-specific curves would reduce the overall rate of SGA diagnoses among visible minorities by 36%, with relative reductions of 45% among the newborns of South Asian mothers and 43% among those of Filipina mothers (Table 1). A similar approach was used to analyze the effect of maternal ethnicity on the rate of LGA (Table 2 and Figure). Only 4.7% of newborns of visible minority mothers have birth weights above the national 90th percentile threshold.37 Again, this is most noticeable among South Asian and Filipina women (Table 2), meaning that most cases of LGA in these groups are not currently detected using national metrics of LGA. Adoption of growth curves that are customized for maternal ethnicity, especially in multi-ethnic urban areas like Toronto, may lead to a more accurate diagnosis of SGA and LGA. This may conceivably reduce the unnecessary use of health resources in obstetrical and neonatal care. Customization simply means moving from “clinical judgement” to a more formalized approach for the evaluation of fetal growth in antenatal care, based on a more quantitative, standardized, and objective process. Nevertheless, clinicians should bear in mind three potential limitations of the use of customized curves: first, there are mathematical assumptions that form the basis for this approach, as discussed above. Second, most models developed so far do not account for mixed ethnicity within couples. Third, models developed to date do not adjust for paternal factors. Notwithstanding these limitations, the reality is that important clinical decisions like induction of labour are commonly made on the basis of the sonographic estimation of fetal weight, which itself has a significant margin of imprecision and error.38 Importantly, while we have analyzed the effect of maternal ethnicity alone, adding other customized measures such as
maternal height, weight, and parity may further improve the predictive value. In addition, although we have focused on the possible benefits of the use of customized curves in urban Canada, rural Canada has also seen an increase in the proportion of immigrants and visible minorities, customized curves probably apply there too. The use of customized growth curves needs to be validated in large prospective multicentre studies with sufficient statistical power to detect significant adverse perinatal outcomes. ACKNOWLEDGEMENTS
Dr Kingdom is supported by the Rose Torno Chair at Mount Sinai Hospital. Dr Shah and Dr Ray are supported by Applied Research Chair in Reproductive and Child Health Services and Policy Research from the Canadian Institutes for Health Research. REFERENCES 1. Zhang J, Merialdi M, Platt LD, Kramer MS. Defining normal and abnormal fetal growth: promises and challenges. Am J Obstet Gynecol 2010;202:522–8. 2. Urquia ML, Ray JG. Seven caveats on the use of low birthweight and related indicators in health research. J Epidemiol Community Health 2012;66:971–5. 3. Stratton JF, Scanaill SN, Stuart B, Turner MJ. Are babies of normal birth weight who fail to reach their growth potential as diagnosed by ultrasound at increased risk? Ultrasound Obstet Gynecol 1995;5:114–8. 4. Owen P, Harrold AJ, Farrell T. Fetal size and growth velocity in the prediction of intrapartum caesarean section for fetal distress. Br J Obstet Gynaecol 1997;104:445–9. 5. Barker DJ, Gluckman PD, Godfrey KM, Harding JE, Owens JA, Robinson JS. Fetal nutrition and cardiovascular disease in adult life. Lancet 1993;341:938–41. 6. M Kady S, Gardosi J. Perinatal mortality and fetal growth restriction. Best Pract Res Clin Obstet Gynaecol 2004;18:397–410. 7. Jacobsson B, Ahlin K, Francis A, Hagberg G, Hagberg H, Gardosi J. Cerebral palsy and restricted growth status at birth: population-based case-control study. BJOG 2008;115:1250–5. 8. Lausman A, McCarthy FP, Walker M, Kingdom J. Screening, diagnosis, and management of intrauterine growth restriction. J Obstet Gynaecol Can 2012;34:17–28. 9. Oros D, Figueras F, Cruz-Martinez R, Meler E, Munmany M, Gratacos E. Longitudinal changes in uterine, umbilical and fetal cerebral Doppler indices in late-onset small-for-gestational age fetuses. Ultrasound Obstet Gynecol 2011;37:191–5. 10. Singh T, Leslie K, Bhide A, D’Antonio F, Thilaganathan B. Role of second-trimester uterine artery Doppler in assessing stillbirth risk. Obstet Gynecol 2012;119:256–61. 11. Gardosi J, Chang A, Kalyan B, Sahota D, Symonds EM. Customised antenatal growth charts. Lancet 1992;339:283–7. 12. Gardosi J, Mongelli M, Wilcox M, Chang A. An adjustable fetal weight standard. Ultrasound Obstet Gynecol 1995;6:168–74. 13. Gardosi J. Customized fetal growth standards: rationale and clinical application. Semin Perinatol 2004;28:33–40.
FEBRUARY JOGC FÉVRIER 2014 l 169
Commentary
14. Hadlock FP, Harrist RB, Martinez-Poyer J. In utero analysis of fetal growth: a sonographic weight standard. Radiology 1991;181:129–33. 15. McCowan L, Stewart AW, Francis A, Gardosi J. A customised birthweight centile calculator developed for a New Zealand population. Aust N Z J Obstet Gynaecol 2004;44:428–31. 16. Mongelli M, Figueras F, Francis A, Gardosi J. A customized birthweight centile calculator developed for an Australian population. Aust N Z J Obstet Gynaecol 2007;47:128–31. 17. Figueras F, Meler E, Iraola A, Eixarch E, Coll O, Figueras J, et al. Customized birthweight standards for a Spanish population. Eur J Obstet Gynecol Reprod Biol 2008;136:20–4. 18. Gardosi J, Francis A. A customized standard to assess fetal growth in a US population. Am J Obstet Gynecol 2009;201:25 e1–7. 19. Unterscheider J, Geary MP, Daly S, McAuliffe FM, Kennelly MM, Dornan J, et al. The customized fetal growth potential: a standard for Ireland. Eur J Obstet Gynecol Reprod Biol 2013;166:14–7. 20. de Jong CL, Gardosi J, Dekker GA, Colenbrander GJ, van Geijn HP. Application of a customised birthweight standard in the assessment of perinatal outcome in a high risk population. Br J Obstet Gynaecol 1998;105:531–5.
27. Gardosi J, Kady SM, McGeown P, Francis A, Tonks A. Classification of stillbirth by relevant condition at death (ReCoDe): population based cohort study. BMJ 2005;331:1113–7. 28. Network G. GROW (Gestation Related Optimal Weight): customised antenatal growth chart software; versions 5.x-8.x, 2000–2012. Available at: http://www.gestation.net. Accessed October 22, 2013. 29. Royal College of Obstetricians and Gynaecologists. The investigation and management of the small for gestational age fetus. Green Top Guideline No. 31, RCOG 2002. 30. Mikolajczyk RT, Zhang J, Betran AP, Souza JP, Mori R, Gülmezoglu AM, et al. A global reference for fetal-weight and birthweight percentiles. Lancet 2011;377:1855–61. 31. Hutcheon JA, Zhang X, Cnattingius S, Kramer MS, Platt RW. Customised birthweight percentiles: does adjusting for maternal characteristics matter? BJOG 2008;115:1397–404. 32. Hutcheon JA, Walker M, Platt RW. Assessing the value of customized birth weight percentiles. Am J Epidemiol 2011;173:459–67. 33. Hutcheon JA, Zhang X, Platt RW, Cnattingius S, Kramer MS. The case against customised birthweight standards. Paediatr Perinat Epidemiol 2011;25:11–6.
21. Clausson B, Gardosi J, Francis A, Cnattingius S. Perinatal outcome in SGA births defined by customised versus population-based birthweight standards. BJOG 2001;108:830–4.
34. Kase BA, Carreno CA, Blackwell SC. Customized estimated fetal weight: a novel antenatal tool to diagnose abnormal fetal growth. Am J Obstet Gynecol 2012;207.
22. McCowan LM, Harding JE, Stewart AW. Customized birthweight centiles predict SGA pregnancies with perinatal morbidity. BJOG 2005;112:1026–33.
35. De Souza LR, Urquia ML, Sgro M, Ray JG. One size does not fit all: differences in newborn weight among mothers of Philippine and other East Asian origin. J Obstet Gynaecol Can 2012;34:1026–37.
23. Figueras F, Figueras J, Meler E, Eixarch E, Coll O, Gratacos E, et al. Customised birthweight standards accurately predict perinatal morbidity. Arch Dis Child Fetal Neonatal Ed 2007;92:F277–80.
36. Ray JG, Sgro M, Mamdani MM, Glazier RH, Bocking A, Hilliard R, et al. Birth weight curves tailored to maternal world region. J Obstet Gynaecol Can 2012;34:159–71.
24. Gardosi J, Francis A. Adverse pregnancy outcome and association with small for gestational age birthweight by customized and population-based percentiles. Am J Obstet Gynecol 2009;201:28 e1–8.
37. Kramer MS, Platt RW, Wen SW, Joseph KS, Allen A, Abrahamowicz M, et al. A new and improved population-based Canadian reference for birth weight for gestational age. Pediatrics 2001;108:E35.
25. Charkaluk ML, Marchand-Martin L, Ego A, et al. The influence of fetal growth reference standards on assessment of cognitive and academic outcomes of very preterm children. J Pediatr 2012;161:1053–8.
38. Melamed N, Yogev Y, Meizner I, Mashiach R, Bardin R, Ben-Haroush A. Sonographic fetal weight estimation: which model should be used? J Ultrasound Med 2009;28:617–29.
26. Mattos SS, Chaves ME, Costa SM, Zeitlin J, Arnaud C, Burguet A, et al.; Epipage Study Group. Which growth criteria better predict fetal programming? Arch Dis Child Fetal Neonatal Ed 2013;98:F81–4.
39. Statistics Canada. National Household Survey (NHS) 2001. Available at: http://www12.statcan.gc.ca/nhs-enm/index-eng.cfm. Accessed July 26, 2013. Ottawa (ON): Statistics Canada; 2001.
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Should We Use Customized Fetal Growth Percentiles in Urban Canada? Nir Melamed, MD, MSc,1 Joel G. Ray, MD, MSc,2 Prakesh S. Shah, MD,3 Howard Berger, MD,2 John C. Kingdom, MD, FRCSC1 Maternal-Fetal Medicine Division (Placenta Clinic), Department of Obstetrics and Gynaecology, Mount Sinai Hospital, University of Toronto, Toronto ON
1
Department of Obstetrics and Gynaecology, St. Michael’s Hospital, University of Toronto, Toronto ON
2
Department of Pediatrics, Mount Sinai Hospital, University of Toronto, Toronto ON
3
Abstract An increasingly common challenge in antenatal care of the small for gestational age (SGA) fetus is the distinction between the constitutionally (physiologically) small fetus and the fetus affected by pathological intrauterine growth restriction (IUGR). We discuss here the rationale and the evidence for the use of customized growth percentiles for the purpose of distinguishing between the fetus with true IUGR and the fetus with constitutional SGA. We also provide estimates of the potential effects of adopting ethnicity-specific birth weight curves on the rates of SGA and large for gestational age status in multi-ethnic metropolitan cities in North America and Europe, such as the City of Toronto. Using customized growth percentiles would result in a considerable decline in the rate of a false-positive diagnosis of SGA among visible minorities, and improve the detection rate of true large for gestational age fetuses among these groups.
Résumé La distinction entre les fœtus constitutionnellement (physiologiquement) petits et les fœtus affectés par un retard de croissance intra-utérin pathologique (RCIU) constitue un défi de plus en plus commun dans le cadre des soins prénataux prodigués aux fœtus présentant une hypotrophie fœtale (HF). Nous discutons ici de la logique et des données soutenant l’utilisation de percentiles de croissance adaptés aux fins de la distinction entre les fœtus présentant un réel RCIU et les fœtus présentant une HF constitutionnelle. Nous offrons également des estimations des effets potentiels de l’adoption de courbes de poids de naissance propres à une origine ethnique particulière sur les taux de fœtus présentant une HF et les taux de fœtus présentant une hypertrophie fœtale au sein de villes métropolitaines multiethniques d’Amérique du Nord et d’Europe (comme la ville de Toronto). L’utilisation de percentiles de croissance adaptés se traduirait en une baisse considérable du taux de diagnostic faux positif d’HF chez les minorités visibles, ainsi qu’en une amélioration du taux de détection des fœtus présentant une réelle hypertrophie fœtale chez ces groupes. Key Words: Customized, growth, percentiles Competing Interests: None declared.
THE NATURE OF THE PROBLEM
A
32-year-old nulliparous woman of South Asian origin is seen by her obstetrician at 33 weeks of gestation. Her pregnancy has been uncomplicated to date, but her physician is concerned that the fetus is small, on the basis of a symphysis-fundal height equivalent to a pregnancy of 31 weeks’ GA. An ultrasound examination is performed, and the EFW is at the fifth percentile for GA. The woman’s height is 152 cm and her weight is 60 kg. The current pregnancy was accurately dated by a first trimester ultrasound. One week later, a repeat ultrasound examination reveals a normal biophysical profile score, a normal amniotic fluid index, and normal umbilical artery Doppler waveforms. Her obstetrician feels that this is most likely a healthy, constitutionally SGA fetus, but agrees to continue weekly fetal monitoring thereafter as a precaution. At 37 weeks, the EFW is at the third percentile for GA, while the biophysical score, amniotic fluid index, and Doppler waveforms remain normal. However, her obstetrician expresses discomfort with further expectant management, and recommends delivery. Two days later, after failed induction of labour, the woman undergoes Caesarean section. Although the Apgar scores are normal, the newborn is admitted to the NICU for five days following respiratory difficulties attributed to transient tachypnea of the newborn and delayed adaptation to extrauterine life. This case illustrates that a diagnosis of SGA in the fetus may result in cautionary behaviour on the part of the clinician (which may inadvertently heighten maternal
Received on September 7, 2013 Accepted on October 11, 2013
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J Obstet Gynaecol Can 2014;36(2):164–170
Should We Use Customized Fetal Growth Percentiles in Urban Canada?
and infant surveillance) and interventions that may in turn result in “iatrogenic” morbidity. This case also suggests that better tools are needed to aid the clinician in distinguishing between two forms of fetal SGA.1 The first is the constitutionally small fetus, defined as a fetus with an estimated weight or birth weight below the 10th percentile for gestational age, but whose “smallness” is merely attributed to genetic growth potential, without related negative effects on health. The second form of SGA arises from fetal IUGR, wherein physiologically regulated growth is impeded by one or more pathologic factors, such as placental dysfunction.2 Although pathological IUGR is commonly suspected when the estimated fetal weight is below the 10th percentile for gestational age, IUGR can be present even when the fetal weight is above the 10th percentile for gestational age.3,4 In contrast to constitutional SGA, pathological IUGR is associated with an increased risk of adverse outcomes, including stillbirth, neonatal mortality and morbidity, and long-term adverse outcomes.5–7 Current tools used to distinguish between constitutional SGA and pathological IUGR include the biophysical profile score, amniotic fluid volume, and umbilical artery Doppler studies.8 However, the sensitivity of these standard tools may be limited, especially in cases of lateonset IUGR.9 Doppler studies of the fetal middle cerebral artery9 and uterine artery10 may identify the at-risk SGA fetus near term, in whom induction of labour or Caesarean section might be justified to avoid stillbirth. However, these methods require ultrasound expertise, adding further to the costs of antenatal care, with no proven high-level evidence of benefit. Another approach to distinguish between pathological IUGR and constitutional SGA is through the use of customized fetal growth percentiles. Such customized measures account for factors that affect normal physiologic variation in fetal growth and weight, and therefore may be of special importance in Canadian communities with high ethnic diversity among whom there may be differences in normal fetal growth.
ABBREVIATIONS EFW
estimated fetal weight
GA
gestational age
IUGR
intrauterine growth restriction
LGA
large for gestational age
SGA
small for gestational age
CUSTOMIZED PERCENTILES: THE CONCEPT
The concept of customized growth percentiles was articulated by Gardosi et al. in 1992.11 These authors suggested that intrauterine fetal growth (i.e., fetal growth potential) is affected by multiple physiological (rather than pathological) factors that contribute to normal variation in birth weight. Thus, it is unreasonable to judge the growth of all fetuses according to uniform population-based curves, although this practice is all too common in most clinical settings, including in Canada. Customization (i.e., personalization) allows the clinician to better evaluate each pregnancy for the presence of reduced fetal growth by judging each fetus against its own predicted growth potential. Using multivariate analysis of birth weight data from uncomplicated pregnancies, Gardosi and colleagues identified several factors that consistently predicted fetal growth, including maternal ethnicity, parity, pre-pregnancy height and weight, and fetal sex.12,13 They calculated adjustment coefficients for each of these factors (per population studied) and then developed a software tool to determine the individual customized optimal birth weight at 40 weeks’ gestation for an individual fetus on the basis of the aforementioned variables. Next, Gardosi developed a “proportionality equation,” derived from the work of Hadlock et al.,14 and determined the proportion of the fetal weight at 40 weeks’ gestation that is achieved at any given prior gestational age, assuming that these proportions are constant for all fetuses. By combining the individual term optimal weight at 40 weeks with the proportionality equation, Gardosi generated fetal growth curves specifically reflecting the growth potential of the individual non-pathologically affected fetus throughout pregnancy.12 Nevertheless, it should be emphasized that this approach was based on several assumptions that remain to be proven, including: 1. all fetuses grow in utero according to the same pattern (i.e., meeting the proportionality equation); 2. the effects of the various maternal and fetal predictors of fetal weight on the optimal weight, as well as the variation in optimal weight, are similar at different gestational ages; and 3. most of the variation in optimal weight is explained by gestational age and fetal sex. CUSTOMIZED PERCENTILES: THE EVIDENCE
Since the introduction by Gardosi et al.12 of the customized fetal growth concept, other researchers have generated population-specific adjustment coefficients and validated FEBRUARY JOGC FÉVRIER 2014 l 165
Commentary
Effect of adaptation of ethnicity-specific birth weight percentile curves on the rate of SGA and LGA in the population of Toronto
The graph presents the distribution of birth weight at 40 weeks based on the current national (Kramer et al.37) and South Asian-specific36 birth weight curves. The actual current SGA rate (18.3%) is demonstrated by the proportion of newborns below the current national 10th percentile threshold (Kramer et al.37: males [40 weeks]—3079 g, females [40 weeks]—2955 g) in the ethnicity-specific birth weight curves.35,36 The proportion is denoted by the areas under the graph: A (light blue, 8.3%) + B (orange, 10.0%). The new SGA rate (10.0%) in the case of adaptation of the ethnicity-specific birth weight curves is demonstrated by the proportion of newborns below the new ethnicity-specific 10th percentile threshold in the ethnicity-specific birth weight curves (2906 g).35,36 The proportion is denoted by the area under the graph: B (orange, 10.0%). The actual current LGA rate (3.7%) is demonstrated by the proportion of newborns above the current national 90th percentile threshold (Kramer et al.37: males [40 weeks]—4200 g, females [40 weeks]—4034 g) in the ethnicity-specific birth weight curves (Ray et al.36). The proportion is denoted by the area under the graph: C (light blue, 3.7%). The new LGA rate (10.0%) in the case of adaptation of the ethnicity-specific BW curves is demonstrated by the proportion of newborns above the new ethnicity-specific 90th percentile threshold in the ethnicity-specific birth weight curves (4018g) (Ray et al.36). The proportion is denoted by the areas under the graph: C (light blue, 3.7%) + D (orange, 6.3%).
the benefits of using customized growth percentiles in multiple populations in countries including the United Kingdom, Sweden, Australia, New Zealand, Ireland, Spain, and the United States.11,15–19 Use of customized growth percentiles decreases both the false-positive and falsenegative rates of SGA below the 10th percentile, reflected by the observation that fetuses with a diagnosis of SGA below their customized 10th percentile are at considerably higher risk for adverse outcomes (stillbirth, neonatal death, neonatal morbidity, cerebral palsy, and longterm neurodevelopmental and metabolic abnormalities) compared with using the 10th percentile cut-point on a uniform population-based curve.20–26 Indeed, in the case of “unexplained” stillbirth, using customized growth curves introduces unrecognized IUGR as a contributing factor in as many as 40% of cases.27 More recent studies have observed, at the other end of the spectrum, that identifying an LGA fetus above the 90th percentile using customized growth 166 l FEBRUARY JOGC FÉVRIER 2014
percentiles better predicts LGA-related complications than does using uniform population-based curves.26 An online web-based software program has improved access to the calculation of customized percentiles.28 The Royal College of Obstetricians and Gynaecologists endorsed the use of customized growth percentiles in its recent Green Top Guideline “The investigation and management of the small for gestational age fetus.”29 Alternative methods for the customization of growth percentiles have been explored during recent years. In a recent study,30 Mikolajczyk et al. explored a simplified customization approach in which the fetal growth curve published by Hadlock et al.14 is adjusted to a local population by multiplying the calculated weight at each gestational age by a constant factor, namely, the ratio between the observed mean birth weight in the local population at 40 weeks’ gestation and the estimated weight at 40 weeks according to the fetal growth curve published by Hadlock et al. Following validation, using data from a large WHO global survey from 24 countries in Africa, Asia, and Latin America, the authors concluded that the performance of this simplified method is comparable to the full customization approach developed by Gardosi.12 Several investigators have challenged the concept of customized growth percentiles. Hutcheon et al.31 suggested that the main reason for the better performance of the customized growth percentiles is that they use ultrasoundbased fetal growth curves, rather than birth weight-based curves, yet the latter form the basis for most national population-based curves. The authors also found that the variables used in Gardosi’s model12 accounted for only 25% of the birth weight variability.31 In another recent study, Hutcheon et al. ran a simulation analysis of a hypothetic cohort using a database from the Royal Victoria Hospital in Montreal and, again, suggested that the customized approach adds little predictive ability.32,33 However, the interpretation of this sophisticated analysis depends to a large extent on the validity of the multiple assumptions that formed the basis for this analysis, which remains to be proven. SHOULD CUSTOMIZED PERCENTILES BE USED IN URBAN CANADA?
A considerable amount of evidence has accumulated during recent years to support the adoption of customization methods for fetal growth and the detection of IUGR, even when used with sonographic fetal weight estimation rather than birth weight.34 We suggest that the benefits of customization are likely to be substantial, especially within the multi-ethnic communities found in large urban centres across Canada.
12.3
12.6
8.5
3.1
5.1
2.8
Ethnic group
South Asian
Southeast and East Asian
African and Caribbean
Middle Eastern and North African
Filipino
Latin American
3514
3398
3501
3462
3432
3389
Median
3005
2928
3018
2958
2963
2906
10th percentile
15.6 (15.0 to 16.3)
11.7 (11.0 to 12.4)
17.6 (16.2 to 19.0)
11.7 (11.0 to 12.3)
14.9 (14.4 to 15.5)
14.6 (14.3 to 14.9)
18.3 (17.6 to 19.0)
SGA rate according to current thresholds, % (95% CI)‡
10.0
10.0
10.0
10.0
10.0
10.0
10.0
New rate (%)
–5.6 (–6.3 to –5.0)
–1.7 (–2.4 to –1.0)
–7.6 (–9.0 to –6.2)
–1.7 (–2.3 to –1.0)
–4.9 (–5.5 to –4.4)
–4.6 (–4.9 to –4.3)
–8.3 (–9.0 to –7.6)
Absolute change, % (95% CI)
–36.0 (–38.6 to –33.3)
–14.2 (–19.1 to –9.0)
–43.0 (–47.4 to –38.1)
–14.2 (–18.9 to –9.2)
–33.0 (–35.5 to –30.4)
–31.5 (–32.9 to –30.1)
–45.2 (–47.3 to –43.1)
Relative change, % (95% CI)
‡The proportion of newborns in each ethnic group who might be currently classified as SGA using the 10th percentile threshold within the Canadian growth curves published by Kramer et al.37 For males and females at 40 weeks’ gestation the thresholds are 3079 g and 2955 g, respectively.
56 (50 to 63)
17 (10 to 24)
76 (62 to 90)
17 (10 to 23)
49 (44 to 55)
46 (43 to 49)
83 (76 to 90)
Fetuses that would no longer be “incorrectly” identified as SGA (per 1000 fetuses), n (95% CI)
Proposed effect of adopting ethnicity-specific birth weight curves on the rate of SGA
†Based on recently published population-based birth weight percentile curves (Ray et al.35,36). Values represent the median and 10th percentile of birth weight at 40 weeks of gestation.
*Based on the 2011 National Household Survey.39
Overall
Prevalence of that ethnic group in Toronto*
Ethnicity-specific birth weight curve values at 40 weeks, grams†
Table 1. Effect of the use of ethnicity-specific birth weight percentile curves on the rate of SGA diagnoses in the population of Toronto
Should We Use Customized Fetal Growth Percentiles in Urban Canada?
FEBRUARY JOGC FÉVRIER 2014 l 167
168 l FEBRUARY JOGC FÉVRIER 2014
12.3
12.6
8.5
3.1
5.1
2.8
Ethnic group
South Asian
Southeast and East Asian
African and Caribbean
Middle Eastern and North African
Filipino
Latin American
3514
3398
3501
3462
3432
3389
Median
4138
4025
4139
4120
4039
4018
10th percentile
4.7 (4.4 to 4.9)
7.3 (6.8 to 7.8)
3.8 (3.4 to 4.3)
6.3 (5.9 to 6.8)
6.2 (5.9 to 6.5)
4.0 (3.9 to 4.1)
3.7 (3.5 to 3.9)
LGA rate according to current thresholds, % (95% CI)‡
10.0
10.0
10.0
10.0
10.0
10.0
10.0
New rate (%)
5.3 (5.1 to 5.6)
2.7 (2.2 to 3.2)
6.2 (5.7 to 6.6)
3.7 (3.2 to 4.1)
3.8 (3.5 to 4.1)
6.0 (5.9 to 6.1)
6.3 (6.1 to 6.5)
Absolute change, % (95% CI)
113.8 (102.2 to 126.1)
37.6 (28.8 to 47.1)
161.4 (132.1 to 195.2)
57.7 (47.8 to 68.5)
62.4 (54.7 to 70.5)
152.0 (145.1 to 159.0)
168.5 (153.3 to 184.9)
Relative change, % (95% CI)
‡The proportion of newborns in each ethnic group who might be currently classified as LGA using the 90th percentile threshold within the Canadian growth curves published by Kramer et al.37 For males and females at 40 weeks gestation the thresholds are 4200 g and 4034 g, respectively.
53 (51 to 56)
27 (22 to 32)
62 (57 to 66)
37 (32 to 41)
38 (35 to 41)
60 (59 to 61)
63 (61 to 65)
Fetuses that would no longer be “incorrectly” identified as LGA (per 1000 fetuses), n (95% CI)
Proposed effect of adopting ethnicity-specific birth weight curves on the rate of LGA
†Based on recently published population-based birth weight percentile curves (Ray et al.35,36). Values represent the median and 90th percentile of birth weight at 40 weeks of gestation.
*Based on the 2011 National Household Survey.39
Overall
Prevalence of that ethnic group in Toronto*
Ethnicity-specific birth weight curve values at 40 weeks, grams†
Table 2. Effect of the use of ethnicity-specific birth weight percentile curves on the rate of LGA diagnoses in the population of Toronto
Commentary
Should We Use Customized Fetal Growth Percentiles in Urban Canada?
To illustrate this, we analyzed the effects of an adjustment for only a single factor—maternal ethnicity—on the rates of SGA and LGA in the diverse population of the city of Toronto as a representative of urban Canada, based on the recently published Ontario ethnicity-specific birth weight curves.35,36 The ethnic distribution of the population of Toronto, 49.1% of which are visible minorities, is presented in Table 1. We initially calculated the proportion of newborns in each ethnic group who might be currently classified as SGA using the 10th percentile threshold within the Canadian growth curves published by Kramer et al.37 (Figure and Table 1). Overall, 15.6% of pregnancies among the visible minority groups are currently classified as SGA, with rates varying by ethnic group (Table 1). Adoption of the ethnicity-specific curves would reduce the overall rate of SGA diagnoses among visible minorities by 36%, with relative reductions of 45% among the newborns of South Asian mothers and 43% among those of Filipina mothers (Table 1). A similar approach was used to analyze the effect of maternal ethnicity on the rate of LGA (Table 2 and Figure). Only 4.7% of newborns of visible minority mothers have birth weights above the national 90th percentile threshold.37 Again, this is most noticeable among South Asian and Filipina women (Table 2), meaning that most cases of LGA in these groups are not currently detected using national metrics of LGA. Adoption of growth curves that are customized for maternal ethnicity, especially in multi-ethnic urban areas like Toronto, may lead to a more accurate diagnosis of SGA and LGA. This may conceivably reduce the unnecessary use of health resources in obstetrical and neonatal care. Customization simply means moving from “clinical judgement” to a more formalized approach for the evaluation of fetal growth in antenatal care, based on a more quantitative, standardized, and objective process. Nevertheless, clinicians should bear in mind three potential limitations of the use of customized curves: first, there are mathematical assumptions that form the basis for this approach, as discussed above. Second, most models developed so far do not account for mixed ethnicity within couples. Third, models developed to date do not adjust for paternal factors. Notwithstanding these limitations, the reality is that important clinical decisions like induction of labour are commonly made on the basis of the sonographic estimation of fetal weight, which itself has a significant margin of imprecision and error.38 Importantly, while we have analyzed the effect of maternal ethnicity alone, adding other customized measures such as
maternal height, weight, and parity may further improve the predictive value. In addition, although we have focused on the possible benefits of the use of customized curves in urban Canada, rural Canada has also seen an increase in the proportion of immigrants and visible minorities, customized curves probably apply there too. The use of customized growth curves needs to be validated in large prospective multicentre studies with sufficient statistical power to detect significant adverse perinatal outcomes. ACKNOWLEDGEMENTS
Dr Kingdom is supported by the Rose Torno Chair at Mount Sinai Hospital. Dr Shah and Dr Ray are supported by Applied Research Chair in Reproductive and Child Health Services and Policy Research from the Canadian Institutes for Health Research. REFERENCES 1. Zhang J, Merialdi M, Platt LD, Kramer MS. Defining normal and abnormal fetal growth: promises and challenges. Am J Obstet Gynecol 2010;202:522–8. 2. Urquia ML, Ray JG. Seven caveats on the use of low birthweight and related indicators in health research. J Epidemiol Community Health 2012;66:971–5. 3. Stratton JF, Scanaill SN, Stuart B, Turner MJ. Are babies of normal birth weight who fail to reach their growth potential as diagnosed by ultrasound at increased risk? Ultrasound Obstet Gynecol 1995;5:114–8. 4. Owen P, Harrold AJ, Farrell T. Fetal size and growth velocity in the prediction of intrapartum caesarean section for fetal distress. Br J Obstet Gynaecol 1997;104:445–9. 5. Barker DJ, Gluckman PD, Godfrey KM, Harding JE, Owens JA, Robinson JS. Fetal nutrition and cardiovascular disease in adult life. Lancet 1993;341:938–41. 6. M Kady S, Gardosi J. Perinatal mortality and fetal growth restriction. Best Pract Res Clin Obstet Gynaecol 2004;18:397–410. 7. Jacobsson B, Ahlin K, Francis A, Hagberg G, Hagberg H, Gardosi J. Cerebral palsy and restricted growth status at birth: population-based case-control study. BJOG 2008;115:1250–5. 8. Lausman A, McCarthy FP, Walker M, Kingdom J. Screening, diagnosis, and management of intrauterine growth restriction. J Obstet Gynaecol Can 2012;34:17–28. 9. Oros D, Figueras F, Cruz-Martinez R, Meler E, Munmany M, Gratacos E. Longitudinal changes in uterine, umbilical and fetal cerebral Doppler indices in late-onset small-for-gestational age fetuses. Ultrasound Obstet Gynecol 2011;37:191–5. 10. Singh T, Leslie K, Bhide A, D’Antonio F, Thilaganathan B. Role of second-trimester uterine artery Doppler in assessing stillbirth risk. Obstet Gynecol 2012;119:256–61. 11. Gardosi J, Chang A, Kalyan B, Sahota D, Symonds EM. Customised antenatal growth charts. Lancet 1992;339:283–7. 12. Gardosi J, Mongelli M, Wilcox M, Chang A. An adjustable fetal weight standard. Ultrasound Obstet Gynecol 1995;6:168–74. 13. Gardosi J. Customized fetal growth standards: rationale and clinical application. Semin Perinatol 2004;28:33–40.
FEBRUARY JOGC FÉVRIER 2014 l 169
Commentary
14. Hadlock FP, Harrist RB, Martinez-Poyer J. In utero analysis of fetal growth: a sonographic weight standard. Radiology 1991;181:129–33. 15. McCowan L, Stewart AW, Francis A, Gardosi J. A customised birthweight centile calculator developed for a New Zealand population. Aust N Z J Obstet Gynaecol 2004;44:428–31. 16. Mongelli M, Figueras F, Francis A, Gardosi J. A customized birthweight centile calculator developed for an Australian population. Aust N Z J Obstet Gynaecol 2007;47:128–31. 17. Figueras F, Meler E, Iraola A, Eixarch E, Coll O, Figueras J, et al. Customized birthweight standards for a Spanish population. Eur J Obstet Gynecol Reprod Biol 2008;136:20–4. 18. Gardosi J, Francis A. A customized standard to assess fetal growth in a US population. Am J Obstet Gynecol 2009;201:25 e1–7. 19. Unterscheider J, Geary MP, Daly S, McAuliffe FM, Kennelly MM, Dornan J, et al. The customized fetal growth potential: a standard for Ireland. Eur J Obstet Gynecol Reprod Biol 2013;166:14–7. 20. de Jong CL, Gardosi J, Dekker GA, Colenbrander GJ, van Geijn HP. Application of a customised birthweight standard in the assessment of perinatal outcome in a high risk population. Br J Obstet Gynaecol 1998;105:531–5.
27. Gardosi J, Kady SM, McGeown P, Francis A, Tonks A. Classification of stillbirth by relevant condition at death (ReCoDe): population based cohort study. BMJ 2005;331:1113–7. 28. Network G. GROW (Gestation Related Optimal Weight): customised antenatal growth chart software; versions 5.x-8.x, 2000–2012. Available at: http://www.gestation.net. Accessed October 22, 2013. 29. Royal College of Obstetricians and Gynaecologists. The investigation and management of the small for gestational age fetus. Green Top Guideline No. 31, RCOG 2002. 30. Mikolajczyk RT, Zhang J, Betran AP, Souza JP, Mori R, Gülmezoglu AM, et al. A global reference for fetal-weight and birthweight percentiles. Lancet 2011;377:1855–61. 31. Hutcheon JA, Zhang X, Cnattingius S, Kramer MS, Platt RW. Customised birthweight percentiles: does adjusting for maternal characteristics matter? BJOG 2008;115:1397–404. 32. Hutcheon JA, Walker M, Platt RW. Assessing the value of customized birth weight percentiles. Am J Epidemiol 2011;173:459–67. 33. Hutcheon JA, Zhang X, Platt RW, Cnattingius S, Kramer MS. The case against customised birthweight standards. Paediatr Perinat Epidemiol 2011;25:11–6.
21. Clausson B, Gardosi J, Francis A, Cnattingius S. Perinatal outcome in SGA births defined by customised versus population-based birthweight standards. BJOG 2001;108:830–4.
34. Kase BA, Carreno CA, Blackwell SC. Customized estimated fetal weight: a novel antenatal tool to diagnose abnormal fetal growth. Am J Obstet Gynecol 2012;207.
22. McCowan LM, Harding JE, Stewart AW. Customized birthweight centiles predict SGA pregnancies with perinatal morbidity. BJOG 2005;112:1026–33.
35. De Souza LR, Urquia ML, Sgro M, Ray JG. One size does not fit all: differences in newborn weight among mothers of Philippine and other East Asian origin. J Obstet Gynaecol Can 2012;34:1026–37.
23. Figueras F, Figueras J, Meler E, Eixarch E, Coll O, Gratacos E, et al. Customised birthweight standards accurately predict perinatal morbidity. Arch Dis Child Fetal Neonatal Ed 2007;92:F277–80.
36. Ray JG, Sgro M, Mamdani MM, Glazier RH, Bocking A, Hilliard R, et al. Birth weight curves tailored to maternal world region. J Obstet Gynaecol Can 2012;34:159–71.
24. Gardosi J, Francis A. Adverse pregnancy outcome and association with small for gestational age birthweight by customized and population-based percentiles. Am J Obstet Gynecol 2009;201:28 e1–8.
37. Kramer MS, Platt RW, Wen SW, Joseph KS, Allen A, Abrahamowicz M, et al. A new and improved population-based Canadian reference for birth weight for gestational age. Pediatrics 2001;108:E35.
25. Charkaluk ML, Marchand-Martin L, Ego A, et al. The influence of fetal growth reference standards on assessment of cognitive and academic outcomes of very preterm children. J Pediatr 2012;161:1053–8.
38. Melamed N, Yogev Y, Meizner I, Mashiach R, Bardin R, Ben-Haroush A. Sonographic fetal weight estimation: which model should be used? J Ultrasound Med 2009;28:617–29.
26. Mattos SS, Chaves ME, Costa SM, Zeitlin J, Arnaud C, Burguet A, et al.; Epipage Study Group. Which growth criteria better predict fetal programming? Arch Dis Child Fetal Neonatal Ed 2013;98:F81–4.
39. Statistics Canada. National Household Survey (NHS) 2001. Available at: http://www12.statcan.gc.ca/nhs-enm/index-eng.cfm. Accessed July 26, 2013. Ottawa (ON): Statistics Canada; 2001.
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