Because previous research has shown that children are at risk of both stunting and waisting, might be born with both, pass from one state to the other over time, and accumulate risks to their health and life through, the combined rate were calculated.

The study was carried out by using publicly accessible anonymized data, by means of encrypted individual health card numbers ⁽¹¹⁾.

The study included 25948 singleton live births. Mean maternal age was 25.7 years (SD 6.3), and near 50% had > 12 years of schooling. Mean BMI was 24.3 k/m², 14.6% were smokers, 7.0% hypertensive, and 3.1% diabetic. The distribution by newborn gender was similar. Mean birth weight was 3306 g (520) and prematurity 11.5% (Table 1).

Table N° 1: Maternal and infant characteristics, composite severe neonatal morbidity/mortality (CNMM) and neonatal phenotypes (N= 25948)

Overall between 1996 and 2001, the birth weight-for-gestational age <3^rd centile was 3.7% of infants under the Urquia criteria, compared with 2.3% under the IG-21^st criteria (p<0.001). Similarly, a substantially lower proportion of live births were <10^th centile of birth weight-for-gestational age under the IG-21^st criteria compared with the Urquia criteria (p<0.001). In contrast, a minimal difference was observed in the proportion of live births >97^th centile under the IG-21^st criteria compared with the Urquia criteria (P= 0.080) (Table 1). The Urquia 3^rd centile value was lower than IG-21^st 3^rd centile before 37 weeks, but then it surpassed IG-21^st until term (Figure 1). Stunting and waisting were 16.6% and 0.9%, respectively under IG-21^st, whereas both combined rate was 0.26%.

figura1a

^{Figure N°1. Third percentile birthweight for Urquia reference and IG-21}

^{Standard by gestational age and sex}

Morbidity and mortality

Table 2 shows rates of neonatal death and severe neonatal morbidity among live births within specific phenotypes categories. The rate of neonatal death among SGA<3^rdcentile was significantly higher under the IG-21^stcriteria compared with the Argentinean reference (9.4 vs 6.4 per 100 live births, p = 0.029). The rate of neonatal death was also higher among SGA <10^th centile under the IG-21^stcriteria compared with the Urquia criteria (p = 0.006). However, rates of neonatal death among live births >97^th centile of the IG-21^st and Urquia criteria were similar (p = 0.08). Neonatal death was three times higher for stunting than for waisting; for combined group rate of neonatal death was 1.79%.

Patterns of all morbidities included in CNMM were also higher among SGA<3^rd and SGA <10^th centile under the IG-21^st standard compared with the Urquia reference, but similar rates was found among >97^th centile for both criteria. Consequently, rates of composite neonatal morbidity/mortality were significantly higher in all centile categories under INTERGROWTH criteria except for the large-for-gestational category (p=0.003 for SGA<3^rd centile, p=0.002 for SGA<10^th centile and p=0.553 for >97^th centile). CNMM was extremely more common for stunting than for waisting under IG-21^st criteria. For combined group rate was 1.51% (Table 2).

Table N° 2: Neonatal mortality and morbidity rates (per 100 live births) among phenotypes categories of the INTERGROWTH-21^st Project standard and Urquia reference.

Phenotypes	All lives Births (n = 25948)		<3rd centile		<10th centile		>97th centile		Stunting		Wasting
Standard or reference	No.	Rate	No.	Rate	No.	Rate	No.	Rate	No.	Rate	No.	Rate
INTERGROWTH 21st standard
Neonatal death	217	0.84	56	9.4	79	5.1	16	0.7	205	4.7	3	1.4
Apgar 5’<7	324	1.2	67	11.2	105	6.8	58	2.5	295	6.8	7	3.3
Resp.support>4 hs	1413	5.4	99	16.7	145	9.5	145	6.3	451	10.4	30	14.5
Seizures	130	0.5	10	1.6	20	1.3	18	0.7	50	1.1	2	0.9
CNMM	1878	7.2	169	28.5	300	19.6	197	8.5	746	17.3	38	0.18
URQUIA reference
Neonatal death	217	0.84	62	6.4	89	3.4	15	0.6	a		a
Apgar 5’<7	324	1.2	78	8.1	127	4.8	54	2.4	a		a
Resp.support>4 hs	1413	5.4	121	12.5	244	9.3	135	6.1	a		a
Seizures	130	0.5	13	1.3	24	0.9	18	0.8	a		a
CNMM	1878	7.2	210	21.8	370	14.2	185	8.0	a		a
^{a: not applicable because the Urquia reference does not include newborn length}
^{CNMM: composite severe neonatal morbidity/mortality; Rate: %}

Analysis by gestational age

Rates among the different phenotypes were compared among live births at 33-36 weeks and 37-42 weeks gestation. For SGA <3^rd centile prevalence under the Urquia references at 33 to less than 37 weeks’ gestation were significantly higher compared with term infants (27.5% vs 3.7% respectively [p<0.001], whereas under the IG-21^st standard a less reduction was observed (16.1% vs 2.1%, respectively [p <0.001]). At <10^rd centile a significant decrease was observed with Urquia reference at 33-36 weeks compared with >37 weeks (7.4% vs 10.8%, respectively [p <0.001]), while for IG-21^st standard figures were 7.0% vs 5.7%, respectively (p=0.002). For >97^th centile, both Urquia and IG-21^st significant reduction were similar at 33-36 weeks compared with >37 weeks (24.2% vs 6.3% [p <0.001]). Finally, under IG-21^st standard the stunting rate was significant higher at 33-36 weeks than > 37 weeks (20.4% vs 16.1%, [p<0.001]), whereas no difference was observed for wasting (0.90% vs 0.78%, [p<0.510]).

Risks of Composite neonatal morbidity/mortality rates

Table 3 highlights a decreasing risk in severe neonatal morbidity/mortality within phenotypes under the Urquia and INTERGROWTH criteria. Among all live births, infants <3^rd centile had higher adjusted rate ratios of CNMM under IG-21^st than the Urquia criteria (3.57 [95 % CI 2.90 – 4.40] vs 2.90 [2.40 – 3.49], respectively. For <10^th centile RRs where 2.67 (2.27 – 3.14) and 1.99 (1.72 – 2.30) for IG21 and Urquia criteria, respectively. In contrast, there was no difference in the risks of CNMM among live births >97^th centile under both criteria (1.27 [1.05 – 1.52] for IG-21^st and 1.26 [1.05 – 1.52] for Urquia). Stunting and waisting showed near three times higher adjusted RRs of CNMM under IG-21^st criteria compared with reference.

Table N° 3: Crude and adjusted RRs for composite adverse neonatal outcome among phenotypes categories of the Urquia reference and INTERGROWTH-21^st Project standard

Phenotypes	Urquia reference		IG-21^st standard
	Crude RR	Adjusted RR ^a	Crude RR	Adjusted RR ^a
	(95% CI)	(95% CI)	(95% CI)	(95% CI)
<3rd centile	1.18	2.90	1.44	3.57
<3rd centile	(1.04-1.33)	(2.40- 3.49)	(1.28- 1.60)	(2.90- 4.40)
<10^thcentile	0.78	1.99	1.11	2.67
<10^thcentile	(0.67- 0.90)	(1.72- 2.30)	(0.99-1.23)	(2.27- 3.14)
>97^thcentile	0.17	1.26	0.18	1.27
>97^thcentile	(0.27- 0.32)	(1.05- 1.52)	(0.04- 0.33)	(1.05-1.52)
Stunting	^b	^b	1.19	2.91
Stunting	^b	^b	(1.10-1.29)	(2.59-3.28)
Wasting	^b	^b	1.23	3.37
Wasting	^b	^b	(0.91- 1.55)	(2.32- 4.89)
^{RR: relative risk; CI: confidence interval}
^{a: adjusted for maternal age, parity, BMI, gestational age, hypertension, diabetes}
^{and infant sex. Non-phenotypes group as the reference.}
^{b: not applicable because the Urquia reference does not include newborn length}

Detection rates

Sensitivity rates by phenotype category showed that 9.02% and 16.0% of all cases of composite neonatal morbidity/mortality occurred among live births <3^rd centile and <10^th centile, respectively, under the IG-21^st criteria, while 11.2% and 19.7% of CNMM occurred among live births <3rd centile and <10th centile under the Urquia criteria. For live birth >97^th centile, sensitivity was slightly higher under IG-21^st criteria compared with Urquia criteria (10.5% vs 9.9%, respectively). Under IG-21^st criteria sensitivity was thirteen times higher for stunting than for waisting (39.8% vs 2.9%, respectively). Youden Index was extremely low for all phenotypes, except for stunting (Table 4).

Table N° 4: Sensitivity, specificity, and predictive values for composite adverse neonatal outcome among phenotypes categories of the INTERGROWTH-21^st Project standard and Urquia reference.

INTERGROWTH-21 standard	Sen	Spe	PPV	NPV	Youden Index
<3rd centile	9.02	98.2	28.5	93.2	0.09
<10^thcentile	16.0	94.9	19.6	93.5	0.13
>97^thcentile	10.5	91.2	8.5	92.9	0.03
Stunting	39.8	85.2	17.3	94.7	0.27
Wasting	2.9	99.2	18.3	94.6	0.03
URQUIAreference
<3rd centile	11.2	96.8	21.8	93.3	0.10
<10^thcentile	19.7	90.7	14.1	93.5	0.12
>97^thcentile	9.9	91.6	8.5	92.9	0.03
^{Sen: sensitivity; Spe: specificity; PPV: positive predictive value; NPV: negative predictive value} ^{Youden Index = Specificity + sensitivity – 1 ⁽¹²⁾}

When detection rates of CNMM by phenotypes were compared by gestational age categories, SGA <3^rd centile sensitivity rate under Urquia reference showed no difference between 33-36 weeks and 37-42 weeks gestation (11.6% vs 11.0%, respectively). In contrast, under IG-21^st standard, the rates showed a marked decrease between 33-36 weeks and 37-42 weeks (11.6% vs 7.7%, respectively).

At <10^rd centile, sensitivity at 33-36 weeks were similar for both criteria but higher than <3^rd centile (19.5% vs 19.0%), whereas at 37-42 weeks sensitivity rate under IG-21^st decreased compared with Urquia reference (14.4% vs 19.8%, respectively). For >97^th centile both criteria presented markedly decrease but similar rates at 33-36 weeks and 37-42 weeks (9.7% and 10.0% for Urquia criteria, and 10.3% and 10.6% for IG-21^st criteria, respectively). Stunting showed the highest detection rates of CNMM under the IG-21^st criteria at both 33-36 weeks and 37-42 weeks (42.6% and 38.4%, respectively). Finally, waisting exhibited the lowest rates in both GA categories under the IG-21^st standard (3.3% at 33-36 weeks, and 2.6% at 37-42 weeks).

Discussion

We present a comparison of phenotypes prevalence and associated neonatal morbidity and mortality risk between a new standard on optimal fetal growth and existing local birthweight reference.

Applying the new INTERGROWTH-21^st birth weight standard, we observed a roughly 40% reduction in the prevalence of SGA <10th centile among the cohorts (Urquia 10.1% vs IG-21^st 5.8%). The SGA-less-than-10 percentile cutoff using the reference may have been too inclusive in identifying neonates at risk due to fetal growth restriction. On the other hand, the relative reduction in prevalence when applying the IG-21^st standard vanished among infants born at 33 to less than 37 weeks’ gestation (Urquia 7.4% vs IG-21^st 7.0%) and was greater in Urquia term infants (10.4% vs IG-21^st 5.7%); this may be attributed that, at preterm gestations, the IG-21^st standard may not reflect optimal fetal growth because preterm birth is inherently pathological and is commonly associated with fetal growth restriction ⁽¹³⁾. In addition, differences in SGA rates between criteria can be related to differences in maternal size. Increasing maternal height and weight are correlated with increasing infant birthweight, even for women of normal BMI ⁽¹⁴⁾.

When applying a more strict criteria (<3^rd centile) the reduction among the cohorts slightly decreased (37%), but difference in prevalence was larger among infants born at 33 to less than 37 weeks’ gestation (Urquia 27.5% vs IG-21^st 16.1%) and was similar in term infants (3.7% vs IG-21^st 2.1%) (Fig.1). This may be attributable to the prescriptive design of the IG-21^st Project, the left shift in birth weight-for-gestational age centiles of the Urquia reference (skewness -0.701 [SE 0.015], K-S test = 0.162 [p<0.001]), and that mothers contributing births to the lower tail of the distribution may be more similar in risk profile between the IG-21^st standard and the Urquia references; for example, they may comprise women who are genetically predisposed to having smaller children ⁽¹⁵⁾. It is also unclear as to the extent to which miscategorization of gestational age due to the use of last menstrual period in the Urquia reference may have affected these findings.

Both the international IG-21^st standard and Urquia reference has revealed a markedly high prevalence of LGA>97^th centile infants than expected, but no difference was observed between them (Urquía 8.4% vs IG-21^st 8.9%). In a previous population study of singleton live births, 0.87% and 9.63% were <3^rd centile and >97^th centile, respectively, under the IG-21^st standard, while 2.27% and 3.55% were <3^rd centile and >97^th centile, respectively, of a Canadian reference ⁽²⁾. Revollo et al. assessed the prevalence of SGA <3^rd centile, stunting and wasting by gestational age in newborns of the Jujuy Province, Argentina at different altitude levels. Prevalence were 1.27%, 3.39% and 4.68% for of SGA<3^rd centile, stunting and wasting, respectively, and significantly higher at >2.000 m.a.s.l. ⁽¹⁶⁾. Finally, in an Australian study, >97^th centile prevalence was 6.2% under IG-21^{st (17)}.

Observed differences in between-country and ethnic-specific fetal growth references potentially reflect differences in maternal socioeconomic status and health ⁽¹⁸⁾. We highlight that the divergence between the IG-21^st standard and the different studies may occur because several risk factors, such as overweight and obesity and gestational diabetes, that are linked to higher birth weight and preterm birth are more prevalent in the studies but excluded from the IG-21^st study ⁽³⁾.

The international standards still need to be tailored to local populations and statistic-based cutoffs (such as < 10^th or > 90^th centile), should ideally be replaced by perinatal risk-based cutoffs to provide an evidence-based triage for neonatal care ⁽³⁾.

Differences were observed in neonatal morbidity and mortality rates within phenotypes of the IG-21^st and Urquia criteria. The relatively less stringent INTERGROWTH criteria for identifying large-for-gestational age infants resulted in relatively low neonatal morbidity/mortality rates among such infants.

This overall picture suggests that, under IG-21^st criteria, Sardá live births have low rates of growth restriction and high rates of excess growth, but higher morbidity/mortality rates in SGA infants, compared with the Urquia reference. The rate of a composite adverse neonatal outcome in a New Zeland study was 17.2% in infants identified as SGA <10^th centile by IG-21^st and 12.1% in those identified as SGA by customized criteria ⁽¹⁷⁾. Differences were attributed to customized birthweight standards that differ from population standards in that they use ultrasound-based measures of fetal size. In a study from India, the infants identified as SGA <10^th centile at birth by IG-21^stcharts had higher incidence of morbidities compared with Fenton growth charts ⁽¹⁹⁾. Under the IG-21^st standard infants <3^rd centile and >97^thcentile had a higher composite neonatal morbidity/mortality rate than a Canadian reference ⁽²⁾. Finally, the neonatal mortality risk of SGA status (< 10th percentile) did not differ significantly between IG-21^stand a commonly used US references ⁽¹⁵⁾. These findings are similar to our study, although the composite of adverse neonatal outcome were different.

Consistently, adjusted CNMM risks in SGA (<3^rd and <10^th) and >97^th centiles where higher under IG-21^st compared with Urquia reference. Elevated adjusted CNMM risks for stunting and waisting is worrisome, because the first accounted after a prolonged intrauterine growth restriction not amenable to rapid nutritional treatment, and is therefore considered to require prevention rather than treatment, whereas the late is an acute and reversible process with adequate nutritional intervention ⁽⁹⁾. In addition, the combined rate (0.26 %) was small than children between 6 months and 59 months in 84 countries (3%, range 0% to 8%) ⁽²⁰⁾, but mortality rate (1.79%) was higher than the most severe form of being wasted (1.4%), underpinning that they accumulate risks to their health and life course (such as promoting human capital and reducing the risk of non-communicable disease) through their combined effects.

In a sensitivity analysis, we find a larger relative reduction in neonatal mortality rate associated to SGA among infants born at term compared to 33 to less than 37 weeks’ gestation (roughly 84% for Urquia vs 87% for IG-21^st).

Despite the fact that children small or large for gestational age have an increased risk of adverse neonatal outcomes irrespective of the reference used for classification, most adverse outcomes occur in infants without this disorder. Consequently, the sensitivity, positive predictive values and Youden Index of these phenotypes for adverse perinatal outcomes were very low⁽²¹⁾.

This study supports the case for an outcome-based determination of IG-21^stcentile cut-offs for surveillance and monitoring of abnormal growth ⁽⁴⁾. The identification of optimal cut-offs for identifying infants at high risk for adverse outcomes needs to balance the proportion of severe neonatal morbidity and neonatal death identified by the cut-off (sensitivity) with the proportion of infants deemed to be high risk (stratification capacity)⁽¹⁰⁾. The optimal IG-21^st centile cut-offs for identifying small- and large-for-gestational age live births will likely be resource/cost dependent and hence spatio-temporally specific.

Growth centiles (or phenotypes) are perhaps best viewed as one input for use in multivariable models for the screening and identification of high risk infants. Obstetric intervention for abnormal fetal growth is ideally guided by multivariable models that include fetal growth centiles and other risk factors such as uterine and middle cerebral artery blood flow ⁽²²⁾.

Limitations include potential errors with regard to gestational age, which would have affected phenotypes under both criteria. In addition, some transcription errors are also possible with regard to the diagnoses of severe neonatal morbidity.

Another limitation was that only a limited range of neonatal morbidity measures could be reported, but these are objective measures that have been shown to identify infants at high risk of major morbidity ^(3,23-24). Strengths of our study were sample size, the inclusion of objective morbidity measures that are infrequently included in other cohort studies, and combined evaluation of stunting and waisting.

Future work will standardize outcome measures because several core outcome sets have also been developed or are in development in the field of neonatology ^(25-26). Lastly, our facility-specific estimates might not be representative for the country, but portray the population included in this study. The Urquia reference will remain useful in understanding the growth status of a newborn in relation to the population attended.

Conslusion

The IG-21 standard identified low rates of growth restriction and high rates of excess growth, but a higher risk of neonatal morbidity and mortality than the Urquia reference.

Limitaciones de responsabilidad

La responsabilidad del trabajo es sólo de los autores.

Exclusividad de publicación:

El estudio no ha sido publicado previamente, ni se ha presentado a otra revista.

Declaración de la originalidad del trabajo que se presenta.

Se trata de un artículo original.

Fuentes de apoyo:

Ninguna.

Conflicto de interés:

Los autores declaran que no existen conflictos de intereses con otros autores, instituciones, laboratorios, profesionales u otros.

Cesión de derechos:

Los autores ceden los derechos de autor a la Universidad Nacional de Córdoba para publicar en la RFCM y para realizar la traducción en inglés.

Bibliografía

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Recibido: 2020-03-30 Aceptado: 2020-04-06

DOI: http://dx.doi.org/10.31053/1853.0605.v77.n2.28064

Maternal Characteristic	Mean (SD) or %
Age, years	25.7	6.3
BMI (kg/m2)	24.3	4.6
Education
High school	11499	46.6
University	771	3.1
Marital or cohabiting	19873	76.5
Nulliparous	10356	39.9
Previous miscarriage	7171	27.6
Previous preterm birth	279	1.1
Smoking in pregnancy	4566	14.6
Hypertension	1823	7.03
Diabetes	816	3.1
Bleeding during pregnancy	365	1.4
Urinary infection	1283	4.9
Infant
Male	12992	50.1
Gestational age, wks	38.8	1.9
Preterm birth	2998	11.5
Birthweight, g	3306	520
Length, cm	48.1	2.5
Head circumference, cm	34.8	1.9
BMI (kg/m2)	14.3	1.8
Composite severe neonatal morbidity/mortality (CNMM)
Neonatal death	217	0.84
Birth asphyxia (Apgar 5’<7)	324	1.2
Respiratory support >4 hs	1413	5.4
Seizures	130	0.5
CNMM	1878	7.2
Phenotypes
Urquia
< 3rd centile	961	3.7
< 10th centile	2609	10.1
> 97th centile	2188	8.4
INTERGROWTH-21st
< 3rd centile	593	2.3
< 10th centile	1527	5.9
> 97th centile	2300	8.9
Stunting	4307	16.6
Wasting	207	0.9
^{BMI: body mass index}