Perinatal Outcomes of Fetuses with Early Growth Restriction, Late Growth Restriction, Small for Gestational Age, and Adequate for Gestational Age

Inácio, Quênya Antunes Silveira; Araujo, Edward; Nardozza, Luciano Marcondes Machado; Petrini, Caetano Galvão; Campos, Victor Paranaíba; Peixoto, Alberto Borges

doi:10.1055/s-0039-1697987

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Revista Brasileira de Ginecologia e Obstetrícia

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Original Article • Rev. Bras. Ginecol. Obstet. 41 (12) • Dec 2019 • https://doi.org/10.1055/s-0039-1697987 copy

Perinatal Outcomes of Fetuses with Early Growth Restriction, Late Growth Restriction, Small for Gestational Age, and Adequate for Gestational Age

Resultados perinatais de fetos com restrição de crescimento precoce, restrição de crescimento tardia, pequenos para a idade gestacional e adequados para a idade gestacional

Authorship SCIMAGO INSTITUTIONS RANKINGS

Abstract

Objective

To evaluate the association between early-onset fetal growth restriction (FGR), late-onset FGR, small for gestational age (SGA) and adequate for gestational age (AGA) fetuses and adverse perinatal outcomes.

Methods

This was a retrospective longitudinal study in which 4 groups were evaluated: 1 - early-onset FGR (before 32 weeks) (n=20), 2 - late-onset FGR (at or after 32 weeks) (n=113), 3 - SGA (n=59), 4 - AGA (n=476). The Kaplan-Meier curve was used to compare the time from the diagnosis of FGR to birth. Logistic regression was used to determine the best predictors of adverse perinatal outcomes in fetuses with FGR and SGA.

Results

A longer timebetween the diagnosis and birthwas observed forAGAthan for late FGR fetuses (p<0.001). The model including the type of FGR and the gestational age at birth was significant in predicting the risk of hospitalization in the neonatal intensive care unit (ICU) (p<0.001). The model including only the type of FGR predicted the risk of needing neonatal resuscitation (p<0.001), of respiratory distress (p<0.001), and of birth at<32, 34, and 37 weeks of gestation, respectively (p<0.001).

Conclusion

Fetal growth restriction and SGA were associated with adverse perinatal outcomes. The type of FGR at the moment of diagnosis was an independent variable to predict respiratory distress and the need for neonatal resuscitation. The model including both the type of FGR and the gestational age at birth predicted the risk of needing neonatal ICU hospitalization.

Keywords:
fetal growth restriction; small for gestational age; adverse perinatal outcomes

	AGA (n= 476)			Early onset FGR (n= 20)			Late onset FGR (n= 113)			SGA (n= 59)			p-value
	Median	Min	Max	Median	Min	Max	Median	Min	Max	Median	Min	Max
Age (years)	27	14	42	28.5	19	36	23.5	14	40	25.5	16	43	0.265
Weight (kg)	69	40	135	65.7	52	117	62.1	47	102	66.8	42	103	0.063
Height (cm)	162	145	180	163	154	173	162	148	173	160.5	146	176	0.729
BMI (kg/m²)	26.2	17.3	46.6	24	19.6	46.3	23.8	18.7	38.9	26	17.5	39.5	0.073
GA at diagnosis (wk)	33.4	25.1	40.1	31.1^d,e	28.4	32.4	36.5^f	32	40.7	36.3^a,b	25.1	39	< 0.001^* Kruskal-Wallis. Pairwise comparison: a: SGA versus early FGR; b: SGA versus late FGR; c: SGA versus AGA; d: early FGR versus late FGR; e: early FGR versus AGA; f: late FGR versus AGA. Dunn exact test p< 0.05. The missing data for the variables age, weight, height, BMI, number of pregnancies, parity, birth weight, Apgar 1st minute, Apgar 5th minute for the AGA, early FGR, late FGR, and SGA groups were: 181, 6, 38, and 15 cases, respectively. The missing data for the variables Apgar 1st minute, Apgar 5th minute for the AGA group were 46 cases. There were no missing data for the following variables: GA at diagnosis, GA at delivery, diagnosis at delivery (days).
Number of pregnancies	2	1	8	1,5	1	3	2^f	1	6	2	1	7	0.039^* Kruskal-Wallis. Pairwise comparison: a: SGA versus early FGR; b: SGA versus late FGR; c: SGA versus AGA; d: early FGR versus late FGR; e: early FGR versus AGA; f: late FGR versus AGA. Dunn exact test p< 0.05. The missing data for the variables age, weight, height, BMI, number of pregnancies, parity, birth weight, Apgar 1st minute, Apgar 5th minute for the AGA, early FGR, late FGR, and SGA groups were: 181, 6, 38, and 15 cases, respectively. The missing data for the variables Apgar 1st minute, Apgar 5th minute for the AGA group were 46 cases. There were no missing data for the following variables: GA at diagnosis, GA at delivery, diagnosis at delivery (days).
Parity	1	0	5	0,5	0	2	0^f	0	4	1^b	0	5	0.01^* Kruskal-Wallis. Pairwise comparison: a: SGA versus early FGR; b: SGA versus late FGR; c: SGA versus AGA; d: early FGR versus late FGR; e: early FGR versus AGA; f: late FGR versus AGA. Dunn exact test p< 0.05. The missing data for the variables age, weight, height, BMI, number of pregnancies, parity, birth weight, Apgar 1st minute, Apgar 5th minute for the AGA, early FGR, late FGR, and SGA groups were: 181, 6, 38, and 15 cases, respectively. The missing data for the variables Apgar 1st minute, Apgar 5th minute for the AGA group were 46 cases. There were no missing data for the following variables: GA at diagnosis, GA at delivery, diagnosis at delivery (days).
GA at delivery (wk)	39	32	41	32^d,e	28	39	38^f	32	40	39^a	32	41	< 0.001^* Kruskal-Wallis. Pairwise comparison: a: SGA versus early FGR; b: SGA versus late FGR; c: SGA versus AGA; d: early FGR versus late FGR; e: early FGR versus AGA; f: late FGR versus AGA. Dunn exact test p< 0.05. The missing data for the variables age, weight, height, BMI, number of pregnancies, parity, birth weight, Apgar 1st minute, Apgar 5th minute for the AGA, early FGR, late FGR, and SGA groups were: 181, 6, 38, and 15 cases, respectively. The missing data for the variables Apgar 1st minute, Apgar 5th minute for the AGA group were 46 cases. There were no missing data for the following variables: GA at diagnosis, GA at delivery, diagnosis at delivery (days).
Diagnosis at delivery (days)	32	0	104	4.0^d	0	70	4.0^f	0	52	19.0^b,c	0	104	< 0.001^* Kruskal-Wallis. Pairwise comparison: a: SGA versus early FGR; b: SGA versus late FGR; c: SGA versus AGA; d: early FGR versus late FGR; e: early FGR versus AGA; f: late FGR versus AGA. Dunn exact test p< 0.05. The missing data for the variables age, weight, height, BMI, number of pregnancies, parity, birth weight, Apgar 1st minute, Apgar 5th minute for the AGA, early FGR, late FGR, and SGA groups were: 181, 6, 38, and 15 cases, respectively. The missing data for the variables Apgar 1st minute, Apgar 5th minute for the AGA group were 46 cases. There were no missing data for the following variables: GA at diagnosis, GA at delivery, diagnosis at delivery (days).
Birthweight (g)	3,250	1,760	4,185	1,512.5^d,e	765	2,820	2,465^f	1,380	3495	2807,5^a,b,c	1485	3830	< 0.001^* Kruskal-Wallis. Pairwise comparison: a: SGA versus early FGR; b: SGA versus late FGR; c: SGA versus AGA; d: early FGR versus late FGR; e: early FGR versus AGA; f: late FGR versus AGA. Dunn exact test p< 0.05. The missing data for the variables age, weight, height, BMI, number of pregnancies, parity, birth weight, Apgar 1st minute, Apgar 5th minute for the AGA, early FGR, late FGR, and SGA groups were: 181, 6, 38, and 15 cases, respectively. The missing data for the variables Apgar 1st minute, Apgar 5th minute for the AGA group were 46 cases. There were no missing data for the following variables: GA at diagnosis, GA at delivery, diagnosis at delivery (days).
Apgar 1^st minute	9	4	10	8.5^d,e	6	9	9	6	10	9^c	3	10	< 0.001^* Kruskal-Wallis. Pairwise comparison: a: SGA versus early FGR; b: SGA versus late FGR; c: SGA versus AGA; d: early FGR versus late FGR; e: early FGR versus AGA; f: late FGR versus AGA. Dunn exact test p< 0.05. The missing data for the variables age, weight, height, BMI, number of pregnancies, parity, birth weight, Apgar 1st minute, Apgar 5th minute for the AGA, early FGR, late FGR, and SGA groups were: 181, 6, 38, and 15 cases, respectively. The missing data for the variables Apgar 1st minute, Apgar 5th minute for the AGA group were 46 cases. There were no missing data for the following variables: GA at diagnosis, GA at delivery, diagnosis at delivery (days).
Apgar 5t^h minute	9	7	10	9^d,e	7	10	9	8	10	9^a	7	10	0.004^* Kruskal-Wallis. Pairwise comparison: a: SGA versus early FGR; b: SGA versus late FGR; c: SGA versus AGA; d: early FGR versus late FGR; e: early FGR versus AGA; f: late FGR versus AGA. Dunn exact test p< 0.05. The missing data for the variables age, weight, height, BMI, number of pregnancies, parity, birth weight, Apgar 1st minute, Apgar 5th minute for the AGA, early FGR, late FGR, and SGA groups were: 181, 6, 38, and 15 cases, respectively. The missing data for the variables Apgar 1st minute, Apgar 5th minute for the AGA group were 46 cases. There were no missing data for the following variables: GA at diagnosis, GA at delivery, diagnosis at delivery (days).

	AGA(n= 476)			Early onset FGR(n= 20)			Late onset FGR(n= 113)			SGA(n= 59)			p-value
	Median	Min	Max	Median	Min	Max	Median	Min	Max	Median	Min	Max
HC (mm)	301.1	229.7	351.5	264.1^d,e	224.8	279.4	308.5	271	334.6	307.1^a,b	199	321.5	< 0.001^* Kruskal-Wallis. Pairwise comparison: a: SGA versus early FGR; b: SGA versus late FGR; c: SGA versus AGA; d: early FGR versus late FGR; e: Early FGR versus AGA; f: late FGR versus AGA. Dunn exact test p< 0.05. There was no missing data for all analyzed ultrasound variables.
AC (mm)	290.4	198.9	368.2	229.8^d,e	191	246.5	289.8^f	241.3	321.1	299.3^a,c	192.3	322.6	< 0.001^* Kruskal-Wallis. Pairwise comparison: a: SGA versus early FGR; b: SGA versus late FGR; c: SGA versus AGA; d: early FGR versus late FGR; e: Early FGR versus AGA; f: late FGR versus AGA. Dunn exact test p< 0.05. There was no missing data for all analyzed ultrasound variables.
FDL (mm)	62.1	43.3	76.1	53^d,e	47.7	58.5	65.3	55.7	73.6	63.4^a,d,c	40.3	69.5	< 0.001^* Kruskal-Wallis. Pairwise comparison: a: SGA versus early FGR; b: SGA versus late FGR; c: SGA versus AGA; d: early FGR versus late FGR; e: Early FGR versus AGA; f: late FGR versus AGA. Dunn exact test p< 0.05. There was no missing data for all analyzed ultrasound variables.
HC/AC	1.04	0.9	1.2	1.16^d,e	0.98	1.31	1.1^f	0.97	1.2	1^a,b,	0.93	1.15	< 0.001^* Kruskal-Wallis. Pairwise comparison: a: SGA versus early FGR; b: SGA versus late FGR; c: SGA versus AGA; d: early FGR versus late FGR; e: Early FGR versus AGA; f: late FGR versus AGA. Dunn exact test p< 0.05. There was no missing data for all analyzed ultrasound variables.
EFW (g)	2,107	727	3,722	1,126.5^d,e	732	1,425	2,192.5^f	1,340	2,857	2,281^a,c	585	2,744	< 0.001^* Kruskal-Wallis. Pairwise comparison: a: SGA versus early FGR; b: SGA versus late FGR; c: SGA versus AGA; d: early FGR versus late FGR; e: Early FGR versus AGA; f: late FGR versus AGA. Dunn exact test p< 0.05. There was no missing data for all analyzed ultrasound variables.
LVP (cm)	4.9	2.1	9.8	3.7^e	0	5.4	4.2^f	0	6.9	4.6^a,b	1.8	7.3	< 0.001^* Kruskal-Wallis. Pairwise comparison: a: SGA versus early FGR; b: SGA versus late FGR; c: SGA versus AGA; d: early FGR versus late FGR; e: Early FGR versus AGA; f: late FGR versus AGA. Dunn exact test p< 0.05. There was no missing data for all analyzed ultrasound variables.
UtA PI	0.7	0.42	1.81	1.48^d,e	0.67	2.58	0.75	0.35	1.71	0.66^a	0.49	1.67	< 0.001^* Kruskal-Wallis. Pairwise comparison: a: SGA versus early FGR; b: SGA versus late FGR; c: SGA versus AGA; d: early FGR versus late FGR; e: Early FGR versus AGA; f: late FGR versus AGA. Dunn exact test p< 0.05. There was no missing data for all analyzed ultrasound variables.
UA PI	0.91	0.54	1.47	1.24^d,e	0.82	4.8	0.96	0.57	1.45	0.9^a	0.6	1.21	< 0.001^* Kruskal-Wallis. Pairwise comparison: a: SGA versus early FGR; b: SGA versus late FGR; c: SGA versus AGA; d: early FGR versus late FGR; e: Early FGR versus AGA; f: late FGR versus AGA. Dunn exact test p< 0.05. There was no missing data for all analyzed ultrasound variables.
MCA PI	1.93	0.92	2.8	1.76	1.14	2.36	1.67^f	0.96	2.6	1.73^b	1.04	2.66	< 0.001^* Kruskal-Wallis. Pairwise comparison: a: SGA versus early FGR; b: SGA versus late FGR; c: SGA versus AGA; d: early FGR versus late FGR; e: Early FGR versus AGA; f: late FGR versus AGA. Dunn exact test p< 0.05. There was no missing data for all analyzed ultrasound variables.
Cerebral placental ratio	2.06	1.14	3.92	1.42^e	0.25	2.73	1.74^f	0.88	3.42	1.92^a,b	1.19	3.21	< 0.001^* Kruskal-Wallis. Pairwise comparison: a: SGA versus early FGR; b: SGA versus late FGR; c: SGA versus AGA; d: early FGR versus late FGR; e: Early FGR versus AGA; f: late FGR versus AGA. Dunn exact test p< 0.05. There was no missing data for all analyzed ultrasound variables.

	AGA			Early onset FGR			Late onset FGR			SGA			p-value
	n	n	%	n	n	%	n	n	%	n	n	%	p-value
Delivery < 28 wk
Yes	1	476	0.2	2	20	10.0	0	113	0.0	0	59	0.0	†
No	475	476	99.8	18	20	90.0	113	113	100.0	59	59	100.0
Delivery < 32 wk
Yes	6	476	1.3	12	20	60.0	3	113	2.7	2	59	3.4	< 0.001^* Chi-squared. † It was not possible to perform statistical tests on variables with < 3 patients in any category of answer.
No	470	476	98.7	8	20	40.0	110	113	97.3	57	59	96.6
Delivery < 34 wk
Yes	13	476	2.7	13	20	65.0	8	113	7.1	3	59	5.1	< 0.001^* Chi-squared. † It was not possible to perform statistical tests on variables with < 3 patients in any category of answer.
No	463	476	97.3	7	20	35.0	105	113	92.9	56	59	94.9
Delivery < 37 wk
Yes	39	476	8.2	14	20	70.0	27	113	23.9	12	59	20.3	< 0.001^* Chi-squared. † It was not possible to perform statistical tests on variables with < 3 patients in any category of answer.
No	437	476	91.8	6	20	30.0	86	113	76.1	47	59	79.7
Birthweight
AGA	426	472	90.3	5	20	25.0	44	113	38.9	39	59	66.1	< 0.001^* Chi-squared. † It was not possible to perform statistical tests on variables with < 3 patients in any category of answer.
SGA	29	472	6.1	15	20	75.0	69	113	61.1	20	59	33.9
BGA	17	472	3.6	0	20	0.0	0	113	0.0	0	59	0.0
Apgar < 7 at 5^th minute
Yes	0	430	0.0	0	20	0.0	0	113	0.0	0	59	0.0	†
No	430	430	100.0	20	20	100.0	113	113	100.0	59	59	100.0	†
Neonatal ICU
Yes	20	476	4.2	17	20	85.0	28	113	24.8	6	59	10.2	< 0.001^* Chi-squared. † It was not possible to perform statistical tests on variables with < 3 patients in any category of answer.
No	456	476	95.8	3	20	15.0	85	113	75.2	53	59	89.8
Fetal demise
Yes	0	476	0.0	0	20	0.0	0	113	0.0	0	59	0.0	†
No	476	476	100.0	20	20	100.0	113	113	100.0	59	59	100.0	†
Neonatal demise
Yes	0	476	0.0	1	20	5.0	1	113	0.9	0	59	0.0	†
No	476	476	100.0	19	20	95.0	112	113	99.1	59	59	100.0	†
Neonatal resuscitation
Yes	35	476	7.4	14	20	70.0	22	113	19.5	6	59	10.2	< 0.001^* Chi-squared. † It was not possible to perform statistical tests on variables with < 3 patients in any category of answer.
No	441	476	92.6	6	20	30.0	91	113	80.5	53	59	89.8
Hypoglycemia
Yes	45	393	11.5	14	20	70.0	45	113	39.8	16	59	27.1	< 0.001^* Chi-squared. † It was not possible to perform statistical tests on variables with < 3 patients in any category of answer.
No	348	393	88.5	6	20	30.0	68	113	60.2	43	59	72.9
Hypomagnesaemia
Yes	5	19	26.3	10	20	50.0	9	113	8.0	3	59	5.1	< 0.001^* Chi-squared. † It was not possible to perform statistical tests on variables with < 3 patients in any category of answer.
No	14	19	73.7	10	20	50.0	104	113	92.0	56	59	94.9
Hypothermia
Yes	11	474	2.3	13	20	65.0	20	113	17.7	6	59	10.2	< 0.001^* Chi-squared. † It was not possible to perform statistical tests on variables with < 3 patients in any category of answer.
No	463	474	97.7	7	20	35.0	93	113	82.3	53	59	89.8
Respiratory distress
Yes	45	475	9.5	17	20	85.0	31	113	27.4	12	59	20.3	< 0.001^* Chi-squared. † It was not possible to perform statistical tests on variables with < 3 patients in any category of answer.
No	430	475	90.5	3	20	15.0	82	113	72.6	47	59	79.7

	OR	95%CI	p-value
Delivery < 32 wk
SGA	2.7	0.54–13.9	0.222
Early FGR	117.5	35.2–391.5	< 0.001^* Binary logistic regression.
Late FGR	2.13	0.52–8.7	0.288
Delivery < 34 wk
SGA	1.9	0.52–6.9	0.325
Early FGR	66.1	22.6–193.1	< 0.001^* Binary logistic regression.
Late FGR	2.7	1.09–6.7	0.031^* Binary logistic regression.
Delivery < 37 wk
SGA	2.9	1.4–5.8	0.004^* Binary logistic regression.
Early FGR	26.1	9.5–71.8	< 0.001^* Binary logistic regression.
Late FGR	3.5	2.0–6.0	< 0.001^* Binary logistic regression.
Neonatal ICU
SGA	2.3	0.59–8.69	0.23
Early FGR	77.1	11.27–527.75	< 0.001^* Binary logistic regression.
Late FGR	7.2	2.83–18.01	< 0.001^* Binary logistic regression.
Neonatal resuscitation
SGA	1.4	0.573–3.55	0.445
Early FGR	29.4	10.64–81.2	< 0.001^* Binary logistic regression.
Late FGR	3	1.7–5.4	< 0.001^* Chi-squared. † It was not possible to perform statistical tests on variables with < 3 patients in any category of answer.
Respiratory distress
SGA	2.4	1.20–4.93	0.013 *
Early FGR	54.14	15.30–191.90	< 0.001^* Binary logistic regression.
Late FGR	3.6	2.15–6.04	< 0.001^* Binary logistic regression.

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[1] Address for correspondence Edward Araujo Júnior, PhD, Rua Botucatu, 720, 04023-062, Vila Clementino, São Paulo, SP, Brazil (e-mail: araujojred@terra.com.br).