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Mode of delivery according to Robson classification and perinatal outcomes in restricted and small for gestational age fetuses

Abstract

Objective

To evaluate the mode of delivery according to Robson classification (RC) and the perinatal outcomes in fetal growth restriction (FGR) and small for gestational age (SGA) fetuses.

Methods

Retrospective cohort study by analyzing medical records of singleton pregnancies from two consecutive years (2018 and 2019). FGR was defined according to Delphi Consensus. The Robson groups were divided into two intervals (1–5.1 and 5.2–10).

Results

Total of 852 cases were included: FGR (n = 85), SGA (n = 20) and control (n=747). FGR showed higher percentages of newborns < 1,500 grams (p<0.001) and higher overall cesarean section (CS) rates (p<0.001). FGR had the highest rates of neonatal resuscitation and neonatal intensive care unit admission (p<0.001). SGA and control presented higher percentage of patients classified in 1 - 5.1 RC groups, while FGR had higher percentage in 5.2 - 10 RC groups (p<0.001). FGR, SGA and control did not differ in the mode of delivery in the 1-5.1 RC groups as all groups showed a higher percentage of vaginal deliveries (p=0.476).

Conclusion

Fetuses with FGR had higher CS rates and worse perinatal outcomes than SGA and control fetuses. Most FGR fetuses were delivered by cesarean section and were allocated in 5.2 to 10 RC groups, while most SGA and control fetuses were allocated in 1 to 5.1 RC groups. Vaginal delivery occurred in nearly 60% of FGR allocated in 1-5.1 RC groups without a significant increase in perinatal morbidity. Therefore, the vaginal route should be considered in FGR fetuses.

Fetal growth retardation; Cesarean section; Pregnancy outcome; Infant, small for gestational age; Gestational age; Infant, newborn; Fetus; Robson classification

Introduction

Fetal growth restriction (FGR) is a common obstetric complication, affecting 5%–10% of singleton pregnancies and is associated with adverse perinatal outcomes such as fetal and neonatal death, prematurity and need for neonatal respiratory support.(11. Temming LA, Dicke JM, Stout MJ, Rampersad RM, Macones GA, Tuuli MG, et al. Early second-trimester fetal growth restriction and adverse perinatal outcomes. Obstet Gynecol. 2017;130(4):865-9.)The most appropriate way to define FGR would be the fetus that has not reached its intrauterine growth potential due to some degree of placental insufficiency.(22. Nardozza LM, Caetano AC, Zamarian AC, Mazzola JB, Silva CP, Marçal VM, et al. Fetal growth restriction: current knowledge. Arch Gynecol Obstet. 2017;295(5):1061-7. doi: 10.1007/s00404-017-4341-9)However, there is no consensus regarding on objective diagnostic criteria,(33. Frøen JF, Gardosi JO, Thurmann A, Francis A, Stray-Pedersen B. Restricted fetal growth in sudden intrauterine unexplained death. Acta Obstet Gynecol Scand. 2004;83(9):801-7. doi: 10.1111/j.0001-6349.2004.00602.x) considering that some fetuses are constitutionally smaller due to the influence of genetics and ethnicity.(44. Damhuis SE, Ganzevoort W, Gordijn SJ. Abnormal fetal growth: small for gestational age, fetal growth restriction, large for gestational age: definitions and epidemiology. Obstet Gynecol Clin North Am. 2021;48(2):267-79. doi: 10.1016/j.ogc.2021.02.002
https://doi.org/10.1016/j.ogc.2021.02.00...
)These fetuses are referred to as small for gestational age (SGA) and exhibits similar morbidity and mortality rates to appropriate for gestational age (AGA) fetuses.

Robson classification (RC), published in 2001,(55. Robson MS. Classification of caesarean sections. Fetal Matern Med Rev. 2001;12(1):23-39. doi: 10.1017/S0965539501000122
https://doi.org/10.1017/S096553950100012...
)allows allocation of parturients in ten groups based on six parameters [parity, gestational age (GA) at delivery, previous cesarean section, number of fetuses, fetal presentation, and labor onset]. It is simple, objective, uses well-established obstetric criteria and is completely inclusive and mutually exclusive, so that each patient can only be allocated in one of the groups. This fact, in addition to enabling further reliable comparisons, facilitates the identification of the characteristics of pregnant women that progress to cesarean deliveries, and detects modifiable factors in order to reduce cesarean rates. Chart 1 describes the characteristics of parturients included in each group. Since 2015, the World Health Organization (WHO) has been recommended RC to monitor cesarean section rates in maternity hospitals.(66. Betran AP, Torloni MR, Zhang JJ, Gülmezoglu AM. WHO statement on caesarean section rates. BJOG. 2016;123(5):667-70. doi: 10.1111/1471-0528.13526)

Chart 1
Robson classification

The objective of this study was to evaluate the mode of birth delivery, according to Robson classification, and the perinatal outcomes in FGR and SGA, comparing them with other fetus deliveries of the maternity hospital with estimated weight above the tenth percentile.

Methods

A retrospective cohort study was conducted by analyzing medical records at São Paulo Hospital of the Federal University of São Paulo - Paulista School of São Paulo (UNIFESP - EPM), from January 2018 to December 2019. Given the design and objectives of the study, it was important to include all eligible patients to avoid sampling bias. If it was the possibility of contact with the participants who remained at our service, a consent form was written and available. For participants who could not be contacted, a declaration of confidentiality and data anonymization was signed, in accordance with local recommendations.

The exclusion criteria were: multiple gestation, fetal malformation, or fetal infection suspected on ultrasound or identified in the postnatal period. This study classified FGR according to the definition published in 2016, using the Delphi procedure that consisted to the following: Early FGR (< 32 weeks) - three solitary parameters are described: abdominal circumference (AC) < 3rd centile, estimated fetal weight (EFW) < 3rd centile or absent end-diastolic flow in the umbilical artery (UA) Doppler. Contributory parameters are: AC or EFW < 10th centile combined with a pulsatility index (PI) > 95th centile in either the UA or in the uterine artery Doppler. Late FGR (≥ 32 weeks) - two solitary parameters (AC or EFW < 3rd centile) and the presence of at least two contributory parameters (EFW or AC < 10th centile, AC or EFW crossing centiles > two quartiles on growth charts, cerebroplacental ratio <5th centile or UA-PI > 95th centile) were defined.(77. Gordijn SJ, Beune IM, Thilaganathan B, Papageorghiou A, Baschat AA, Baker PN, et al. Consensus definition of fetal growth restriction: a Delphi procedure. Ultrasound Obstet Gynecol. 2016;48(3):333-9. doi: 10.1002/uog.15884)

The patients were classified into three groups: (I) FGR – EFW < 10th percentile by the Hadlock et al.(88. Hadlock FP, Harrist RB, Carpenter RJ, Deter RL, Park SK. Sonographic estimation of fetal weight. The value of femur length in addition to head and abdomen measurements. Radiology. 1984;150(2):535-40. doi: 10.1148/radiology.150.2.6691115
https://doi.org/10.1148/radiology.150.2....
)table and met FGR criteria, according to Delphi Consensus;(77. Gordijn SJ, Beune IM, Thilaganathan B, Papageorghiou A, Baschat AA, Baker PN, et al. Consensus definition of fetal growth restriction: a Delphi procedure. Ultrasound Obstet Gynecol. 2016;48(3):333-9. doi: 10.1002/uog.15884)(II) SGA – EFW < 10th percentile by the Hadlock et al.(88. Hadlock FP, Harrist RB, Carpenter RJ, Deter RL, Park SK. Sonographic estimation of fetal weight. The value of femur length in addition to head and abdomen measurements. Radiology. 1984;150(2):535-40. doi: 10.1148/radiology.150.2.6691115
https://doi.org/10.1148/radiology.150.2....
)table without the FGR criteria, according to Delphi Consensus;(77. Gordijn SJ, Beune IM, Thilaganathan B, Papageorghiou A, Baschat AA, Baker PN, et al. Consensus definition of fetal growth restriction: a Delphi procedure. Ultrasound Obstet Gynecol. 2016;48(3):333-9. doi: 10.1002/uog.15884)(III) Control – other deliveries of the maternity hospital with EFW > 10th percentile, according to the Hadlock et al.(88. Hadlock FP, Harrist RB, Carpenter RJ, Deter RL, Park SK. Sonographic estimation of fetal weight. The value of femur length in addition to head and abdomen measurements. Radiology. 1984;150(2):535-40. doi: 10.1148/radiology.150.2.6691115
https://doi.org/10.1148/radiology.150.2....
)table.

For the definition of FGR or SGA, the last ultrasound scan report performed in the service was evaluated. In the reports, the Doppler parameters of the umbilical and middle cerebral arteries were evaluated according to the Arduini and Rizzo(99. Arduini D, Rizzo G. Normal values of pulsatility index from fetal vessels: a cross-sectional study on 1556 healthy fetuses. J Perinat Med. 1990;18(3):165-72. doi: 10.1515/jpme.1990.18.3.165) curve and the uterine arteries Doppler were evaluated according to the Gómez et al.(1010. Gómez O, Figueras F, Fernández S, Bennasar M, Martínez JM, Puerto B, et al. Reference ranges for uterine artery mean pulsatility index at 11-41 weeks of gestation. Ultrasound Obstet Gynecol. 2008;32(2):128-32. doi: 10.1002/uog.5315) curve.

Management of FGR is summarized in chart 2 according to the local protocol at the time of delivery.(1111. Caetano AC, Nardozza LM. Obstetric management. In: Nardozza LM, Araújo Júnior E, Rizzo G, Deter RL, editors. Fetal growth restriction: current evidence and clinical practice. Berlin: Springer; 2019. p. 187-91.)The adverse perinatal outcomes evaluated were: birth weight, 5-min Apgar score, umbilical cord pH, need for neonatal resuscitation, neonatal intensive care unit (NICU) admission, fetal death, and in-hospital death.

Chart 2
Local management of fetal growth restriction

To perform the comparison of the three groups regarding the mode of delivery by RC, each group was aggregated into two intervals, as shown below: (I) Robson Group 1 – 5.1 = all singleton pregnancies of a fetus in cephalic presentation regardless of parity and onset of labor (spontaneous, induced, or absent), admitted with GA ≥ 37 weeks and having up to one previous cesarean section; (II) Robson Group 5.2–10 = all singleton pregnancies ≥ 37 weeks with two or more previous cesarean sections, cephalic preterms, and all non-cephalic presentations regardless of GA. It should be noted that Group 8 (multiple gestation) was not included in our evaluation. The choice of intervals was based on the fact that the Robson Group (1 -5.1) corresponded to patients with a higher probability of vaginal delivery, both due to the intrinsic characteristics of the pregnant women in this group and to our follow-up management protocol.

We classified the indications for cesarean section into three groups. (I) Fetal indication – indication by any means of objective evaluation of fetal vitality such as Doppler abnormalities on ultrasound or fetal heart rate on intermittent auscultation or on cardiotocography. (II) Obstetric indication – any antepartum or intrapartum indication for conditions predominantly related to the gestational period or intrapartum such as arrested cervical dilation, arrested progression of fetal presentation and prior uterine scars. (III) Maternal indication – any maternal medical conditions induced by pregnancy or previously present comorbidity that worsens during pregnancy or contraindicates the vaginal delivery.

Data were tabulated in Excel 2010 spreadsheet (Microsoft Corp., Redmond, WA, USA) and analyzed using IBM SPSS Statistics for Windows software (version 22.0, IBM Corp, Armonk, NY, USA). The information on quantitative variables was summarized using mean, standard deviation (SD), median, interquartile range (IQR), and minimum and maximum values. The information from the qualitative variables was summarized using simple frequency and percentage.

To compare the groups in relation to quantitative variables, which did not show normal distribution, the Kruskal–Wallis non-parametric test was used, followed by the Mann–Whitney non-parametric test with Bonferroni correction. To compare the groups with regard to the qualitative variables, the Chi-Square test or, when necessary, the Likelihood ratio test was used. In all analyses, p-value <0.05 was considered significant.

This study was approved by the Research Ethics Committee of UNIFESP (CAAE: 29823419.0.0000.5505) (CEP: 4.053.519).

Results

During the study period, 1063 pregnant women were admitted, 123 being fetuses with EFW < 10th percentile and 940 with EFW > 10th percentile (control group). Of the 123 fetuses with EFW < 10th percentile, 18 were excluded: 3 congenital heart diseases, 1 ambiguous genitalia, 10 genetic alterations (3 trisomy 21, 1 monosomy X, and 6 undefined genetic syndromes), 1 bilateral congenital cataract, 1 cytomegalovirus, and 2 skeletal dysplasias. Of the 105 fetuses included, 85 were classified as FGR and 20 as SGA. Of the 940 cases in the control group, 193 fetuses were excluded: 45 multiple pregnancies, 120 fetal malformations, 19 fetal infections, 6 out-of-service deliveries, and 3 cases with incomplete data in the medical records.

Table 1 presents the sociodemographic maternal characteristics and adverse perinatal outcomes in the three groups evaluated. The mean maternal age ± SD in the control, SGA, and FGR groups were 30.4 ± 7.1, 27.9 ± 6.4, and 28.3 ± 7.5 years, respectively, being significantly lower in the FGR group compared to the control group (p=0.012).

Table 1
Sociodemographic maternal characteristics and adverse perinatal outcomes according to the three groups evaluated

We observed higher cesarean section rates in FGR compared to SGA and control group (p < 0.001). The percentage of GA at birth ≥ 37 weeks was significantly higher in the SGA and control than in the FGR group (p < 0.001). In addition, the median GA at delivery was significantly lower in FGR than in SGA and control groups (p < 0.001), which did not differ from each other with respect to this variable. The control group had a higher percentage of newborn (NB) weight ≥ 2500 grams, half of the SGA had NB group had weight ≥ 2500 grams, and the other half had NB weight in the 1500–2499 grams range. FGR was the only group that showed a higher percentage of NBs with weights < 1500 grams, when compared to the other groups (p < 0.001). The median 5-min Apgar score was significantly higher in the control group than in the other groups (p < 0.001), which did not differ from one another. However, when we categorized the Apgar score into the clinically significant value (< 7 and ≥ 7) we found no difference between the groups (p=0.184). The percentage of neonatal resuscitation was significantly higher in the FGR group than the control group (p < 0.001). The percentage of NICU admission was significantly higher in FGR group than in the other groups (p < 0.001).

Table 2 presents the variables of Robson classification according to the three groups evaluated. The percentage of nulliparous women was significantly lower in the control group than in the others (p < 0.001), which did not differ from each other with respect to parity. The percentage of previous cesarean section was significantly lower in FGR than in SGA and control (p < 0.001), which did not differ from one another with respect to this variable. The percentage of breech presentation was significantly higher in the FGR group than in the other groups (p < 0.001), which did not differ from one another with respect to this variable. The percentage of absent labor was significantly higher in the FGR (p< 0.001). The percentage of spontaneous labor was significantly higher in the control group, while the percentage of induced labor was significantly higher in the SGA group (p < 0.001).

Table 2
Robson classification variables according to the three groups evaluated

Regarding cesarean section indications, fetal and obstetric indications were respectively higher and lower in the FGR group (p < 0.001). Maternal indication for cesarean section was significantly higher (p < 0.001) in the SGA group (Table 3).

Table 3
Comparison between the three groups regarding indications for cesarean section

There was a significant difference between the mode of delivery in relation to Robson groups. The percentage of vaginal deliveries was significantly higher in the interval of Robson groups 1 to 5.1, than in the interval 5.2 to 10 (p < 0.001). In the SGA and control groups there was a higher percentage of pregnant women in the range 1–5.1, while in the FGR group there was a higher percentage in the interval 5.2–10 (p < 0.001). Table 4 presents the comparison between the three groups regarding the mode of delivery for each of Robson’s group intervals. For Robson interval 1–5.1, no significant difference was observed between the groups regarding the mode of delivery; as all groups have a higher percentage of vaginal deliveries (p = 0.476). For Robson groups 5.2–10, a higher percentage of cesarean sections was observed in all groups, but the percentage of pregnant women in the control group who progressed to vaginal delivery in this interval of RC was higher than in the other groups (p=0.009). The distribution of births according to the 10 Robson groups report is available in chart 3.

Table 4
Comparison between the three groups regarding the type of delivery for each of Robson’s group intervals
Chart 3
Distribution of births according to the 10 Robson groups report

Discussion

Our study found a higher percentage of fetuses classified as FGR than SGA, unlike what is described in literature.(1212. Unterscheider J, Daly S, Geary MP, Kennelly MM, McAuliffe FM, O'Donoghue K, et al. Optimizing the definition of intrauterine growth restriction. Am J Obstet Gynecol. 2013;208(4):290.e1-6. doi: 10.1016/j.ajog.2013.02.007)This higher proportion can be explained by the complexity of the cases followed up and referred to our service, which is a tertiary center that treats pregnant women with several comorbidities. Such comorbidities have the potential to generate severe and early placental insufficiency, with a greater likelihood of FGR.

Placental implantation abnormalities are very common in the first pregnancy,(1313. Robinson JS, Moore VM, Owens JA, McMillen IC. Origins of fetal growth restriction. Eur J Obstet Gynecol Reprod Biol. 2000;92(1):13-9. doi: 10.1016/s0301-2115(00)00421-8)which is consistent with our findings of lower median age in the FGR group and a higher percentage of nulliparous women in pregnancies with estimated fetal weight < 10th percentile. Cesarean section was statistically more frequent in the FGR group, as expected, since these fetuses have a higher risk of Doppler abnormalities and a higher risk of intrapartum fetal vitality compromise. A retrospective study of 100 cases of labor induction in fetuses with late FGR showed 63% vaginal deliveries, 32% cesarean sections, and 5% operative vaginal deliveries. Doppler abnormalities of the AU, middle cerebral artery and cerebroplacental ratio were observed to be associated with increased risk of cesarean section.(1414. Simeone S, Marchi L, Canarutto R, Pina Rambaldi M, Serena C, Servienti C, et al. Doppler velocimetry and adverse outcome in labor induction for late IUGR. J Matern Neonatal Med. 2017;30(3):323-8. doi: 10.3109/14767058.2016.1171839)As expected, GA at delivery was low in the FGR group. Deliveries ≥ 37 weeks occurred in 49.4% in the FGR, 95% in the SGA, and 80.5% in the control groups. A Spanish study published in 2022 involving 655 AGA (appropriate for gestational age), 62 SGA, 132 early FGR, and 57 late FGR fetuses (classified by Delphi Consensus) found similar GA at delivery in AGA (39: interquartile range - IQR 39–40) and SGA (39: IQR 38–40) fetuses and statistically lower in fetuses classified as early FGR (32: IQR 29–38) when compared to the other groups. A difference was observed in the GA of fetuses with late FGR (38: IQR 36–49) when compared to AGA and SGA.(1515. Lubrano C, Taricco E, Coco C, Di Domenico F, Mandò C, Cetin I. Perinatal and neonatal outcomes in fetal growth restriction and small for gestational age. J Clin Med. 2022;11(10):2729. doi: 10.3390/jcm11102729)

The need for neonatal resuscitation and NICU admission were significantly higher in the FGR group. In a retrospective longitudinal study, pregnant women carrying fetuses with early FGR, late FGR, SGA, and AGA were included for correlation with adverse neonatal outcomes. Logistic regression model including FGR type and GA at delivery was considered in predicting risk of NICU admission. Model including only the type of FGR (early or late) better predicted risk of need for neonatal resuscitation, respiratory distress, and birth at GA < 32, 34, and 37 weeks, respectively.(1616. Inácio QA, Araujo Júnior E, Nardozza LM, Petrini CG, Campos VP, Peixoto AB. Perinatal outcomes of fetuses with early growth restriction, late growth restriction, small for gestational age, and adequate for gestational age. Rev Bras Ginecol Obstet. 2019;41(12):688-96. doi: 10.1055/s-0039-1697987
https://doi.org/10.1055/s-0039-1697987...
)

In the evaluation of all the deliveries included in the study, most of the pregnant women who progressed to vaginal delivery were classified in Robson groups 1 to 5.1. When we compared the distribution of the pregnant women in the two intervals of Robson groups, there was a higher percentage in the FGR group in the interval 5.2–10. This probably occurred because of a higher incidence of preterm births with cephalic presentation and a higher incidence of breech presentation associated with prematurity in fetuses with a high probability of true growth restriction and a high probability of being born prematurely.

Regarding the type of delivery, there was no statistical difference between the groups in Robson intervals 1–5.1, with vaginal delivery being the most common, which is in line with Robson classification that aims to screen pregnant women with a high probability of vaginal delivery. In the second interval (Robson 5.2–10), cesarean section was more common in all groups.

Analyzing only the FGR group it was intuitive to find a high overall percentage of cesarean deliveries due to the potential severity of the cases. However, when we selected the most eligible patients for vaginal delivery in the FGR group (Robson 1–5.1), the percentage of vaginal delivery was 59.5% and no increase in stillbirth was observed when compared to the other groups.

To date, there are no studies specifically evaluating the contribution of pregnant women with EFW < 10th percentile on cesarean section rates based on Robson classification. This evaluation is important because the evidences show that vaginal delivery, in selected FGR fetuses and with adequate monitoring, may be possible and safe for the mother–fetus binomial.

In 2016, a study of cesarean section rates in Brazil was published by Nakamura-Pereira et al.,(1717. Nakamura-Pereira M, Leal MC, Esteves-Pereira AP, Domingues RM, Torres JA, Dias MA, et al. Use of Robson classification to assess cesarean section rate in Brazil: the role of source of payment for childbirth. Reprod Health. 2016;13 Suppl 3:128. doi: 10.1186/s12978-016-0228-7)using data from 2011 to 2012 from the public and private facilities. The sample included 23,940 women, who were classified into one of Robson’s ten groups. The total cesarean section rate was 51.9% (42.9% in the public sector and 87.9% in the private sector), with 70% performed in pregnant women of the Groups 2, 5, and 10. High-risk pregnant women had significantly higher rates of cesarean sections than low-risk pregnant women in almost all groups in the public sector. Group 2 was the largest in this study, corresponding to 20% of the entire population, and 70% of the pregnant women in this group underwent antepartum cesarean section and 30% had induced labor.

Similar data was found in our study regarding the overall cesarean section rate (48.9%) and the groups that contributed the most were Groups 2 (19.7%), 5 (32.4%) and 10 (22.5%) totaling 74.6% of the total cesarean sections. However, in our study, the largest group was Group 10, corresponding to 18.3% of the entire population, probably secondary to the characteristics of the maternity hospital, which is a tertiary referral center for high-risk cases.

This study had some limitations, some of which are inherent related to retrospective studies, such as the use of pre-existing data not systematically collected for this specific purpose. The results reflect more outcomes in the FGR group than in the SGA group, due to the relatively small number of participants in the SGA group (n=20) and therefore the comparison of the SGA group with the others may not be accurate. Our control group did not represent the usual low-risk obstetric population, as most of our patients already have some high-risk condition.

Selection bias was mitigated by the fact that all data collection and tabulation was carried out by a single researcher, who used all means available in the electronic medical record platform to locate the medical records of the pregnant women and their newborns. The medical records of all patients in the RCF and SGA groups were found. In the control group, only three records of the 940 eligible patients could not be found, therefore, resulting in less than 0.5% of loss of information for this reason.

Conclusion

Fetuses with FGR had higher cesarean section rates and worse perinatal outcomes than SGA and AGA fetuses. However, when we evaluated mortality data (fetal death and in-hospital death) no statistical difference was observed in our study population, which can be attributed to a good prenatal care follow-up of these cases. Fetuses with FGR had higher cesarean section rates in groups 5.2–10. On the other hand, when patients eligible for vaginal delivery in the FGR group (Robson 1–5.1) were selected, there were approximately 60% vaginal deliveries with satisfactory perinatal outcomes. This data is important to motivate the professionals about the safety in trying and conducting labor in this context in eligible patients.

References

  • 1
    Temming LA, Dicke JM, Stout MJ, Rampersad RM, Macones GA, Tuuli MG, et al. Early second-trimester fetal growth restriction and adverse perinatal outcomes. Obstet Gynecol. 2017;130(4):865-9.
  • 2
    Nardozza LM, Caetano AC, Zamarian AC, Mazzola JB, Silva CP, Marçal VM, et al. Fetal growth restriction: current knowledge. Arch Gynecol Obstet. 2017;295(5):1061-7. doi: 10.1007/s00404-017-4341-9
  • 3
    Frøen JF, Gardosi JO, Thurmann A, Francis A, Stray-Pedersen B. Restricted fetal growth in sudden intrauterine unexplained death. Acta Obstet Gynecol Scand. 2004;83(9):801-7. doi: 10.1111/j.0001-6349.2004.00602.x
  • 4
    Damhuis SE, Ganzevoort W, Gordijn SJ. Abnormal fetal growth: small for gestational age, fetal growth restriction, large for gestational age: definitions and epidemiology. Obstet Gynecol Clin North Am. 2021;48(2):267-79. doi: 10.1016/j.ogc.2021.02.002
    » https://doi.org/10.1016/j.ogc.2021.02.002
  • 5
    Robson MS. Classification of caesarean sections. Fetal Matern Med Rev. 2001;12(1):23-39. doi: 10.1017/S0965539501000122
    » https://doi.org/10.1017/S0965539501000122
  • 6
    Betran AP, Torloni MR, Zhang JJ, Gülmezoglu AM. WHO statement on caesarean section rates. BJOG. 2016;123(5):667-70. doi: 10.1111/1471-0528.13526
  • 7
    Gordijn SJ, Beune IM, Thilaganathan B, Papageorghiou A, Baschat AA, Baker PN, et al. Consensus definition of fetal growth restriction: a Delphi procedure. Ultrasound Obstet Gynecol. 2016;48(3):333-9. doi: 10.1002/uog.15884
  • 8
    Hadlock FP, Harrist RB, Carpenter RJ, Deter RL, Park SK. Sonographic estimation of fetal weight. The value of femur length in addition to head and abdomen measurements. Radiology. 1984;150(2):535-40. doi: 10.1148/radiology.150.2.6691115
    » https://doi.org/10.1148/radiology.150.2.6691115
  • 9
    Arduini D, Rizzo G. Normal values of pulsatility index from fetal vessels: a cross-sectional study on 1556 healthy fetuses. J Perinat Med. 1990;18(3):165-72. doi: 10.1515/jpme.1990.18.3.165
  • 10
    Gómez O, Figueras F, Fernández S, Bennasar M, Martínez JM, Puerto B, et al. Reference ranges for uterine artery mean pulsatility index at 11-41 weeks of gestation. Ultrasound Obstet Gynecol. 2008;32(2):128-32. doi: 10.1002/uog.5315
  • 11
    Caetano AC, Nardozza LM. Obstetric management. In: Nardozza LM, Araújo Júnior E, Rizzo G, Deter RL, editors. Fetal growth restriction: current evidence and clinical practice. Berlin: Springer; 2019. p. 187-91.
  • 12
    Unterscheider J, Daly S, Geary MP, Kennelly MM, McAuliffe FM, O'Donoghue K, et al. Optimizing the definition of intrauterine growth restriction. Am J Obstet Gynecol. 2013;208(4):290.e1-6. doi: 10.1016/j.ajog.2013.02.007
  • 13
    Robinson JS, Moore VM, Owens JA, McMillen IC. Origins of fetal growth restriction. Eur J Obstet Gynecol Reprod Biol. 2000;92(1):13-9. doi: 10.1016/s0301-2115(00)00421-8
  • 14
    Simeone S, Marchi L, Canarutto R, Pina Rambaldi M, Serena C, Servienti C, et al. Doppler velocimetry and adverse outcome in labor induction for late IUGR. J Matern Neonatal Med. 2017;30(3):323-8. doi: 10.3109/14767058.2016.1171839
  • 15
    Lubrano C, Taricco E, Coco C, Di Domenico F, Mandò C, Cetin I. Perinatal and neonatal outcomes in fetal growth restriction and small for gestational age. J Clin Med. 2022;11(10):2729. doi: 10.3390/jcm11102729
  • 16
    Inácio QA, Araujo Júnior E, Nardozza LM, Petrini CG, Campos VP, Peixoto AB. Perinatal outcomes of fetuses with early growth restriction, late growth restriction, small for gestational age, and adequate for gestational age. Rev Bras Ginecol Obstet. 2019;41(12):688-96. doi: 10.1055/s-0039-1697987
    » https://doi.org/10.1055/s-0039-1697987
  • 17
    Nakamura-Pereira M, Leal MC, Esteves-Pereira AP, Domingues RM, Torres JA, Dias MA, et al. Use of Robson classification to assess cesarean section rate in Brazil: the role of source of payment for childbirth. Reprod Health. 2016;13 Suppl 3:128. doi: 10.1186/s12978-016-0228-7

Edited by

Associate Editor: Conrado Milani Coutinho(https://orcid.org/0000-0003-1966-0466) Universidade de São Paulo, Ribeirão Preto, SP, Brazil

Publication Dates

  • Publication in this collection
    12 Aug 2024
  • Date of issue
    2024

History

  • Received
    24 Jan 2023
  • Accepted
    6 Nov 2023
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