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Received: 21 February 2020    Revised: 17 June 2020    Accepted: 4 September 2020

DOI: 10.1002/ijgo.13370

CLINICAL ARTICLE
Obstetrics

Can pre‐eclampsia explain higher cesarean rates in the


different groups of Robson's classification?

Mariana P. Sanchez | Jose P. Guida* | Marcela Simões | Marcos Marangoni‐Junior | 


Christopher Cralcev | Juliana C. Santos | Tabata Z. Dias | Adriana G. Luz | 
Maria L. Costa

Departament of Obstetrics and


Gynecology, University of Campinas, Abstract
Campinas, São Paulo, Brazil Objective: To evaluate the impact of pre‐eclampsia on cesarean delivery by using the
*Correspondence Robson classification.
José P. Guida, Department of Obstetrics Methods: A retrospective cross‐sectional study including all women who delivered in
and Gynecology, University of Campinas,
Campinas, Brazil. a referral maternity hospital in southeast Brazil from January 2017 to February 2018.
Email: zepauloguida@gmail.com Women were classified into 1 of 10 Robson groups and then further subdivided into
pre‐eclampsia (PE) and non‐PE (NPE) groups. Frequency of cesarean was determined
for each group and compared by using χ2 and prevalence ratio.
Results: Overall, 3102 women were included, of whom 1578 (50.9%) delivered by
cesarean. Classification in Robson group 5 was the most frequent among all women
(n=727, 23.4%). In the PE group (n=258, 8.3%), group 10 was the most frequent classifi‐
cation (n=120, 46.5%); in NPE, Robson group 5 was the most frequency (n=682, 24.0%).
Pre‐eclampsia was associated with a higher occurrence of cesarean (77.5% vs 48.4%;
prevalence ratio, 2.29; 95% confidence interval, 1.82–2.82), owing to higher rates in
Robson groups 1, 5, and 10.
Conclusion: Pre‐eclampsia was associated with a higher occurrence of cesarean deliv‐
ery in some Robson groups. Robson classification may be used to evaluate the impact
of specific conditions at a facility level to help plan future interventions to optimize the
use of cesarean.

KEYWORDS
Audit; Birth; Cesarean rates; Delivery; Pre‐eclampsia; Robson classification

1 |  INTRODUCTION for cesarean deliveries; however, it is associated with higher rates of
this type of delivery.8
Pre‐eclampsia is an important cause of severe maternal morbidity, Cesarean rates may reflect the quality of obstetric care. However,
maternal death, and prematurity worldwide. In middle and low‐income the adequate threshold for cesarean remains controversial. In 1985,
countries, hypertensive disorders in pregnancy are the main cause of the WHO stated that cesarean rates higher than 10%–15% were not
complications during the reproductive cycle.1–4 Pre‐eclampsia is diag‐ justifiable by any medical reason in any world region9; however, that
nosed when there is new onset of hypertension (systolic blood pres‐ statement was not supported by scientific evidence but was based
sure ≥140 mm Hg or diastolic blood pressure ≥90 mm Hg), associated on specialist consensus. Recently, in response to increased rates of
with proteinuria or other laboratory or clinical findings of organ dam‐ cesarean deliveries worldwide and to support future recommenda‐
age, after 20 gestational weeks.5–7 Pre‐eclampsia is not an indication tions, WHO conducted a systematic review10 and further declared

Int. J. Gynecol. Obstet. 2020; 1–6 © 2020 International Federation of |  1


wileyonlinelibrary.com/journal/ijgo  
Gynecology and Obstetrics
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2       Sanchez ET AL.

that cesarean delivery does save maternal and neonatal lives, but rates
higher than 15% do not improve maternal, fetal, or perinatal outcomes BOX 1. Robson classification and characteristics of
in low‐risk populations.11 women included in each group.a
Several systems to understand the magnitude of the increase in
Group Characteristics
rates of cesarean have been suggested. Robson proposed a 10‐group
classification, in which every woman is categorized into 1 of 10 groups. 1 Nulliparous, single cephalic, ≥37 wk, in spontane‐
ous labor
The 10 groups are mutually exclusive and totally inclusive, and use of
the classification is easy and dynamic.12,13 Robson classification facil‐ 2 Nulliparous, single cephalic, ≥37 wk, induced or
cesarean before labor
itates comparisons among different regions and facilities, and even
3 Multiparous (excluding previous cesarean), single
between different timepoints within the same facility. It considers
cephalic, ≥37 wk, in spontaneous labor
parity, number of fetuses, fetal presentation, previous cesarean deliv‐
4 Multiparous (excluding previous cesarean), single
ery, gestational age, and onset of labor; however, it does not consider
cephalic, ≥37 wk, induced or cesarean before
maternal or fetal morbidities, intrapartum complications, or indica‐ labor
tions for cesarean. Furthermore, maternal and perinatal outcomes are 5 Previous cesarean, single cephalic, ≥37 wk
not evaluated by this system.
6 All nulliparous breeches
The WHO formally endorsed Robson classification in 2014 as a
7 All multiparous breeches, including previous
global system for assessing, monitoring, and comparing cesarean rates cesarean
among facilities, countries, and regions.11 To our knowledge, only a
8 All multiple pregnancies, including previous
few studies have applied Robson classification to women with spe‐ cesarean
cific conditions.14,15 The aim of the present study was to understand 9 All abnormal lies, including previous cesarean
the impact of pre‐eclampsia on cesarean delivery rates among women 10 All single cephalic, <37 wk, including previous
categorized by the 10 groups of Robson classification. cesarean
a
Based on Ref.11

2 |  MATERIALS AND METHODS


as laboratory or clinical evidence of organic disorders (e.g., creatinine,
The present retrospective cross‐sectional study assessed data from all ≥1.2  mg/dL; transaminase, ≥70  U/L [or twice the reference]; lactate
women who delivered at the Women’s Hospital at the University of dehydrogenase, ≥600 mg/dL; platelets, ≤100 000/dL; headache, sco‐
Campinas, São Paulo, Brazil, between January 1, 2017, and February tomas, or upper‐right abdominal pain).
28, 2018. The research protocol was approved prior to data collec‐ The study was observational and therefore no formal sample size
tion by the local ethics review board (#19450013900005404) and calculation was conducted. To estimate the minimum numbers of
informed consent was waived owing to the retrospective study design. women expected in each Robson group at a 99% confidence level,
The study maternity hospital, an academic and training unit within we considered a previous study conducted in a Brazilian facility with
the University of Campinas, is a public tertiary hospital in southeast a similar number of deliveries.16 Based on that study, the number of
Brazil that provides care for women with low‐ and high‐risk pregnan‐ women expected in each Robson group was group 1, 457; group 2,
cies, covering a population of 1  000  000 individuals. It has approxi‐ 200; group 3, 374; group 4, 135; group 5, 350; group 6, 46; group 7,
mately 2500 low‐ and high‐risk births annually (half of all deliveries 36; group 8, 41; group 9, 8; group 10, 213.
are considered high risk), providing specialized prenatal and delivery Data were stored in Excel 2013 (Microsoft, Redmond, WA, USA)
care for women with hypertension, cardiac disease, diabetes, and fetal and processed with EpiInfo 7.2 (CDC, Atlanta, GA, USA). Each woman
malformations, among other disorders. was classified into 1 of the 10 Robson groups (Box 1) and women were
Data for the present study was obtained by medical chart review. further divided into pre‐eclampsia (PE) and non‐pre‐eclampsia (NPE)
The following variables were retrieved: maternal age, parity, gesta‐ groups. The number of women and frequency of cesarean section in
tional age, number of fetuses, fetal presentation, onset of labor, blood each Robson’s group was obtained, and the occurrence of pre‐eclamp‐
pressure, diagnosis of pre‐eclampsia, presence of proteinuria, and sia in each group was determined. Cesarean rates in each Robson group
presence of renal, hepatic, hematologic, pulmonary, neurologic, or were compared between the PE and NPE groups by χ2 test, and the
cardiac disorders. prevalence ratio and respective confidence intervals (CIs) were calcu‐
The diagnostic criteria considered in the facility for pre‐eclampsia lated. A P value of less than 0.05 was considered statistically significant.
were hypertension coupled with significant proteinuria or presence
of organic damage. Hypertension was defined as the occurrence of
two or more measures of systolic blood pressure higher or equal to 3 | RESULTS
140 mm Hg or diastolic blood pressure higher or equal to 90 mm Hg.
Significant proteinuria was considered when a 24‐hour protein mea‐ In total, there were 3102 deliveries during the study period that were
surement was higher or equal to 300 mg. Organic damage was defined included in the analysis. Overall, the mean age of the study women
Sanchez ET AL. |
      3

was 28.7 ± 6.8 years and 1130 (36.4%) women were nulliparous. The (95% CI, 1.20–5.50) times more likely to undergo a cesarean delivery
mean gestational age at delivery was 38.7 ± 1.7 weeks and diabetes in Robson group 1, and 2.46 (95% CI, 1.65–3.66) times more likely
was the most frequent comorbidity (n=448, 14.4%). Table 1 summa‐ in group 10. The occurrence of cesarean was also higher in Robson
rizes the sociodemographic, obstetric, and clinical characteristics of group 5 for women with pre‐eclampsia (P=0.026). Group 2 was the
the study women. third most frequent Robson group among women with pre‐eclampsia,
Group 5 (women with previous cesarean, single cephalic fetus, and the rate of cesarean in this group was high (59.3%), importantly
and gestational age ≥37 weeks) was the largest Robson group (n=727, contributing to the overall cesarean rate in the PE group.
23.4%), followed by group 1 (nulliparous, single cephalic, ≥37 weeks,
in spontaneous labor; n=614, 19.8%), group 3 (multiparous, single
cephalic, ≥37  weeks, in spontaneous labor; n=576, 18.6%), group 4 | DISCUSSION
10 (single cephalic, <37  weeks, including previous cesarean; n=452,
14.6%), group 2 (nulliparous, single cephalic, ≥37 weeks, induced or The present study evaluated the distribution of deliveries in a tertiary
cesarean before labor; n=292, 9.4%), and group 4 (multiparous, single maternity hospital over 13 months by Robson classification. It also con‐
cephalic, ≥37 weeks, induced or cesarean before labor; n=230, 7.4%) sidered the occurrence of pre‐eclampsia and the association between
(Table 2). Groups 6–9 collectively contributed a small number of cases pre‐eclampsia and cesarean rates among these women. The results
(n=211, 6.8%). demonstrate that there was an overall high cesarean rate, and pre‐
Of the 3102 study women, 1578 (50.9%) delivered by cesarean. eclampsia was associated with a further increase in cesarean delivery.
Excluding groups 6–9 (which had a small impact on the total number Brazil has one of the highest rates of cesarean delivery worldwide.
of cases and had expected high cesarean rates), group 5 had the high‐ Despite national and local17 efforts to reduce cesarean delivery and
est cesarean rate (72.3%) and group 3 had the lowest cesarean rate improve obstetric care, including the implementation of national pro‐
(25.5%). Group 5 was also the responsible for the majority of cesarean grams centered not only on obtaining good perinatal outcomes, but
deliveries performed (33.3%), followed by group 10 (17.7%) and group also on allowing women to have a positive experience during deliv‐
1 (14.4%) (Table 2). ery,18 the incidence of cesarean delivery is increasing in line with the
Overall, 258 (8.3%) of the 3102 study women had pre‐eclampsia, global trend.19 The present study found a cesarean rate (50.9%) higher
of whom 137 (4.4%) were affected before 37 gestational weeks. In the than that reported by another recent multicenter Brazilian study
NPE group (n=2844), Robson group 5 was the most frequent, followed (39%).14 Many factors are associated with the rise in Brazilian cesarean
by groups 1 and 3; in the PE group, by contrast, Robson group 10 was rates, such as quality of prenatal care, assistance during childbirth, role
the most frequent, followed by groups 5 and 2. Overall, 120 (46.5%) of payment sources, women’s cultural believes, empowerment and
women with pre‐eclampsia were in group 10, as compared with 332 autonomy, and even medicolegal issues.15
(11.7%) women without pre‐eclampsia (Table 3). The present distribution of women in Robson groups was similar
The rate of cesarean in each Robson classification was compared to that observed in a national survey conducted in 2010 that included
between the PE and NPE groups (Table 4). In total, 200 (77.5%) women women with severe maternal morbidity19; however, the present fre‐
delivered by cesarean in the PE groups, as compared with 1378 (48.4%) quency of women in group 10 was higher. In contrast to the “Born in
women in the NPE group (prevalence ratio, 2.29; 95% CI, 1.82–2.88; Brazil” study,19 a multicenter study including both referral and regular
P < 0.001). This difference was mainly due to the higher occurrence of care facilities, the present study included data from only one tertiary
cesarean in groups 1, 5, and 10. Women with pre‐eclampsia were 2.57 center; thus, the higher frequency of preterm deliveries is likely to
be related to the greater complexity of cases admitted for childbirth.
T A B L E 1   Sociodemographic, obstetric, and clinical characteristics When comparing rates of cesarean delivery among Robson groups to
of all study women.a the previous national survey,19 the present rates were lower in groups
Value 2 and 4, similar in group 5, and higher in group 10.
Characteristic (n=3102) Robson groups 1–4 (nulliparous or multiparous women without
Age, y 28.66 ± 6.75 previous cesarean) should have considered obstetric management,

Primigravida 1130 (36.4)


because they are at low risk for cesarean delivery (expected frequency
of 10.0%, 35.0%, 3.0%, and 15.0%, respectively).20 In Brazil,19 how‐
Gestational age, wk 38.66 ± 1.68
b ever, even those groups have high rates of cesarean delivery. Reducing
Diabetes   448 (14.4)
the incidence of cesarean in those groups will be key to long‐term
Chronic hypertension 167 (5.4)
reduction of the overall rate of cesarean delivery in Brazil, because
Mode of delivery
having a previous cesarean is the main risk factor for cesarean deliv‐
Cesarean 1578 (50.9)
ery.21 Avoiding a first cesarean will be more effective than convincing
Vaginal 1526 (49.1) a woman to undergo a trial of labor after cesarean.
Analgesia for vaginal delivery 791 (51.9) Whereas other systems consider indications for performing a
a
Values are given as mean ± SD or number (percentage). cesarean, leading to disarray and unstandardized parameters, Robson
b
Including gestational, type 1, and type 2 diabetes. classification considers inclusive and mutually exclusive individual
|
4       Sanchez ET AL.

T A B L E 2   Distribution of the study women by Robson group and cesarean delivery.

No. (%) of cesareans in Contribution of Robson group


Robson group Total no. (%) of women Robson group to overall cesarean rate, %

1 614 (19.8) 227 (37.0) 14.4


2 292 (9.4) 138 (47.3) 8.7
3 576 (18.6) 147 (25.5) 9.3
4 230 (7.4) 78 (33.9) 4.9
5 727 (23.4) 526 (72.3) 33.3
6 57 (1.8) 49 (86.0) 3.1
7 112 (3.6) 94 (84.0) 6.0
8 31 (1.0) 28 (90.3) 1.8
9 11 (0.3) 11 (100) 0.7
10 452 (14.6) 280 (61.9) 17.7
Total 3102 1578 (50.9) 100.0

characteristics, allowing a unique classification of each woman to a Helping to understand the characteristics of a facility (or even
pre‐specified group. Its intuitive design and ease of implementation a region) and comparing a facility, either with itself over time or
are other strengths of the classification. However, the lack of consen‐ with other facilities, are the main strengths of Robson classification.
sus about some variables is a problem: for instance, defining when Its flexibility, reproducibility, robustness, and simplicity have been
labor starts may vary in different settings and may lead to misclassifi‐ recognized as its main advantages, whereas its lack of explanations
cation among groups 1 to 4. In addition, data collected in routine care about the reasons to perform a cesarean are its main drawbacks.22 A
may be not accurate, even in high‐resource countries, and women may study to evaluate the implementation of Robson classification as an
22
not be adequately classified. intervention to reduce cesarean rates would be relevant and would
Another point of concern regarding Robson classification is the provide evidence about the expected cesarean rate for women
fact that it completely ignores maternal morbidities, a condition that, included in each group.22
as the present results have shown, may interfere with cesarean rates. The prevalence of pre‐eclampsia in Brazil is estimated as 1.2%–
This has also been demonstrated in the C‐model, a proposal that uses 4.2%,24 although this number might be underestimated. The pres‐
Robson classification and adds other relevant information, including ent study found a frequency of pre‐eclampsia of 8.3%, and almost
underlying medical conditions and obstetric complications, to better half of the cases occurred before 37 gestational weeks. This high
predict the rate of cesarean for specific cases.23 number is justified by the referral of the most severe cases in the
region to the study institution. In the study facility, as previously
reported,25 induction of labor is considered for pregnant women
T A B L E 3   Distribution of the study women by Robson group and from a gestational age of 32 weeks onward. This recommendation
occurrence of pre‐eclampsia.a may partially explain the high rates of cesarean in group 10; how‐
ever, the number of cases included in group 10 in the present anal‐
NPE group
Robson group PE group (n=258) (n=2844) ysis is too small to support any conclusion. Continuous surveillance
should focus on preterm deliveries and possibly consider an analysis
1 20 (7.7) 594 (21.0)
of subgroups according to gestational age, with targeted interven‐
2 27 (10.5) 265 (9.3)
tions in late preterm, in order to increase induction of labor and
3 10 (3.9) 566 (19.9)
reduce the rate of cesarean.
4 14 (5.4) 216 (7.6)
Among women with pre‐eclampsia that presents after 34 weeks
5 45 (17.4) 682 (24.0) (late‐preterm pre‐eclampsia), the optimal timing for delivery is unclear,
6 7 (2.7) 50 (1.8) and the risks of maternal disease progression need to be considered
7 14 (5.4) 98 (3.4) against the risks of neonatal complications and prematurity. There is
8 1 (0.4) 30 (1.0) strong evidence to suggest that a planned delivery can reduce mater‐
9 0 (0) 11 (0.4) nal morbidity, although it leads to more neonatal intensive care unit
10 120 (46.5) 332 (11.7) admissions due to prematurity; however, increased cesarean section

Total 258 (100) 2844 (100) rates do not decrease neonatal morbidity rates.26
The present study has several limitations. The retrospective study
Abbreviations: NPE, non‐pre‐eclampsia; PE, pre‐eclampsia.
a
Values are given as number (percentage of total number in PE or NPE
design may hinder the accuracy of information obtained and, as a
group). result, some women may have been misclassified in Robson groups.
Sanchez ET AL. |
      5

T A B L E 4   Frequency of cesarean by Robson group and occurrence of pre‐eclampsia.a

No. (%) of cesareans

Robson group PE group NPE group Unadjusted PR (95% CI) P valuea 

1 15 (75.0) 212 (35.7) <0.001 2.57 (1.20–5.50)


2 16 (59.3) 122 (46.0) 0.189 1.32 (0.82–1.10)
3 5 (50.0) 142 (25.1) 0.073 1.49 (0.80–2.78)
4 7 (50.0) 71 (32.9) 0.189 1.34 (0.80–2.28)
5 39 (86.7) 487 (71.4) 0.026 2.14 (1.00–4.55)
6 5 (71.4) 44 (88.0) 0.237 0.42 (0.10–1.68)
7 14 (100) 80 (81.6) 0.080 NA
8 1 (100) 27 (90.0) 0.073 NA
9 0 (0) 11 (100) NA NA
10 98 (81.7) 182 (54.8) <0.001 2.46 (1.65–3.66)
Total 200 (77.5) 1378 (48.4) <0.001 2.29 (1.82–2.88)

Abbreviations: CI, confidence interval; NA, not applicable; NPE, non‐pre‐eclampsia; PE, pre‐eclampsia group; PR, prevalence ratio.
a
By χ2 test.

Due to the study design, only associations were observed from the AU T HO R CO NT R I B U T I O NS
results, and cause and effect was not evaluated. In addition, the study
MPS contributed to data collection and writing the manuscript. MS,
included a relatively small number of deliveries from a single facility
MM, CC, and JC contributed to data collection and revising the manu‐
over approximately 1  year; except for group 8, however, all groups
script. TZD and AGL contributed to study conception and design, data
reached the minimum frequency expected by sample size calculation.
interpretation, and revising the manuscript. JPG and MLC contributed
Another important point is that the facility where the study was
to study conception and design, statistical analysis, data interpreta‐
conducted is a high‐complexity maternity hospital linked to a univer‐
tion, and writing and reviewing the manuscript.
sity. Women who deliver in the hospital tend to have more severe
forms of hypertension or pre‐eclampsia in comparison to those who
deliver in the community or low‐risk settings. The facility is also a train‐ CO NFL I C TS O F I NT ER ES TS
ing unit, and decisions about timing and mode of delivery are shared
The authors have no conflicts of interest.
by a team of specialists. These characteristics will have influenced the
results and may interfere with the external validity of the findings.
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