DOI: 10.1111/1471-0528.
12236
www.bjog.org
Caesarean section and risk for endometriosis: a
prospective cohort study of Swedish registries
lle
E Andolf,a M Thorsell,a K Ka  nb
a
Division of Obstetrics and Gynaecology, Department of Clinical Sciences, Karolinska Institutet, Danderyd Hospital, Stockholm, Sweden
b
Centre of Reproduction Epidemiology, Institution of Clinical Sciences, University of Lund, Lund, Sweden
Correspondence: Dr E Andolf, Division of Obstetrics and Gynaecology, Department of Clinical Sciences, Karolinska Institutet, Danderyd
Hospital, SE182 88 Stockholm, Sweden. Email ellika.andolf@ds.se
Accepted 1 March 2013. Published Online 13 May 2013.
Objective To investigate the association between caesarean
section and later endometriosis.
Design A prospective cohort study.
Setting The Swedish Patient Register (PAR) and the
Swedish Medical Birth Registry (MBR).
Sample Women who were delivered in Sweden between
1986 and 2004.
Methods Women with the diagnosis of endometriosis, defined as
codes 617 (International Classification of Diseases, ninth revision,
ICD9) or N80 (ICD10), were retrieved from the PAR. Obstetric
outcome was assessed through linkage with the MBR. Out of
709 090 women, 3110 were treated as inpatients with a first
diagnosis of endometriosis after their first delivery. Women with a
diagnosis of endometriosis before their first delivery were
excluded. Cox analyses were performed to obtain hazard ratios for
endometriosis and adjusted for maternal age at first delivery, body
mass index, maternal smoking, and years of involuntary
Please cite this paper as: Andolf E, Thorsell M, Kallen K. Caesarean section and risk for endometriosis: a prospective cohort study of Swedish registries.
BJOG 2013;120:10611065.
Introduction
The increasing rate of caesarean sections has raised con-
cerns about both the short- and the long-term maternal
consequences of the procedure.16 The literature on endo-
metriosis as a sequel of caesarean section has focused on
the risk for scar endometrioma,79 which has also been
described in women who delivered vaginally after an episi-
otomy.10 Scar endometriomas usually present as a lump in
the incision, sometimes mistaken for an incisional hernia,
and occasionally with cyclic pain, making surgery neces-
sary.7 However, it is possible that the development of pelvic
endometriosis after caesarean section is overlooked because
symptoms of chronic pelvic pain, dysmenorrheal, and
dyspareunia are less specific. Endometriotic lesions have
been found following laparoscopic subtotal hysterectomy,11
2013 The Authors BJOG An International Journal of Obstetrics and Gynaecology 2013 RCOG
Epidemiology
childlessness at study entry. KaplanMeier estimates were
performed to calculate the risk according to time elapsed.
Main outcome In-hospital diagnosis of endometriosis.
Results The Cox analyses yielded a hazard ratio of 1.8
(95% CI 1.71.9) for endometriosis in women who had had a
previous caesarean section compared with women with vaginal
deliveries only. The risk of endometriosis increased over time:
one additional case of endometriosis was found for every 325
women undergoing caesarean section within 10 years. No
increase in risk could be seen after two caesarean deliveries.
The risk of caesarean scar endometrioma was 0.1%.
Conclusion In addition to the recognised risk of
scar endometrioma, we found an association between caesarean
section and general pelvic endometriosis. Further studies are
needed to confirm our findings.
Keywords Caesarean section, casecontrol study, endometriosis,
epidemiology.
but the risk of endometriosis developing within the pelvis
after caesarean section has not been extensively explored.
Endometriosis is associated with substantial morbidity,
being associated with a reduction in health-related quality
of life,12 an increased risk for ovarian cancer,13 and possibly
even malignant transformation within scar endometri-
oma.14
A previous caesarean section is known to be associated
with an increased risk of chronic pelvic pain.15 Whether
this is related to endometriosis is unknown. The patho-
physiology behind endometriosis is uncertain, but one the-
ory is that degenerating endometrial components undergo
metaplastic transformation when introduced into the
abdominal cavity,16 and this may theoretically happen
when the uterine cavity is opened in the course of
abdominal delivery. Therefore, the objective of this study
1061
 Andolf et al.
was to investigate the association, if any, between in-hospi-
tal diagnosis of endometriosis and caesarean section.
Methods
In a prospective cohort study the Swedish Patient Register
(PAR), kept by the National Board of Health and Welfare,
Stockholm, was used to identify women with a diagnosis of
endometriosis (International Classification of Diseases,
ninth revision, ICD9, 617; ICD10, N80). For scar endome-
triosis the diagnosis of 617G (ICD9) and N80.6 (ICD10)
was used. Using the personal identification number
assigned to each resident in Sweden, the data were linked
to the Swedish Medical Birth Registry (MBR), which is also
kept by the National Board of Health.
The PAR contains information on diagnoses (19871996,
ICD9; 1997 and onwards, ICD10) and operation codes of
all inpatients admitted to any Swedish hospital. The MBR
is also kept by the National Board of Health and Welfare,
and contains medical information on nearly all deliveries in
Sweden (with a coverage of about 99%). Standardised
record forms are used at all antenatal clinics, all delivery
units, and at all paediatric examinations of newborn infants
in the maternity ward. Information on maternal smoking
and body mass index (BMI, kg/m2) are prospectively
recorded by the midwife at the first visit to the antenatal
centre. Copies of the standardised record forms are sent to
the National Board of Health and Welfare, where they are
computerised.17
Women were included if they gave birth to their first
child between 1986 and 2004, a period that was covered by
the PAR register. Cases were excluded if they had a reported
diagnosis of endometriosis before their first delivery, and for
women who had been diagnosed more than once, only the
first diagnosis was counted. The time for entry to the study
was set to the date of the first delivery. The time for the
study exit was set at the date of the first diagnosis of endo-
metriosis, the date of the 55th birthday, or on 31 Decem-
ber 2004 (when the data set was retrieved), depending on
which event happened first. In the descriptive tables, women
with vaginal births before their first caesarean section were
displayed only once, and are presented in the caesarean sec-
tion group only. However, in the analyses, women with vag-
inal births before their first caesarean section contributed
with person-months to the vaginal births group before the
first caesarean section. The main hypothesis was that a cae-
sarean section may increase the risk for endometriosis sev-
eral years after the operation. Thus, after a womans first
caesarean section, all her person-months were designated to
the caesarean section group, irrespectively of whether the
caesarean section was followed by vaginal deliveries or not.
Cox analyses were performed in order to obtain hazard
ratios (HRs) for endometriosis after the first caesarean
1062 2013 The Authors BJOG An International Journal of Obstetrics and Gynaecology 2013 RCOG
section versus the first vaginal labour. The time at risk for
each woman and time to diagnosis, respectively, was
defined as explained above. Adjustments were made for
maternal age at first delivery (continuous variable, qua-
dratic model), BMI (linear, continuous), maternal smoking
(yes/no), and years of involuntary childlessness (linear,
continuous) at study entry (the first delivery). Kaplan
Meier estimates were computed to produce a graph
illustrating the percentage of women who had ever been
diagnosed with endometriosis by the time elapsed from the
first delivery, and delivery mode. The COX- and the
KaplanMeier analyses were performed using GAUSS.18 A
comparison between the descriptive characteristics of
women with caesarean section and women with vaginal
births only was evaluated using chi-square analyses:
P < 0.05 was considered to be significant.
Results
Table 1 shows the descriptive characteristics at first delivery,
of women who had at least one caesarean section or vaginal
deliveries only, respectively, during the study period.
Women who had any caesarean section were older, were
more often overweight, smoked more, and had longer peri-
ods of involuntary childlessness, than had women with vagi-
nal births only. Therefore, all these factors were considered
to be possible confounders in the analyses of a possible asso-
ciation between caesarean section and endometriosis.
Table 2 displays the percentage of women with a diagnosis
of endometriosis reported to the PAR register in 19872005
by mode of delivery and length of follow-up. From Table 2
it is evident that the estimated endometriosis rate is heavily
dependent on the length of follow-up. The crude rates indi-
cate that the incidence of endometriosis was higher among
women who underwent at least one caesarean section than
among women who had vaginal deliveries only.
Cox analyses were performed in order to adequately con-
sider the different lengths of follow-up. These analyses
yielded an almost doubled risk for endometriosis in women
who had had at least one caesarean section (HR 1.8,
95% CI 1.661.94), compared with women who had vaginal
deliveries only (Table 3). The estimate was only marginally
altered when adjustments for maternal age, BMI, smoking,
or years of involuntary childlessness were made. The results
from the Cox analysis, in combination with the absolute
risk for endometriosis in the current population, concluded
that the numbers needed to harm within 10 years were 325,
that is one additional case of endometriosis was found for
every 325 women undergoing caesarean section within
10 years. We did not detect any increased risk of endometri-
osis in women with two caesarean sections, compared with
women with one caesarean section (HR 0.77, 95% CI
0.491.22). The risk for scar endometriosis in all women
 Caesarean section and risk for endometriosis

Table 1. Demographic characteristics of women in Sweden who Table 2. Incidence of endometriosis by mode of delivery and length
gave birth between 1986 and 2004, by study group of follow-up

Study group P* At least one caesarean Vaginal births only

section
At least one Vaginal births
caesarean section only Endometriosis Total Endometriosis Total
n (%) n (%) n (%) n n (%) n

Maternal age Total n 749 (0.6) 130 305 2361 (0.4) 578 785
<20 years 4832 (3.7) 29 155 (5.0) <0.001 Follow-up 715 (0.8) 86 831 2288 (0.5) 438 449
2024 years 30 525 (23.4) 171 536 (29.6) of at least
2529 years 47 483 (36.4) 227 057 (39.2) 5 years
3034 years 32 399 (24.9) 115 656 (20.0) Follow-up 608 (1.1) 54 388 2042 (0.7) 310 908
3539 years 12 205 (9.4) 30 458 (5.3) of at least
40+ years 2861 (2.2) 4923 (0.9) 10 years
Maternal BMI (kg/m2)** Follow-up 311 (1.5) 21 096 1211 (0.9) 136 468
<20 11 236 (12.3) 65 765 (16.0) <0.001 of at least
2024 50 357 (55.1) 248 377 (60.6) 15 years
2529 20 960 (22.9) 73 637 (18.0)
30+ 8829 (9.7) 22 026 (5.4)
Not known 38 923 168 980
Maternal smoking**
respectively. The curve showing the proportion of women
No smoking 97 557 (80.6) 441 702 (81.3) <0.001
<10 cigaretes/day 15 757 (13.0) 68 908 (12.7)
who had ever had a diagnosis of endometriosis among
 10 cigaretes/day 7782 (6.4) 32 673 (6.0) women who underwent caesarean section had a consider-
Not known 9209 35 502 ably steeper slope than the corresponding slope for women
Involuntary childlessness who had vaginal deliveries only.
No 11 5854 (88.9) 533 439 (92.2) <0.001
12 years 6739 (5.2) 25 606 (4.4)
34 years 3852 (3.0) 10 754 (1.9) Discussion
5+ years 3855 (3.0) 8957 (1.5)
Parity***
Main findings
1 44 089 (33.8) 186 442 (32.2) <0.001 In this large population-based prospective cohort study, we
2 61 467 (47.2) 286 991 (49.6) have found an association between in-hospital diagnosis of
3 19 318 (14.8) 87 393 (15.1) any endometriosis and at least one previous caesarean sec-
4+ 5431 (4.2) 17 959 (3.1) tion. The risk was related to time of follow-up. No
Minimum follow-up time**** increased risk could be shown after two caesarean sections.
At least 5 years 86 831 (66.6) 438 449 (75.8) <0.001
The risk for abdominal endometriosis was higher than for
At least 10 years 54 388 (41.7) 310 908 (53.7)
At least 15 years 21 096 (16.2) 136 468 (23.6)
scar endometrioma, which is not previously known (any
endometriosis 0.6%, scar endometriosis 0.1%).
*P value (chi-square test) for differences between study groups.
**Percentages based on known numbers. Strengths
***Summary of womans number of deliveries between 1986 and
The main advantage is the large size of this study. The
2004.
****Time elapsed from the first delivery to the end of the study Swedish registries contain information on practically all
period (31 December 2004). women delivered, and validation has shown that the data
are reliable.17 All Swedish citizens obtain health care funded
publicly, and few seek care outside the system.
delivered by caesarean section was 0.1%. In women with the
diagnosis of endometriosis after caesarean section the pro- Weaknesses
portion with scar endometriosis was 7/749 (9%). We were unable to control for all confounding factors. The
Figure 1 shows the KaplanMeier estimates (with diagnosis of endometriosis is often delayed,19 and
95% CIs) for endometriosis by years after the first vaginal undiagnosed endometriotic lesions may have been present
delivery or the first caesarean section, respectively. For both prior to the first caesarean section. However, this could
groups, the proportion of women who had ever had a also be the case in the vaginal delivery control group. We
diagnosis of endometriosis increased linearly with the time excluded women who had had the diagnosis of endometri-
elapsed from the first vaginal or first abdominal delivery, osis before the first delivery, but as the PAR started in

2013 The Authors BJOG An International Journal of Obstetrics and Gynaecology 2013 RCOG 1063
 Andolf et al.

Table 3. Hazard ratios for endometriosis obtained by Cox analyses

Factor Univariate models Multivariate model*

HR 95% CI HR 95% CI

Maternal age
5year increase, linear term 0.59 0.450.78 0.74 0.560.98
Quadratic term 1.06 1.031.08 1.03 1.001.06
Simultaneous** Simultaneous**
P = 4.0 9 10 9 P = 0.073
Body mass index (kg/m2)
One-step increase 0.99 0.981.00 0.98 0.970.99
Any smoking
Yes versus no 1.22 1.131.33 1.20 1.111.30
Years of involuntary childlessness
1-year step increase, linear term 1.11 1.091.13 1.09 1.071.11
Any caesarean section
Yes versus no 1.82 1.691.97 1.79 1.661.94

*The multivariate model included all of the listed variables.

**P value for the the simultaneous effect of the linear and quadratic term.

Breastfeeding has been reported to be less frequent after

caesarean section.20 Women with previous infertility may
be less inclined to use hormonal contraceptives. Both may
decrease the risk for endometriosis by inhibiting ovulation.
Likewise, previous abdominal surgery has been linked to an
increased risk for endometriosis.21 We lacked this informa-
tion also, which could influence the results. We did not
have access to information on marital status or educational
level; however, previous experience from the Swedish Medi-
cal Birth Register has shown that maternal smoking, parity,
age, and BMI are the factors that are most strongly linked
with delivery mode. Despite this, adjusting for these factors
no more than marginally changed the HR for endometri-
osis (caesarean section versus vaginal birth). Therefore, we
do not think that the analysis would benefit from including
more possible confounding factors.

Figure 1. Percentage of women who have been diagnosed with
endometriosis by years after first vaginal delivery or first caesarean
section, respectively.
1987, women with an in-hospital diagnosis of endometri-
osis before that time could not be excluded. Also, no reli-
able register on outpatients is available in Sweden for the
period studied. If the diagnosis of endometriosis was made
before 1987, or merely as an outpatient diagnosis, this and
the ensuing infertility may have contributed to the indica-
tion for caesarean section, and thus may have distorted the
results. On the other hand, adjustment for years of invol-
untary childlessness only marginally altered our results.
Interpretation
Endometriosis is clinically important in increasing the risk
for pelvic pain, infertility, and cancer; however, it is unclear
from our study whether the observed HR of 1.8 is merely
an association, or is truly indicative that caesarean section
increases the risk of developing endometriosis. Two caesar-
ean sections did not increase the risk of being diagnosed
with endometriosis in our study. This absence of a dose
response effect may, however, reflect the fact that women
who develop endometriosis after a first caesarean section
may be less likely to have another delivery because of pain
symptoms and possible subfertility. Furthermore, women
diagnosed with endometriosis after first caesarean section
are no longer at risk of developing endometriosis for the
first time.

1064 2013 The Authors BJOG An International Journal of Obstetrics and Gynaecology 2013 RCOG

Theoretically, pregnancy and caesarean section could
increase the risk for endometriosis. The pathogenesis of
endometriosis is not fully known, but immunological fac-
tors as well as metaplasia are considered to be important.16
Pregnancy is a state of altered immune response. Metapla-
sia can occur when endometrial cells are spread in the
abdominal cavity after entry into the uterus. One recent
study has shown that scar endometriomas are more fre-
quent after unlaboured caesarean sections. The authors
conclude that this may elucidate the pathogenesis of endo-
metriosis. Immunological changes occur when labour starts.
These changes may contribute to a lower risk of endome-
triosis in laboured caesarean sections.22
Conclusion
Further studies should focus on investigating the pathogen-
esis of endometriosis in relation to pregnancy and delivery,
as well as studies minimising confounding factors such as
diagnosis of endometriosis before the first delivery, previ-
ous surgery, breastfeeding, and hormonal contraception. At
present, the information from this study cannot be used
clinically.
Disclosure of interests
There are no conflicts of interest to declare.
Contribution to authorship
EA took an active role in the conception, planning, carrying
out, analysing, and writing-up of this study. MT and KK
planned, carried out, analysed data, and wrote up the study.
Details of ethics approval
The study was approved by the Research Ethics Committee
at Karolinska Institutet, Stockholm, Sweden, no. 2005/89-
31, date is 16 February 2005.
Funding
Financial support was provided by the Karolinska Institutet
and Martin Rind foundations, and by the Swedish Council
for Work Life and Social Research.
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