Loop Electrosurgical Excision Procedure and the Risk for Preterm

Loop Electrosurgical Excision Procedure and
the Risk for Preterm Delivery
Annu Heinonen, MD, Mika Gissler, DSc, MPolSc, Annika Riska,
Anna-Maija Tapper, MD, PhD, and Maija Jakobsson, MD, PhD
OBJECTIVE: To estimate whether the severity of cervical
intraepithelial neoplasia (CIN) and the loop electrosurgical excision procedure (LEEP) increase the risk for
preterm delivery, and to evaluate the role of repeat LEEP
and time interval since LEEP.
METHODS: This was a retrospective register-based study
from Finland from 1997 to 2009. We linked Hospital
Discharge Register and Finnish Medical Birth Register data.
Case group women consisted of 20,011 women who
underwent LEEP during the study period and their subsequent singleton deliveries in 1998–2009. Control population included women from the Medical Birth Register
with no LEEP (n5430,975). The main outcome measure
was preterm delivery before 37 weeks of gestation.
RESULTS: The risk for preterm delivery increased after
LEEP. Women with previous LEEP had 547 (7.2%) preterm
deliveries, whereas the control population had 30,151
(4.6%) preterm deliveries (odds ratio [OR] 1.61, confidence
interval [CI] 1.47–1.75, number needed to harm 38.5). The
overall preterm delivery rate in the study period was 4.6%
for singleton deliveries. Repeat LEEP was associated with an
almost threefold risk for preterm delivery (OR 2.80, CI 2.28–
3.44). The severity of CIN did not increase the risk for preterm delivery. However, with LEEP for carcinoma in situ
or microinvasive cancer, the risk for preterm delivery was
From the Department of Obstetrics and Gynecology, Helsinki University Central
Hospital, and the National Institute of Health and Welfare, Helsinki, Finland;
and the Nordic School of Public Health, Gothenburg, Sweden.
Supported by grants from the Research Foundation of the University of Helsinki,
Helsinki, Finland.
Presented in abstract form at the EUROGIN Conference, May 8–11, 2011,
Lisbon, Portugal, and as a poster at the 28th International Papillomavirus
Conference, November 30–December 6, 2012San Juan, Puerto Rico,.
Corresponding author: Annu Heinonen, MD, Women’s Hospital, Helsinki University Hospital Haartmaninkatu 2, PL 140, 00029 HUS Finland; e-mail:
[email protected].
Financial Disclosure
The authors did not report any potential conflicts of interest.
© 2013 by The American College of Obstetricians and Gynecologists. Published
by Lippincott Williams & Wilkins.
ISSN: 0029-7844/13
VOL. 121, NO. 5, MAY 2013
MD, PhD,
Jorma Paavonen,
MD, PhD,
higher (OR 2.55, CI 1.68–3.87). The increased risk also was
associated with non-CIN lesions (OR 2.04, CI 1.46–2.87).
Similarly, the risk was increased after diagnostic LEEP (OR
1.39, 95% CI 1.16–1.67). Time interval since LEEP was not
associated with preterm delivery. Adjusting for maternal
age, parity, socioeconomic or marital status, urbanism, and
previous preterm deliveries did not change the results.
CONCLUSION: The risk for preterm delivery was
increased after LEEP regardless of the histopathologic
diagnosis. The risk was highest after repeat LEEP, which
should be avoided, especially among women of reproductive age.
(Obstet Gynecol 2013;121:1063–8)
DOI: 10.1097/AOG.0b013e31828caa31
LEVEL OF EVIDENCE: II
C
ervical intraepithelial neoplasia (CIN) is a precancerous lesion common in women of reproductive age.1
Effective treatment of high-grade lesions is important to
prevent cervical cancer. However, only a small proportion of low-grade lesions proceed to high-grade lesions or
invasive cancer.2,3 The most common treatment for CIN
is loop electrosurgical excision procedure (LEEP). Several studies have shown an association between all types
of excisional treatments of the cervix, including LEEP,
and the risk for preterm delivery.4–7 The risk for preterm
delivery increases with the depth and volume of the
excised cone.8 Before cancerous lesion, CIN itself also
may increase the risk.9,10 Thus, it could be assumed that
this risk increases with the increasing severity of CIN.
The objective was to estimate whether LEEP and
the severity of CIN increase the risk for preterm
delivery. Furthermore, we wanted to assess the effect
of repeat LEEP. We hypothesized that a short time
interval between LEEP and delivery further increases
the risk for preterm delivery.
MATERIAL AND METHODS
We used Hospital Discharge Register to identify
women of reproductive age (15–49 years) who had
OBSTETRICS & GYNECOLOGY
1063
LEEP for cervical lesions from 1997 to 2009. We
linked this information with Medical Birth Register
data to identify subsequent singleton deliveries. The
data linkage was performed by using the encrypted
unique personal identification numbers of women in
both registers. Both registers are controlled by the
National Institute of Health and Welfare and include
the whole population.
The Hospital Discharge Register collects information on all hospitalizations since 1967. According
to the latest quality study, 95% of the hospitalizations
were registered and 97% of main diagnoses concerning pregnancy, delivery, and puerperium were correctly reported. Increased use of electronic patient
journals has further improved the completeness and
validity of the Hospital Discharge Register.11 The
Hospital Discharge Register includes all day surgical
procedures since 1994 and also all outpatient visits in
public hospitals since 1998. The medical procedures
performed at hospitals are identified by surgical procedure codes (since 1997 based on the Finnish version
of Nordic Classification on Surgical Procedures).
The Medical Birth Register is nationwide and
includes baseline data of pregnant women and all
interventions during pregnancy and delivery. It also
includes information on the outcomes of the newborns
during the first 7 days. Data for less than 0.1% of all
newborns are missing from the register, and information
of such cases is routinely obtained from the Central
Population Register and Cause-of-Death Register. The
information in the Medical Birth Register is routinely
controlled by the National Institute of Health and
Welfare, and incorrect information is sent back to the
birth hospital for revision in case of missing or
obviously incorrect data. The data correspond well with
the data in hospital records.11
Preterm delivery was defined as delivery before 37
weeks of gestation. Extremely preterm delivery (less
than 28 weeks of gestation) was studied separately. We
also analyzed the risk for small for gestational age based
on sex-specific national standards,12 low birth weight
(less than 2,500 g), and perinatal deaths (from 22 weeks
of gestation until 1 week after birth). The socioeconomic status was based on the maternal occupation at
the time of delivery and classified according to national
standards kept by Statistics Finland (www.stat.fi/meta/
kas/sosioekon_asema_en.html).
Our case group women consisted of 20,011
women with 25,101 LEEPs from 1997 to 2009. Of
these women 5,114 had subsequent singleton deliveries according to the Medical Birth Register. The total
number of deliveries was 7,636. Our control population consisted of 430,975 women in the Medical Birth
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Heinonen et al
LEEP and Preterm Delivery
Register with no previous LEEP and their subsequent
658,179 singleton deliveries from 1998 to 2009. No
other exclusion criteria were used for the control
population. The Finnish version of the Nordic Classification of Surgical Procedures uses LCD03 code for
LEEP exclusively since 1997. We used this code to
identify patients with LEEP treatment from the Hospital Discharge Register. Furthermore, women with
repeat LEEP had this code at least twice at different
time points. The severity of the CIN lesion was
classified according to the latest version of the International Classification of Diseases (version 10). The codes to
identify severity were as follows: R87.6 abnormal cytology; A63.0 condyloma accuminatum; N87.0 mild dysplasia (CIN 1); N87.1 moderate dysplasia (CIN 2); N87.2
severe dysplasia (CIN 3); N87.9 nonspecific dysplasia;
D06.0, D06.1, D06.7, and D06.9 carcinoma in situ of
cervix; and C53.00–C53.99 carcinoma of the cervix.
For some LEEPs, no corresponding diagnosis was
found and these were classified as nonspecific. The
group formed by diagnosis A63.0 (condyloma accuminatum) was classified as having non-CIN lesions. The
most severe diagnosis was recorded. We checked from
the Hospital Discharge Register all diagnoses of women
who had diagnostic LEEP without CIN. We further
studied the time interval between the procedure and
the delivery.
We calculated odd ratios (ORs), 95% confidence
intervals (CIs), and number needed to harm (NNH) for
preterm delivery. We adjusted these for maternal age,
socioeconomic status, marital status, urbanity of woman’s residence (urban, semi-rural, and rural as defined
by Statistics Finland; www.stat.fi/meta/luokitukset/
kuntaryhmitys/001-2008/1_en.html), and time since
LEEP. In a second model, we adjusted the results for
all of these and also for previous preterm deliveries. We
used logistic regression to adjust for the confounding
factors. To avoid clustering of preterm deliveries within
individuals, we repeated the analyses including only the
first deliveries after LEEP (n55,114) and separately for
primiparous deliveries (n53,355).
The register-keeping organization, the National
Institute of Health and Welfare, authorized the use of
anonymous register data in scientific research. The
ethical evaluation was performed by the register
authorities and the data protection ombudsman who
reviewed the study before the study permission was
given, as required by the legislation.
RESULTS
Characteristics of the study population are presented
in Table 1. The control population was slightly younger than the case population; the mean age of study
OBSTETRICS & GYNECOLOGY
population was 30.8 years (standard deviation [SD] 4.8)
and 30.0 years (SD 5.5) for the control population. The
number of previous deliveries was approximately the
same in both populations; mean parity for study population was 1.0 (SD 1.2) and for the control population
was 0.9 (SD 1.1). The majority of the study population
(61%) belonged to socioeconomic status “other,”
including stay-at-home mothers, students, and others
for whom no specific socioeconomic status could be
determined. Women with LEEP lived more often in
cities and large towns, and these women were more
often single. Women with LEEP were more often
smokers. Up to 18% continued smoking after the first
trimester. In the group of “other socioeconomic status,”
stay-at-home mothers (17.6%), students (18.6%), and
those with unknown occupations smoked more than
parturients in general (15.2%).
Women with previous LEEP had 547 (7.2%)
preterm deliveries, whereas the corresponding figure
among control population was 30,151 (4.6%; OR
1.61, 95% CI 1.47–1.75, NNH 38.5) (Table 2). The
overall preterm delivery rate in the study period was
5.3% for all deliveries and 4.6% for singleton deliveries. The severity of CIN did not increase the risk for
preterm delivery. Loop electrosurgical excision procedure performed for non-CIN lesions increased the
Table 1. Background Characteristics by Delivery in Case and Control Groups
Control Group—Women
Without LEEP
Case Group—Women With LEEP
Characteristic
Maternal age (y)
Younger than 20
20–24
25–29
30–34
35–39
40 and older
Parity
0
1
2
3
4 or more
Socioeconomic status*
Upper white-collar
worker
Lower white-collar worker
Blue-collar worker
Others
Urbanism
City
Population center
Rural
Unknown, abroad
Marital status
Single
Married or cohabiting
Unknown
Smoking status
No
Discontinued during 1st
trimester
Yes
Unknown
All Deliveries
(n57,636)
First Delivery
(n55,114)
Primiparous
Deliveries (n52,255)
Deliveries in Medical Birth
Register (n5658,179)
50
833
2,490
2,766
1,278
219
(0.7)
(10.9)
(32.6)
(36.2)
(16.7)
(2.9)
46
635
1,723
1,766
777
157
(0.9)
(12.4)
(33.7)
(34.7)
(15.2)
(3.1)
46
531
1,290
988
352
48
(1.4)
(15.8)
(38.5)
(29.4)
(10.5)
(1.4)
18,242
109,153
207,706
200,490
99,130
23,457
(2.8)
(16.6)
(31.6)
(30.5)
(15.1)
(3.6)
3,355
2,547
1,126
388
220
(43.9)
(33.4)
(14.7)
(5.1)
(2.9)
3,041
1,150
633
192
98
(59.5)
(22.5)
(12.4)
(3.8)
(1.9)
3,355 (100)
273,489
218,186
100,303
34,989
31,212
(41.6)
(33.1)
(15.2)
(5.3)
(4.7)
663 (8.7)
477 (9.3)
1,688 (22.1)
665 (8.7)
4,620 (60.5)
5,428
1,285
915
8
(71.1)
(16.8)
(12)
(0.1)
336 (10.0)
87,482 (13.3)
1,201 (23.5)
491 (9.6)
2,945 (57.6)
776 (23.1)
240 (7.2)
2,003 (59.7)
179,580 (27.3)
70,614 (10.7)
320,503 (48.7)
3,689
815
605
5
2,552
480
312
2
428,588
111,138
116,871
1,582
(72.1)
(15.9)
(11.8)
(0.1)
(76.1)
(14.3)
(9.6)
(0.1)
(65.1)
(16.9)
(17.8)
(0.2)
985 (12.9)
6,579 (86.2)
72 (0.9)
765 (15.0)
4,295 (84.0)
54 (1.1)
523 (15.6)
2,802 (83.5)
35 (1)
64,191 (9.8)
580,207 (88.2)
13,781 (2.1)
5,733 (75.1)
341 (4.5)
3,744 (73.2)
263 (5.1)
2,589 (77.2)
214 (6.4)
544,078 (82.7)
19,582 (3.0)
1,377 (18.0)
185 (2.4)
982 (19.2)
125 (2.4)
506 (15.1)
52 (1.5)
76,210 (11.6)
18,309 (2.8)
LEEP, loop electrosurgical excision procedure.
Data are n (%).
* Based on maternal occupation at time of delivery. Others include students and housewives.
VOL. 121, NO. 5, MAY 2013
Heinonen et al
LEEP and Preterm Delivery
1065
Table 2. Risk for Preterm Birth After Loop Electrosurgical Excision Procedure, Crude Figures
Diagnoses
Nonspecific†
Cytologic abnormality‡
Non-CIN
CIN grade unknown
CIN 1
CIN 2
CIN 3
Cancer in situ or cancer
Repeat LEEP
Total
LEEP
Singleton Births
1,641
6,253
945
104
3,686
4,730
2,559
908
4,275
25,101
388
1,982
414
24
1,372
1,549
808
299
870
7,636
Preterm Births
30
124
37
1
88
88
51
25
103
547
OR (95% CI)*
(7.7)
(6.3)
(8.9)
(4.2)
(6.4)
(5.7)
(6.3)
(10.9)
(11.8)
(7.2)
1.75
1.39
2.04
0.91
1.43
1.25
1.40
2.55
2.80
1.61
(1.20–2.53)
(1.16–1.67)
(1.46–2.87)
(0.12–6.71)
(1.15–1.77)
(1.01–1.56)
(1.06–1.86)
(1.68–3.87)
(2.28–3.44)
(1.47–1.75)
LEEP, loop electrosurgical excision procedure; OR, odds ratio; CI, confidence interval; CIN, cervical intraepithelial neoplasia.
Data are n or n (%) unless otherwise specified.
* Control population consisted of women in Medical Birth Register without previous LEEP (n525,101 women with preterm birth rate of
4.45%).
†
Corresponding histopathologic diagnosis unknown.
‡
Diagnostic LEEP with no histopathologic abnormality.
risk twofold (OR 2.04, 95% CI 1.46–2.87). However,
for cancerous lesions this risk was somewhat higher
(OR 2.55, 95% CI 1.68–3.87). Repeat LEEP increased
the risk almost threefold (OR 2.80, 95% CI 2.28–
3.44). The risk for having low birth weight was similarly increased (OR 1.50, 95% CI 1.30–1.73). The
risks for extremely preterm delivery (OR 1.27, 95%
CI 0.75–2.16), small for gestational age (OR 0.27,
95% CI 0.70–1.31), and perinatal death (OR 1.25,
95% CI 0.76–1.89) were not increased.
Adjustment for maternal age, socioeconomic status, marital status, and urbanism did not change the
results. Time interval since LEEP had no effect (OR
0.98, 95% CI 0.96–1.00). We repeated the analyses
separately for the first delivery after LEEP and for primiparous women, but it did not change the results
(Table 3). Even adjusting for previous preterm deliveries did not change the results.
DISCUSSION
Our study shows that LEEP is associated with
increased risk for preterm delivery. The increasing
severity of CIN did not increase the risk for preterm
delivery. This risk also was increased after LEEPs
performed for non-CIN lesions. Repeat LEEP was
a strong risk factor for preterm birth. The so-called
diagnostic LEEP was strikingly common during the
study period and also increased the risk for preterm
delivery. These procedures peaked in 1999–2000
(n5859) but have been gradually declining since then
(n5282 in 2009; data not shown).
Our study has several strengths. We used highquality population-based data from the Finnish Medical Birth Register and Hospital Discharge Register
with high coverage and proven quality. We obtained
data from more than 7,000 deliveries including 547
preterm deliveries. The large study population and
Table 3. Risk for Preterm Birth by Severity of Histology, Adjusted for Background Factors
All Deliveries
Adjusted 1*
Adjusted 2†
Cytologic abnormality
Non-CIN
CIN 1
CIN 2
CIN 3
Cancer in situ or cancer
Repeat LEEP
Time interval since LEEP
1.65 (1.47–1.85)
1.43
2.16
1.50
1.30
1.44
2.56
2.77
0.98
(1.17–1.74)
(1.53–3.07)
(1.19–1.88)
(1.04–1.63)
(1.08–1.93)
(1.68–3.90)
(2.23–3.45)
(0.96–1.00)
First Deliveries After LEEP
1.63
1.66
1.43
1.75
1.58
1.57
1.63
2.50
2.52
0.99
(1.34–1.98)
(1.37–2.02)
(1.06–1.92)
(0.99–3.10)
(1.14–2.20)
(1.16–2.14)
(1.10–2.42)
(1.38–4.48)
(1.74–3.64)
(0.96–1.05)
Primiparous Deliveries After LEEP
1.61 (1.34–1.93)
1.39
2.15
1.33
1.34
1.44
3.28
2.59
1.00
(1.05–1.85)
(1.34–3.43)
(0.96–1.85)
(0.98–1.85)
(0.94–2.20)
(1.81–5.94)
(1.91–3.50)
(0.97–1.03)
LEEP, loop electrosurgical excision procedure; CIN, cervical intraepithelial neoplasia.
Data are odds ratio (95% confidence interval).
* Adjusted for maternal age, socioeconomicstatus, marital status, living environment, and time since procedure.
†
Adjusted for all these and previous preterm deliveries.
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OBSTETRICS & GYNECOLOGY
the absence of reporting, recall, and participation bias
improve the credibility of our results. We were able to
adjust for several important variables, such as maternal
age, socioeconomic status, marital status, and urbanism.
Adjusting for previous preterm deliveries, which is
known to be the main risk factor for preterm delivery,13
did not change the results. In addition, we had information about maternal smoking recorded during the
first antenatal visit. Women with LEEP smoked more
often during pregnancy than other women. We did not
adjust specifically by smoking status because socioeconomic status and smoking are known to be strongly
correlated in Finland.14 We chose to adjust for socioeconomic status rather than smoking, because the data
of socioeconomic status are more accurate.
This study also has some limitations. The risk for
preterm delivery increases with the depth and volume
of the excised cone,8 and those performing colposcopies attempt to tailor cones to be less than 10 mm in
depth.15 We could not determine the cone size because
this information is not available in the register. However, the risk for preterm delivery was higher after
LEEP performed for high-grade CIN or cancer than
after LEEP preformed for low-grade CIN. Deeper
cones are undoubtedly performed for such lesions.
Some LEEPs may have been performed in private clinics not captured by the registers. In Finland, however,
only few LEEP procedures are performed outside hospitals. Therefore, it is unlikely that a small number of
missing cases would have changed our results.
When using national register data, the comparison
group consists of a population of normal pregnant
women, which might exaggerate the risk for preterm
birth. However, in a study by Sadler et al16 the comparison group was formed by untreated colposcopy patients,
and the risk associated with LEEP was still significant.
Thus, we have no reason to believe that changing our
comparison group would change the results.
Previous meta-analyses1,4,6 and many single
studies5,16–18 have demonstrated increased risk for preterm delivery after LEEP. The risk was again observed in
recent studies from Belgium7 and England, although in
the latter to a smaller degree than in previous studies.19
The study from Belgium consisted of a small study population (n597); however, the study from England was
large, with 4,776 deliveries after cervical treatment,
although the methods of treatment included other treatment as well as LEEP. The new finding in our study was
that the severity of CIN lesion did not correlate with the
risk for preterm delivery. This is in accordance with
a Danish register-based study.17 In one study the risk
for preterm birth was increased among women
with untreated CIN 3 lesions.10 Women who had poor
VOL. 121, NO. 5, MAY 2013
compliance with treatment for CIN 3 may, in fact, have
other risk factors for preterm delivery such as poor education, lower socioeconomic class, sexually transmitted
diseases, or smoking. Reilly et al20 found that the risk for
preterm birth was increased among colposcopy patients
regardless of treatment. However, the reason for colposcopy referral or severity of lesions was not reported.
The time interval between LEEP procedure and
delivery had no effect on the risk for preterm delivery.
In one study, the short interval between the treatment
and delivery increased the risk for preterm delivery.21
This study, however, did not consider several confounding factors making the results difficult to interpret. Our
results indicate that women do not need to postpone
pregnancy after LEEP.
According to our study, the overall risk for
preterm delivery is elevated after LEEP. Thus, careful
consideration is important when treating women of
reproductive age for CIN. In particular, repeat LEEP
should be avoided if possible.
REFERENCES
1. Kyrgiou M, Koliopoulos G, Martin-Hirsch P, Arbyn M,
Prendiville W, Paraskevaidis E. Obstetric outcomes after conservative treatment for intraepithelial or early invasive cervical
lesions: systematic review and meta-analysis RID B-6887-2009.
Lancet 2006;367:489–98.
2. Moscicki A, Schiffman M, Kjaer S, Villa LL. Updating the natural
history of HPV and anogenital cancer. Vaccine 2006;24:42–51.
3. Wright TC Jr, Massad LS, Dunton CJ, Spitzer M, Wilkinson EJ,
Solomon D, et al. 2006 consensus guidelines for the management of women with cervical intraepithelial neoplasia or adenocarcinoma in situ. Obstet Gynecol 2007;197:340–5.
4. Arbyn M, Kyrgiou M, Simoens C, Raifu AO, Koliopoulos G,
Martin-Hirsch P, et al. Perinatal mortality and other severe
adverse pregnancy outcomes associated with treatment of cervical intraepithelial neoplasia: meta-analysis RID B-6887–2009.
BMJ 2008;337:a1284.
5. Jakobsson M, Gissler M, Paavonen J, Tapper A. Loop electrosurgical excision procedure and the risk for preterm birth. Obstet
Gynecol 2009;114:504–10.
6. Bruinsma FJ, Quinn MA. The risk of preterm birth following
treatment for precancerous changes in the cervix: a systematic
review and meta-analysis. BJOG 2011;118:1031–41.
7. Simoens C, Goffin F, Simon P, Barlow P, Antoine J, Foidart J,
et al. Adverse obstetrical outcomes after treatment of precancerous cervical lesions: a Belgian multicentre study. BJOG
2012;119:1247–55.
8. Noehr B, Jensen A, Frederiksen K, Tabor A, Kjaer SK. Depth
of cervical cone removed by loop electrosurgical excision procedure and subsequent risk of spontaneous preterm delivery.
Obstet Gynecol 2009;114:1232–8.
9. Bruinsma F, Lumley J, Tan J, Quinn M. Precancerous changes
in the cervix and risk of subsequent preterm birth. BJOG 2007;
114:70–80.
10. Shanbhag S, Clark H, Timmaraju V, Bhattachaya S,
Cruickshank M. Pregnancy outcome after treatment for cervical
intraepithelial neoplasia. Obstet Gynecol 2009;114:727–35.
Heinonen et al
LEEP and Preterm Delivery
1067
11. Gissler M, Shelley J. Quality of data on subsequent events in
a routine medical birth register. Med Inform Internet Med
2002;27:33–8.
12. Pihkala J, Hakala T, Voutilainen P, Raivio K. Characteristic of
recent fetal growth curves in Finland. Duodecim 1989;105:1540–6.
13. Goldenberg RL, Culhane JF, Iams JD, Romero R. Preterm
birth 1-epidemiology and causes of preterm birth. Lancet
2008;371:75–84.
14. Jaakkola N, Jaakkola M, Gissler M, Jaakkola J. Smoking during
pregnancy in Finland: determinants and trends, 1987-1997. Am
J Public Health 2001;91:284–6.
15. Ang C, Mukhopadhyay A, Burnley C, Faulkner K, Cross PA,
Martin-Hirsch P, et al. Histological recurrence and depth of
loop treatment of the cervix in women of reproductive age:
incomplete excision versus adverse pregnancy outcome. BJOG
2011;118:685–92.
16. Sadler L, Saftlas A, Wang W, Exeter M, Whittaker J,
McCowan L. Treatment for cervical intraepithelial neoplasia
and risk of preterm delivery RID C-2215-2009. JAMA 2004;
291:2100–6.
17. Noehr B, Jensen A, Frederiksen K, Tabor A, Kjaer SK. Loop
electrosurgical excision of the cervix and subsequent risk for
spontaneous preterm delivery: a population-based study of singleton deliveries during a 9-year period. Obstet Gynecol 2009;
201:33.e1.
18. Albrechtsen S, Rasmussen S, Thoresen S, Irgens LM,
Iversen OE. Pregnancy outcome in women before and after
cervical conisation: population based cohort study. BMJ 2008;
337:a1343.
19. Castanon A, Brocklehurst P, Evans H, Peebles D, Singh N,
Walker P, et al. Risk of preterm birth after treatment for cervical intraepithelial neoplasia among women attending colposcopy in England: retrospective-prospective cohort study.
BMJ 2012;345:e5174.
20. Reilly R, Paranjothy S, Beer H, Brooks CJ, Fielder HM,
Lyons RA. Birth outcomes following treatment for precancerous changes to the cervix: a population-based record linkage
study. BJOG 2012;119:236–44.
21. Himes KP, Simhan HN. Time from cervical conization to pregnancy and preterm birth. Obstet Gynecol 2007;109:314–9.
Standards for Different Types of Articles
Guidelines for five different types of articles have been adopted by Obstetrics & Gynecology:
1. CONSORT (Consolidated Standards of Reporting Trials) standards for reporting randomized trials
2. PRISMA (Preferred Reporting Items for Systematic Reviews and Meta-Analyses) guidelines for metaanalyses and systematic reviews of randomized controlled trials
3. MOOSE (Meta-analysis of Observational Studies in Epidemiology) guidelines for meta-analyses and
systematic reviews of observational studies
4. STARD (Standards for Reporting of Diagnostic Accuracy) standards for reporting studies of diagnostic
accuracy
5. STROBE (Strengthening the Reporting of Observational Studies in Epidemiology) guidelines for the
reporting of observational studies
Investigators who are planning, conducting, or reporting randomized trials, meta-analyses of randomized trials,
meta-analyses of observational studies, studies of diagnostic accuracy, or observational studies should be thoroughly familiar with these sets of standards and follow these guidelines in articles submitted for publication.
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