Original Article

J Med Screen
2014, Vol. 21(1) 38–50
Condom use in prevention of Human ! The Author(s) 2014
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DOI: 10.1177/0969141314522454

neoplasia: systematic review of msc.sagepub.com

longitudinal studies

Janni Uyen Hoa Lam1, Matejka Rebolj1,, Pierre-Antoine Dugué1,

Jesper Bonde2,3, My von Euler-Chelpin1 and Elsebeth Lynge1

Abstract
Objectives: Based on cross-sectional studies, the data on protection from Human Papillomavirus (HPV) infections related to
using male condoms appear inconsistent. Longitudinal studies are more informative for this purpose. We undertook a system-
atic review of longitudinal studies on the effectiveness of male condoms in preventing HPV infection and cervical neoplasia.
Methods: We searched PubMed using MeSH terms for articles published until May 2013. Articles were included if they studied
a change in non-immunocompromized women’s cervical HPV infection or cervical lesion status along with the frequency of
condom use.
Results: In total, 384 abstracts were retrieved. Eight studies reported in 10 articles met the inclusion criteria for the final
review. Four studies showed a statistically significantly protective effect of consistent condom use on HPV infection and on
regression of cervical neoplasia. In the remaining four studies, a protective effect was also observed for these outcomes,
although it was not statistically significant.
Conclusions: Consistent condom use appears to offer a relatively good protection from HPV infections and associated
cervical neoplasia. Advice to use condoms might be used as an additional instrument to prevent unnecessary colposcopies
and neoplasia treatments in cervical screening, and to reduce the risk of cervical cancer.

Keywords
condom, Human Papillomavirus, cervical cancer, cervical neoplasia, infection, prevention

Date received: 2 December 2013; accepted: 13 January 2014

The studies showed mixed results. The inconsistency of

Introduction
Persistent infection with sexually transmitted high-risk
genotypes of Human Papillomavirus (HPV) is a necessary
cause of cervical cancer.1 Vaccines protect against two of
the 13 high-risk HPV genotypes.2 Treatment of screen-
detected cervical intraepithelial neoplasia (CIN) can
reduce the incidence of cervical cancer. However, cervical
cancer can still develop after CIN treatment,3 and after
normal screening tests.4 Screening and vaccination are not
used routinely where the burden of cervical cancer is
highest.
Use of male condoms (henceforth denoted as ‘‘con-
doms’’) has shown a considerable protective effect, when
used correctly and consistently, against several sexually
transmitted infections (STI), including human immuno-
deficiency virus, trichomoniasis, chlamydia, and gonor-
rhea. Data on protective effect from HPV infections and
related cervical lesions have been less consistent. In their
systematic review from 2002, Manhart and Koutsky iden-
tified 20 relevant studies, 19 of them cross-sectional.5
the evidence regarding a protective effect could suggest
that condoms are not a highly effective method of prevent-
ing HPV infections.
The findings from Manhart and Koutsky’s review were
echoed in a 2004 report on cervical cancer prevention to
the USA Congress from the Centers for Disease Control
and Prevention (CDC). The report concluded that con-
doms cannot be recommended for primary prevention of
genital HPV infections, although it also stated that
1
Department of Public Health, University of Copenhagen, DK-1014
Copenhagen
2
Department of Pathology, Copenhagen University Hospital Hvidovre,
DK-2650 Hvidovre
3
Clinical Research Centre, Copenhagen University Hospital Hvidovre,
DK-2650 Hvidovre
Corresponding author:
Matejka Rebolj, Department of Public Health, University of Copenhagen,
Øster Farimagsgade 5, DK-1014 Copenhagen K, Denmark.
Email: mare@sund.ku.dk
Lam et al.
evidence suggested effectiveness against cervical cancer.6
Also in 2004, the US Food and Drug Administration
(FDA) considered changing the labeling of condoms by
adding information on the lack of evidence showing pro-
tection against HPV infections.7 The proposed labeling
change could have spillover effects, eg. by undermining
condom use to avoid other STI. This took place despite
acknowledging Manhart and Koutsky’s cautionary obser-
vation that the reviewed studies were not set up to evalu-
ate condom use, did not adequately measure condom use,
and, because of cross-sectional design, could not establish
the temporal sequence between exposure and outcome.5
This debate underscores the importance of a careful
assessment of epidemiological evidence used in making
public health recommendations.
Compared with cross-sectional studies, longitudinal
studies are more reliable in establishing whether non-
use of condoms preceded an infection/disease. By 2006,
two longitudinal studies had been published showing a
protective effect of condoms on HPV infections.8,9 These
studies led, in 2008, to the FDA ruling against the
change of condom labeling, and the CDC now also
acknowledges that condoms can be useful in preventing
HPV infections and related diseases. More relevant lon-
gitudinal studies have been published since, and these
can potentially give more information on the effective-
ness of condoms for the purpose. We undertook a sys-
tematic review of longitudinal studies on the use of
condoms in preventing HPV infections and cervical neo-
plasia, assessing in depth their study designs. As devel-
oped countries will probably be switching from cytology-
to HPV-based primary cervical screening in the near
future, we discussed the relevance of the findings in the
context of cervical screening.
Methods
A systematic search in PubMed (Appendix) retrieved 384
abstracts. All retrieved reviews and meta-analyses were
perused for additional studies. Although a formal ranking
of study quality was not made, two authors (JUHL, MR)
independently selected relevant studies and abstracted all
information on the studies and their quality into pre-
specified tables. In case of disagreement, consensus was
used. Additional information on the included studies
was obtained from related publications.
English, French, Danish, Norwegian, Swedish,
German, Chinese, or Dutch-language longitudinal studies
on condom use and HPV infections or cervical lesions were
included. The studies assessed a change in the woman’s
HPV infection (ie. incidence, clearance, persistence), or a
change in her cervix uteri diagnosis (ie. incidence, regres-
sion, persistence of cytologically or histologically con-
firmed lesions). It has been hypothesized that regression
of CIN might be accelerated by condoms blocking a con-
tinuous transmission of HPV infections.8 We therefore
considered that studies detecting a change in CIN as the
outcome are also informative for our purpose.
39
Studies were excluded if: they included a substantial
proportion of immunocompromized women, used non-
cervical HPV samples, studied female condoms, did not
include a control group, or did not measure condom use in
all sexual partnerships. Studies reporting only baseline
measurements of condom use were excluded, as any
change in the use during follow-up can be related to the
final outcome. Finally, studies were excluded if condom
use was categorized broadly, eg. in yes-no or ever-never
categories. The ‘‘yes’’ and ‘‘ever’’ categories include an
unspecified proportion of inconsistent condom users,
making it difficult to interpret the reported outcomes.
Statistical analysis
Reported indicators of relative risk (RR) of HPV infec-
tions associated with condom use were collected, regard-
less of oncogenicity (risk) of the detected genotypes.
Although low-risk genotypes do not cause cervical
cancer, the risk-based classification has been changing.
Also, there is no evidence suggesting that the protection
from HPV differs by the genotypes’ oncogenicity.
RR for one study10 was recalculated by the authors of
this review and annotated by square brackets; the 95%
confidence interval (CI) was calculated assuming normal
distribution for log(RR). Owing to heterogeneity in the
designs of the studies, a summary effect measure was
not computed. For incidence- and persistence-type out-
comes, measures of RR <1 for users v non-users indicated
a protective effect of condoms, whereas for clearance- and
regression-type outcomes, this was the case with RR >1.
Results
Based on the PubMed search, full texts were retrieved for
33 articles. Eight studies reported in 10 articles met the
inclusion criteria.8–17 For one study, we tabulated the
results from the first of three published articles; all three
reported the same endpoint with marginally different
inclusion criteria.15
Condom use and HPV infections
Ho et al.14 followed 399 HPV-negative US students
(Tables 1, 2). Their samples, obtained every six months
for about two years, were tested with two HPV assays
(polymerase chain reaction (PCR) MY09/11, Southern
blot hybridization), and the woman was considered
HPV-positive if at least one of the two was positive.
Information on condom use was collected at each visit.
The relative risk (RR) of an incident HPV infection for
women always, compared with never, using condoms
since the last visit was 0.8 (95% CI: 0.4–1.4; Table 3).
The RR was adjusted for several indicators of sexual
behavior, including the partners’ risk level.
In the study by Winer et al.,9 82 initially virginal
women were tested for HPV every four months. Samples
were analyzed using PCR PGMY09/MY11 assay, and
Table 1. Study designs of the included studies (in chronological order) focusing on the relationship between condoms, HPV infections, and cervical intraepithelial neoplasia.
Authors, year of publication
Thomas et al. 199010
Ho et al. 199814
Moscicki et al. 200113
Hogewoning et al. 20038
Inclusion criteria for the study other
than the ability to provide
Country Study design informed consent
Australia Controlled trial (partially Attending dysplasia clinic for investiga-
random allocation) tion of an abnormal smear
USA Cohort study First or second y students from a state
university and/or planning to stay in
the area for 52.5 y, not currently
pregnant, not planning to become
pregnant in 3 y, no prior cervical
biopsy or CIN treatment, 51 follow-
up visit
USA Cohort study 13–20 y, attending 1 of 2 family planning
clinics and having a pelvic exam for
any reason, non-pregnant, not cur-
rently using antibiotics, not received
or scheduled for cervical ablation, not
planning to move in 6 mo, not men-
tally retarded, English speaking,
HPVþ on HPV Profile assay, 51
HPVþ result and 53 visits, no
prevalent LSIL, did not develop HSIL
before LSIL
The Netherlands Randomized Referred for colposcopy because of an
clinical trial abnormal smear (5mild dysplasia)
and/or colposcopically or histologi-
cally diagnosed CIN, the woman and
her partner had no other sexual
partners, no CIN treatment at base-
line (i.e., CIN2 and CIN3 over 52
cervical quadrants), no regular
condom use for birth control at
baseline
Sociodemographic characteristics
of women at baseline
Me age: 25 y (18–44), me # of sex part-
ners: 6 (1–30), me period exclusively
with current partner: 24 mo (0–168),
51 extraneous partner during study
17%, smokers 65% (intervention
group) and 60% (control group)
Me age: 20 y (SD ¼ 3), non-White 43%,
13% no vaginal intercoursea
Me age 20 y (SD ¼ 2), non-White 47%,
no college 46%, md # sex partners: 5
(IQR ¼ 3–9), chlamydia or gonor-
rhoea 4%, md length sexually active
3 y, md # new partners in last 2
months 0 (IQR ¼ 0–1)
Intervention arm:b me age 34.1 y (range:
19.1–54.7); colposcopically-confirmed
CIN: CIN1 53%, CIN2 45%, CIN3
2%; histologically confirmed CIN: no
biopsy 9%, no CIN 13%, CIN1 28%,
CIN2 48%, CIN3 2%; smoking 38%,c
users of oral contraceptives 46%;c me
age at first intercourse 16.3 y (range:
13–21);c history of STI 8%;c me # of
lifetime sex partners 5.6 (range: 1–
15);c other sexual partner last year
8%;c married/living together 92%;c me
duration of relation 9.7 y (range: 0.6–
35);c me frequency of sexual inter-
course per mo 7.2 (range: 0–22.5) c
Control arm:b me age 35.1 y (range:
22.5–52.6); colposcopically-confirmed
CIN: CIN1 59%, CIN2 39%, CIN3
2%; histologically confirmed CIN: no
biopsy 7%, no CIN 18%, CIN1 41%,
CIN2 31%, CIN3 3%; smoking 64%,c
users of oral contraceptives 64%;c me
age at first intercourse 16.2 y (range:
40
Definition of condom use
Intervention group: asked to use
condoms for every sex act in
6 mo; Control group: asked to
avoid condoms for 6 mo; assessed
by interview after 3 and 6 mo
Always vs. never in the period since
the previous visit; assessed by
questionnaire at each visit
Always vs. less than always in the
period since previous visit;
assessed by interview at baseline
and interval visits
Intervention arm: asked to use con-
doms during genital-genital con-
tact for at least 3 mo (md
duration of use: 6 mo (range: 3.0–
53.7), failure to use: 7 women
with a md of 2 times (range:
1–5));b Control arm: no condom
use; verbally verified at each visit
by asking the frequency of
condom use failure
Journal of Medical Screening 21(1)
(continued)
Table 1. Continued
Inclusion criteria for the study other
than the ability to provide Sociodemographic characteristics
Lam et al.

Authors, year of publication
Winer et al. 20069
Shew et al. 200612
Sánchez-Alemán et al. 201111
Munk et al. 201215-17
Country Study design informed consent
USA Cohort study 18–22 y, undergraduate students, never
had vaginal intercourse or had first
intercourse with one male partner in
42 weeks before enrolment, had a
cervix, not pregnant, in good general
health, had vaginal intercourse during
study
USA Cohort study 14–17 y, attending primary care adoles-
cent health clinics, able to understand
English, not have any serious psychi-
atric disturbances or mental handi-
caps, not pregnant
Mexico Cohort study Sexually active university students
Norway Cohort study 25–40 y, referred to gynecology out-
patient clinic for evaluation of atypical
cytological cervical smear detected in
population-based screening, not
pregnant, no immune diseases, not
treated for immunosuppression, no
previous CIN treatment, biopsy-cone
excision interval 580 d
of women at baseline Definition of condom use
c c
13–21); history of STI 16%; me # of
lifetime sex partners 6.3 (range: 1-
30);c other sexual partner last year
0%;c married/living together 88%;c me
duration of relation 8.7 y (range: 1–
28);c me frequency of sexual inter-
course per mo 7.2 (range: 1–22.5)c
Me age: 19.3 y (SD ¼ 0.7) 100% use vs. 50 to 99% use vs. 5–
49% use vs. <5% use during 8 mo
before HPV testing;d assessed by
web-based diary every 2 weeks
Me age 15.3 y, African American 85%, <60% of coital events protected by
prior sexual experience 95%, me age condom during an HPV infection
at first coitus 13.2 y (SD ¼ 1.7) vs. >60% condom use in the last
3 mo;e assessed by interview at
every clinic visit, and by daily dia-
ries for 12 weeks at a time
Me age 21.2 y, me age at sexual debut Consistent (always) vs. inconsistent
18.7, me age of partner at woman’s (almost always, half of the time,
sexual debut 21.6 y, current smoker almost never, never) use over
36.9%, marijuana use 9.7%, self- lifetime; assessed by questionnaire
reported STI 2.5%, emergency
contraceptive pill as regular contra-
ception method 6.8%, consistent
condom use 19.8%, 52 sex partners
18.1%, same-sex sexual partner 3.4%,
casual partners 9.7%
Md age 32 y (range: 25–41),15 had given Consistent use vs. non-use or
birth 58% (md age 24 y),16 smoking inconsistent use in the period
33%, >10 sex partners 54%, 415 y at between baseline and final visit;f
first sexual intercourse 26%17 assessed by interview at baseline
and third visit

Abbreviations: # ¼ number, CIN ¼ cervical intraepithelial neoplasia, d ¼ day(s), HPV ¼ Human Papillomavirus, HSIL ¼ high-grade squamous intraepithelial lesions, IQR ¼ interquartile range, LSIL ¼ low-grade squamous
intraepithelial lesions, md ¼ median, me ¼ mean, mo ¼ month(s), SD ¼ standard deviation, STI ¼ sexually transmitted infections, y ¼ year(s).
a
Whole sample of 608 recruited women, among whom 26% were HPVþ.
b
For all 125 randomized women.
c
Based on 41% of the sample with returned questionnaires.
d
Calculated by dividing the number of condoms used for vaginal intercourse by the number of instances of vaginal intercourse during the 8-month study period.
e
Proportion of condom-protected coital events during the duration of a specific HPV infection.
41

f
Consistent use defined as partners using condoms for all instances of sexual intercourse.

Table 2. Description of women included in the studies, and main endpoints.
Authors, year of publication
10
Thomas et al. 1990
Ho et al. 199814
Moscicki et al. 200113
Hogewoning et al. 20038
Winer et al. 20069
42
Baseline cervical status
(HPV or cervical Assessment of HPV assay (# of Planned follow-up
lesions) Main study endpoint(s) endpoint detectable genotypes) duration (interval) Loss to follow-up
Histologically con- Histologically con- Biopsy at study entry, Not relevant for def- 6 mo (every 3 mo) None
firmed and adjudi- firmed regression of and at 3 (if indicated inition of outcome
cated CIN1a untreated CIN1 by cytology and/or
colposcopy) and 6
mo
HPV- Non-type-specific inci- Cervicovaginal lavage PCR MY09/MY11 and 3 y (every 6 mo, Me follow-up time
dent HPV infection at each visit HMB01, Southern range: 3–24)b 2.2 y, max 3.4 y, md
blot hybridization # of visits 5 b
(16 HR þ 22 LR
genotypes)
Normal cytology and Incident LSIL on cytol- Cytology and colpos- Not relevant for def- NR (every 4 mo if Md # of visits 10 (IQR:
HPV- on a PCR ogy after prior HPV copy;c at baseline inition of outcome HPVþ, or 6 mo if 5–16), md follow-up
assay at baseline and infection and interval visits HPV-) time 56 (IQR: 27–
first follow-up, 82); those with <3
HPVþ at baseline visits had fewer sex
on the HPV Profile partners at baseline
assay and lower SES than
women with 53
visits and 51
HPV þ result
Colposcopically con- Colposcopic regres- CIN regression: PCR GP5 þ /6 þ EIA NR (at 3, 6, and 12 Intervention arm: md
firmed CIN 1 or sion of CIN (2 con- smears and colpos- (14 HR þ 6 LR months after base- follow-up time
CIN2/3 smaller than secutive normal copy; biopsy only if genotypes) line, and subse- 16.4 mo (range: 3.0–
2 cervical quad- colposcopic diag- suspected CIN pro- quently every 12 85.4); Control
rants; Intervention noses); clearance of gression; colpo- months until CIN group: 12.8 mo
arm: 87% HPVþ at HPV (2 consecutive scopic diagnoses treatment if any) (3.1–63.0)d
baseline, Control negative HPV tests) were adjudicated
arm: 80% HPVþ at from
baselined photographs; HPV
clearance: HPV
testing
HPV- Genotype-specific inci- HPV testing (clinician- PCR PGMY09/MY11, NR (every 4 mo, Me follow-up time:
dent HPV infection, and self-collected) reverse line-blot (19 md ¼ 4.1 mo) 33.9 mo
and incident cervical and cytology at HR þ 18 LR (SD ¼ 11.8), me #
squamous intrae- every visit genotypes) of visits: 8.6
pithelial lesions on (SD ¼ 2.9)
cytologye
(continued)
Journal of Medical Screening 21(1)
 Lam et al.

Table 2. Continued

Baseline cervical status

(HPV or cervical Assessment of HPV assay (# of Planned follow-up
Authors, year of publication lesions) Main study endpoint(s) endpoint detectable genotypes) duration (interval) Loss to follow-up

Shew et al. 200612 HPV þ at baseline or Genotype-specific HPV testing: clinican- PCR/reverse blot strip 27 mo (every 3 mo Me follow-up time:
during follow-upf HPV clearanceg collected every assay with non- at the clinic, and 2.2 y (range: 2.0–
3 mo, self-collected degenerate primers weekly at home for 2.4)
every week for 12 (19 HR þ 8 LR 12 weeks at a time)
weeks at a time genotypes)
Sánchez-Alemán et al. 201111 HPV- Incident HPV infection Self-collected HPV Hybrid Capture 2 (13 NRh Me follow-up duration:
testing HR genotypes) 1.71 y
Munk et al. 201215–17 Histologically con- Histologically con- Colposcopy at the Not relevant for def- 53 visits (second visit No loss to follow-up
firmed CIN2/3 (22% firmed regression of second visit, col- inition of outcome 7–9 weeks after by design
CIN2, 78% CIN3) untreated CIN (95% poscopy þ cone baseline, third visit
HPVþ)i excision at the third 12–24 weeks after
visit; histology was baseline, md 113 d
adjudicated (range: 84–171)
Abbreviations: # ¼ number, CIN ¼ cervical intraepithelial neoplasia, HPV ¼ Human Papillomavirus, HPV-/þ ¼ HPV negative/positive, HR ¼ high-risk genotypes (classification of high-risk genotypes as defined by authors
of studies), HSIL ¼ high-grade squamous intraepithelial lesions, IQR ¼ interquartile range, LR ¼ low-risk genotypes (classification of low-risk genotypes as defined by authors of studies), LSIL ¼ low-grade squamous
intraepithelial lesions, max ¼ maximum, md ¼ median, me ¼ mean, mo ¼ month(s), NR ¼ not reported, PCR ¼ polymerase chain reaction, SES ¼ socioeconomic status, STI ¼ sexually transmitted infections, y ¼ year(s).
a
34 out of 42 (81%) patients in whom the distribution of HPV on initial colposcopy was fully charted had vulval and/or vaginal involvement.
b
Whole sample of 608 recruited women, among whom 26% were HPVþ.
c
Majority of women with LSIL also underwent biopsy to rule out HSIL.
d
For all 125 randomized women.
e
Events detected during visits at which no instances of vaginal intercourse were recorded during the previous 8 months were excluded.
f
HPV infection defined as 52 positive specimens for a specific HPV genotype.
g
Defined as 52 negative specimens for the genotype before end of follow-up.
h
The interval was not clearly specified. Women were recruited in 2001, 2002 and 2003, and follow-up was carried out during the years 2002, 2003 and 2005.
i
Defined as 4CIN1 in the subsequent cone. HPV testing based on formalin fixed paraffin embedded cervical biopsies, using the Linear Array assay (37 HR þ LR genotypes) on all samples, and the AMPLICOR assay (13
HR genotypes) on samples negative on Linear Array.
43

Table 3. Summary of study outcomes.
Study endpoint
Regression of untreated his-
tologically-confirmed CIN
Incident HPV infection
Incident LSIL
Regression of untreated col-
poscopically confirmed
CIN
Clearance of HPV infection
Incident HPV infection
Condom use: exposure vs. refer-
ence group (n of women in ana-
Authors, year of lysis, or by condom use if
publication reported)
10
Thomas et al. 1990 54% condom use in all sex acts,
38% some use, 8% no coitus
(n ¼ 26) vs. 95% non-use, 5%
some use (n ¼ 20)
Ho et al. 199814 Always vs. never use (n ¼ 399)
Moscicki et al. 200113 Always vs. less than always
(n ¼ 496)
Hogewoning et al. 20038 Intervention arm (n ¼ 50) vs.
control arm (n ¼ 48)c
Hogewoning et al. 20038 Intervention arm (n ¼ 48) vs.
control arm (n ¼ 36)d
Winer et al. 20069 <5% (36.9 wy) vs. 5–49% (31.3
wy) vs. 50–99% (43.4 wy) vs.
100% (31.7 wy) use (n ¼ 82)
44
Conclusion regarding
effectiveness of condoms
Estimate of the relative in preventing cervical
risk (95% CI) Adjustments dysplasia
[RR ¼ 0.77 (95% CI: 0.47– None Not significantly protective
1.27)a]
RR ¼ 0.8 (95% CI: 0.4–1.4)b Age, race, alcohol consumption, Not significantly protective
# of sex partners in prior 6
and 7–12 mo, anal sex, fre-
quency of vaginal sex, male
partner’s # of lifetime part-
ners, main partner currently
in school, income, lifestyle,
smoking, recreational drugs,
oral contraceptives, # of
casual sex partners, frequency
of oral sex, sex with alcohol
or drugs, postcoital bleeding,
sex during menstruation,
douchingb
HR ¼ 0.82 (95% CI: 0.48– None Not significantly protective
1.41)
HR ¼ 3.1 (95% CI: 1.4-7.1) HPV status at baseline, histologic Significantly protective
CIN grade at baseline, age at
baseline
HR ¼ 12.1 (95% CI: 1.5–97.2) HPV status at baseline, histologic Significantly protective
CIN grade at baseline, age at
baseline
All genotypes 5–49% vs. # of new sex partners, # of pre- Significantly protective
<5%: HR ¼ 1.0 (95% CI: vious partners of sex partner
0.5–1.8) 50–99%
vs. < 5%: HR ¼ 0.5 (95%
CI: 0.3–0.9) 100% vs.
<5%: HR ¼ 0.3 (95% CI:
0.1–0.6) High-risk geno-
types: 5–49% vs. <5%:
HR ¼ 1.0 (95% CI:
NR) 50–99% vs. <5%:
HR ¼ 0.3 (95% CI:
NR) 100% vs. <5%:
HR ¼ 0.3 (95% CI:
NR) Low-risk geno-
types: 5–49% vs. <5%:
HR ¼ 1.0 (95% CI:
NR) 50–99% vs. <5%:
Journal of Medical Screening 21(1)
(continued)
Table 3. Continued
Condom use: exposure vs. refer- Conclusion regarding
ence group (n of women in ana- effectiveness of condoms
Lam et al.

Authors, year of lysis, or by condom use if Estimate of the relative in preventing cervical
Study endpoint publication reported) risk (95% CI) Adjustments dysplasia

HR ¼ 0.8 (95% CI:

Incident cervical squamous
intraepithelial lesions
Clearance of HPV infection
Incident HPV infection
Regression of untreated CIN
Winer et al. 20069
Shew et al. 200612
Sánchez-Alemán et al. 201111
Munk et al. 201215
<5% (37.0 wy) vs. 5–49% (24.8
wy) vs. 50–99% (35.0 wy) vs.
100% (32.1 wy) use (n ¼ 82)
<60% use vs. >60% use (n ¼ 49)
Inconsistent (321.9 wy) vs. con-
sistent use (73.8 wy) (n ¼ 237)
Consistent (n ¼ 18) vs. incon-
sistent or non-use of con-
doms (n ¼ 144)
NR) 100% vs. <5%:
HR ¼ 0.3 (95% CI: NR)
All genotypes 5–49% vs. # of new sex partners, # of pre- Not significantly protective
<5%: HR ¼ 0.5 (95% CI: vious partners of sex partner
0.1–3.2) 50–99% vs. (in 8 months before HPV
<5%: HR ¼ 0.9 (95% CI: testing)
0.2–3.6) 100% vs. <5%:
HR ¼ 0.0 (95% CI: 0–1.8)
HR ¼ 0.58 (95% CI: 0.35– # of partners during an HPV Significantly protective
0.97)e infection, # of coital events
during an HPV infection,
oncogenic HPV type, C tra-
chomatis / T vaginalis
coinfection
Inconsistent, 1 partner vs. Current tobacco consumption, Not significantly protective
consistent, 1 partner: marijuana use, self-reported
HR ¼ 2.1 (95% CI: 0.8– STI, emergency contraceptive
5.3) Consistent, 52 pill
partners vs. consistent, 1
partner: HR ¼ 4.8 (95%
CI: 0.5–
42.9) Inconsistent, 52
partners vs. consistent, 1
partner: HR ¼ 3.8 (95%
CI: 1.4–10.2)f
OR ¼ 5.28 (95% CI: 1.68– pRb, CIN length, CD4þ stroma Significantly protective
16.62)

Abbreviations: RR ¼ relative risk, HR ¼ hazard ratio, ¼ number, wy ¼ woman-years at risk, STI ¼ sexually transmitted infections, OR ¼ odds ratio.
a
Calculated as 0.70 (95% CI: 0.38–1.31) for comparing histologically confirmed regression in women with 100% use of condoms or no coitus (n ¼ 16) vs. women with non-use of condoms (n ¼ 19).
b
The use of condoms during vaginal sex was reported by authors as not significant in multivariate time-dependent proportional-hazards analysis; however, no RR estimate was shown. The RR estimate shown in this
table was reported by Manhart and Koutsky after obtaining additional data from the investigators.5
c
Of the 125 randomized women, 17 were excluded due to lack of follow-up data after they showed a normal colposcopy once.
d
Of the 125 randomized women, 34 were excluded because they were HPV- at baseline, had cervical scrapes that were inadequate for HPV testing at baseline and/or during follow-up, or there was no available follow-
up data on HPV after they were HPV- once. From the remaining 91 women, HR was based on 84 women.
e
Limited to periods during which sexual intercourse occurred.
f
Number of sexual partners during the past year.
45
46
genotyped with a reverse line-blot assay. Every two weeks,
these women were asked to complete web-based diaries
(91% complete) detailing sexual acts including condom
use. Consistent users during eight months before HPV
testing had a substantially lower risk of acquiring HPV
compared with women using condoms in <5% of sexual
acts, Hazards ratio (HR) ¼ 0.3 (95% CI: 0.1–0.6).
Frequent but inconsistent condom use, defined as use in
50–99% of sexual acts, was also associated with a lower
frequency of incident HPV infections, HR ¼ 0.5 (95% CI:
0.3–0.9). Infrequent users (5–49% of sexual acts) had the
same risk of HPV infections as women using condoms
<5% of the time, HR ¼ 1.0 (95% CI: 0.5–1.8). All esti-
mates were adjusted for indicators of sexual behaviour,
including the partners’ risk level. No consistent user had
incident squamous intraepithelial lesions on cytology, but
the numbers were too small to reach statistical
significance.
In the study by Shew et al.12 49 adolescents were asked
every three months to keep daily diaries on sexual activity,
including condom use. Every week the girls obtained an
HPV self-sample (HPV evaluation was undertaken using
PCR/reverse blot strip assay), and every three months
they underwent sampling performed by a clinician.
Adjusted for indicators of sexual behaviour, HPV infec-
tions cleared faster in girls who used condoms in >60% of
sexual acts (sample median) compared with those
who used condoms less frequently, HR ¼ 0.6 (95% CI:
0.4–1.00).
In a study by Sánchez-Alemán et al.11 237 women
appeared to have been tested for HPV yearly, and their
use of condoms was assessed over their lifetime. Samples
were analyzed using the high-risk probe on the Hybrid
Capture 2 assay. The risk of HPV infections increased
with the number of sexual partners, and the use of con-
doms was not significantly protective when adjusting for
this number, HR ¼ 1.9 (95% CI: 0.8–4.4). Among women
with one sexual partner, inconsistent users had a higher
risk of HPV infections, but not significantly so, HR ¼ 2.1
(95% CI: 0.8–5.3). No protective effect was found among
women with two or more sexual partners, with similar
relative risks for consistent and inconsistent condom use,
HR ¼ 4.8 (95% CI: 0.5–42.9) and HR ¼ 3.8 (95% CI: 1.4–
10.2), respectively. The estimates were adjusted for several
lifestyle indicators.
Condom use and CIN lesions
Thomas et al.10 followed 46 women with untreated CIN1,
and asked them either to consistently use condoms in the
next six months (intervention group), or to avoid using
condoms (control group). Women were assessed by cytol-
ogy and colposcopy at three and six months, when com-
pliance with condom use was also assessed in an interview.
In the intervention group, only 54% of women used con-
doms consistently, while 38% reported some use.
Histologically-confirmed CIN regression was not statistic-
ally significantly more frequent in the intervention than
Journal of Medical Screening 21(1)
in the control group, [unadjusted RR ¼ 0.8 (95% CI:
0.5–1.3)].
Moscicki et al.13 followed 496 women aged 13–20 in
intervals of 4–6 months. Women were initially free of
cytological abnormalities but tested positive for HPV at
least once during the follow-up. Condom use was assessed
at all visits. Consistent users had an unadjusted HR ¼ 0.8
(95% CI: 0.5–1.4) of developing cytologically-confirmed
low-grade squamous intraepithelial lesions compared with
women who did not always use condoms. Women were
selected into the study if they tested positive on the HPV
Profile assay, but (twice) negative on a PCR HPV assay.
Hence, we did not consider the reported results for inci-
dent HPV infections representative, as some of the infec-
tions considered incident on a PCR assay may have
actually been persistent infections, originally detected by
the HPV Profile assay.
In a randomized clinical trial by Hogewoning et al.8
125 women with a colposcopic impression of CIN1 or
CIN2/3 not stretching over more than one cervical quad-
rant and not using condoms for contraception were either
recommended to use condoms for at least three months
(intervention arm), or were not recommended to use con-
doms (control arm). Compliance with condom use was
further stimulated by provision of free Durex fetherlite
condoms. Women were assessed colposcopically at three
and six months, and thereafter every six months.
Consistency of condom use was verified verbally at each
visit. Compliance in the intervention arm was high, with
seven out of 64 women reporting on average two failures
in condom use throughout the whole study. Actual use of
condoms in the control group was not reported. After two
years, the intervention group had a higher rate of regres-
sion of colposcopically-determined CIN than the control
group, HR ¼ 3.1 (95% CI: 1.4–7.1), and also more fre-
quently cleared the baseline HPV infection, HR ¼ 12.1
(95% CI: 1.5–97.2; tested using the PCR GP5 þ /
6 þ assay). All estimates were adjusted for HPV status,
CIN grade, and age at baseline.
At baseline, Munk et al.15-17 asked 162 women with
histologically-confirmed CIN2/3 to continue using their
usual form of contraception, and to return for colposcopy
two months, and again about three to six months after the
baseline. Condom use was determined from interviews at
baseline and final visits. Consistent condom use was asso-
ciated with significantly more frequent regression of
CIN2/3 compared with inconsistent use or non-use,
odds ratio (OR) ¼ 5.3 (95% CI: 1.7–16.6), adjusted for
clinical variables. In inconsistent users, CIN2/3 regressed
as frequently (13%) as in non-users (17%), p ¼ 0.9.
However, the protective effect of consistent use was only
seen in women who, at baseline, were not infected with
HPV16.
Discussion
Four out of eight longitudinal studies showed a statistic-
ally significant protective effect of condoms in prevention
Lam et al.
of HPV infections and cervical neoplasia. This means that
consistent users had: a significantly lower risk of becoming
infected with HPV, a higher chance to clear the existing
infections, or a higher chance of high-grade CIN regres-
sion without surgical intervention. In the remaining four
studies, a protective effect was also observed for these
outcomes, although it was not statistically significant.
This is a substantially more positive message compared
with that from an earlier systematic review including
predominantly cross-sectional studies.5
Nevertheless, there are several reasons to suggest
that the effectiveness of condoms may be underestimated,
even in these longitudinal studies. As in vitro studies
showed that condoms are a nearly impermeable barrier
for transmission of small viruses like HPV,18 why is it
that the observed protective effect is not higher in
in vivo studies? Several design weaknesses of the currently
available studies, discussed below, may have contributed
to this.
HPV can be transmitted by skin contact,19;20 and is
found in male genital areas not covered by a condom.21
Furthermore, errors and problems such as breakage, slip-
page, or late application are also common.22 Hence, infec-
tion pathways and incorrect use, that are unaccounted for
in studies, make condoms appear less protective against
HPV infections.23 In the study by Winer et al, the associ-
ation between HPV infections and condom use was not
changed after accounting for correctness of use in consist-
ent users.9 Other studies did not verify that condoms were
used correctly.
The risk of acquiring HPV is strongly related to the
number of sexual partners.11,12,14,24,25 Condom use
appears to be higher among casual and new sexual part-
ners than among regular ones.5,26-29 Hence, exposure to
infections is often imbalanced between condom users and
non-users, and would need to be accounted for in the
analyses. Although several studies attempted to control
this by, for example, adjusting for the number of sexual
partners, or history of STI, some residual confounding is
likely to have remained.26 Differences in host characteris-
tics between condom users and non-users, eg. their
immunological status, which could explain the variation
in HPV clearance rates, were not studied.
Cultural norms play an important role in how truth-
fully sensitive information is disclosed to researchers. As
use of condoms is socially desirable, it might be reported
more frequently than justified by reality,30,31 thereby dilut-
ing the observed protective effect of condoms. Other rea-
sons for misclassification of condom use have been
discussed in the literature. For example, long recall peri-
ods may be associated with more frequently inaccurate
reporting of use.23,30,32,33 Correct recall may be a particu-
lar challenge for women who frequently engage in sexual
acts,32 which is in itself a risk factor for acquiring an HPV
infection. It has been argued that validity of self-reports
increases when questionnaires or electronic diaries are
used, instead of face-to-face interviews,31,34 but the latter
were still frequently used in the reviewed studies.
47
It should also be noted that the life-time protective
effect of condoms is smaller than that observed in epi-
demiological studies. Even per sexual act, condoms are
not 100% effective. Therefore, the proportion of women
without an HPV infection will gradually decrease with an
increasing number of sexual acts.18,35 In epidemiological
studies typically covering a relatively short period, only a
certain proportion of life-time infections can be observed.
The length of the reviewed studies varied, however, only
two12,14 adjusted for the frequency of sexual intercourse
during follow-up.
When the outcome of interest is detection of HPV
infections, differences in condom quality and instructions
for use, sampling methods, and the utilized HPV assays
should be taken into account. Only one study8 reported
which brand of condoms was distributed to women to
increase compliance. Sampling methods varied across stu-
dies. For example, Ho et al. used a lavage sample.14
Lavage sampling returns varying volumes for HPV test-
ing, and this variability might affect the HPV positivity
rate. Sampling for HPV has developed tremendously since
that study was undertaken; contemporary utensils and
media secure a more uniform result for the subsequent
HPV analysis. Finally, the time span between the publica-
tions in this systematic review (1990–2012), also highlights
the technical progress in HPV detection technologies.
Whereas earliest studies detected HPV using PCR and
southern blotting methods, later studies used MY09/11
or GP5 þ /6 þ consensus primers with line blot detection,
and, finally, the FDA-approved Hybrid Capture 2 assay.
If these studies were redone today, modern HPV sampling
and testing technologies would probably lead to a higher
degree of reproducibility of study results.
Implications for cervical screening
Substantial proportions of younger cohorts are now vac-
cinated against HPV genotypes 16/18. As demonstrated
by the reviewed studies, the benefit of continuing
condom use could derive either from partial primary pre-
vention of infections9 or from partial prevention of re-
infections.8,12,15 Consistent use of condoms in real life
would be difficult to maintain over the entire sexually
active life. However, the frequency of regular condom
use could be increased by innovations that would make
the condom less cumbersome,36 whereas their effectiveness
could perhaps be improved by increasing awareness about
correct use.
For decades, cervical cancer has been successfully con-
trolled by cytology-based cervical screening.37 Because
HPV testing is more sensitive in detecting high-grade
CIN and preventing cervical cancers,38 many countries
are now considering replacing cytology with HPV testing.
However, one of the main concerns with HPV-based
screening is a high number of infected women with no
underlying high-grade CIN or cervical cancer (false-
positive tests), even among those aged 530 years.39
Although the hypothesis has not been formally studied,
48
what the data from the reviewed longitudinal studies seem
to suggest is that (a more consistent) use of condoms
might potentially reduce the number of women with
(false-)positive primary screening HPV tests who would
need further clinical management.
There are other implications of the reviewed condom
studies that are relevant in cervical screening. Firstly,
treatment of CIN is sometimes associated with pain,
bleeding, and possibly a higher frequency of severe obstet-
ric outcomes.40 Studies in women with CIN lesions
included in this review showed that condoms could be
used to prevent unnecessary surgical CIN treatments. In
those studies, the beneficial effect was already seen after
relatively short periods of consistent use. However, it
remains to be determined whether this effect can be main-
tained over a longer period. In the context of the generally
short study durations, a reason for cautiousness is that
the tissue prone to infections and cancerous growths
is removed by CIN treatment; when lesions regress spon-
taneously as a consequence of condom use, this tis-
sue remains intact and susceptible to new disease
processes.
Secondly, condom users appeared to clear HPV infec-
tions faster than non-users, possibly by reducing continu-
ous transmission of the virus between sexual partners.12 In
HPV-based cervical screening, many women are expected
to test HPV-positive without having cervical abnormal-
ities.41 As these women have a substantial risk of future
high-grade CIN, they will be referred for colposcopy if
their infections persist. The persistence of these infections,
and with it the need for colposcopy referral, could perhaps
be reduced if women used condoms consistently through-
out the waiting period. Finally, another possible indica-
tion for recommending consistent and correct condom use
could be in women after surgical treatment of CIN.
Women with untreated CIN3 have a 30% chance of
developing cervical cancer in 30 years,42 but with treat-
ment this risk decreases by approximately 95%.43
Nevertheless, women treated for CIN continue having a
higher incidence of cervical cancer than the general popu-
lation3, possibly because of a higher frequency of new or
repeated HPV infections. These two indications for use of
condoms in supplementing the effect of cervical screening
have not yet been formally studied.
Conclusion
Consistent use of condoms appears to offer relatively
good, though partial, protection from HPV infections
and associated cervical diseases, although many aspects
of this protection remain to be elucidated. Even in longi-
tudinal studies, the protective effect of correct condom use
is probably underestimated. Carefully undertaken pro-
spective cohort studies or randomized controlled trials
are warranted to further determine the potential role
of condoms in prevention of HPV infections and related
cervical lesions.
Journal of Medical Screening 21(1)
Declaration of conflicting interests
JUHL, PAD, and MEC declare no competing interests.
MR, JB and EL are currently undertaking a compara-
tive study of four HPV assays, involving collaboration
with the following assay manufacturers: Qiagen, Roche,
Genomica, and Hologic/Gen-Probe.
MR and her employer received honoraria from Qiagen
for lectures.
JB has served as a paid advisor to Roche Molecular
Systems and Genomica, and received honoraria from
Hologic/Gen-Probe, Roche, Qiagen, Genomica, and BD
Diagnostics for lectures. He has received funding and/
or consumables to carry out assay evaluations from
Hologic/Gen-Probe, Genomica, Qiagen, Roche, and BD
Diagnostics.
EL served as an unpaid advisor to Hologic/Gen-Probe
and Norchip.
None of the authors was compensated for their work
on this project, holds stock, or received bonuses from any
of the manufacturers.
Financial disclosure
This work was supported by the Danish Strategic
Research Council [grant number: 10–092793 to MR] and
the University of Copenhagen [to PAD].
None of the funders had a role in the study design, in
the collection, analysis, and interpretation of the data, in
the writing of the report, and in the decision to submit the
article for publication. The researchers worked independ-
ently of the funders.
Previous presentations
This work was presented as an oral communication at
Eurogin 2013, 3–6 November 2013, Florence, Italy
(abstract number: OC11–1).
Funding
This research received no specific grant from any
funding agency in the public, commercial, or not-for-profit
sectors.
Acknowledgments
The authors thank Lene Borrits (Royal Danish Library) for help
with the search strategy, and Bryan Howard Goldman
(Department of Public Health, University of Copenhagen) for
statistical help.
References
1. Walboomers JM, Jacobs MV, Manos MM, et al. Human
papillomavirus is a necessary cause of invasive cervical
cancer worldwide. J Pathol 1999;189(1): 12–19.
2. Bouvard V, Baan R, Straif K, et al. A review of human car-
cinogens–Part B: biological agents. Lancet Oncol 2009;10(4):
321–322.
Lam et al.
3. Rebolj M, Helmerhorst T, Habbema D, et al. Risk of cer-
vical cancer after completed post-treatment follow-up of cer-
vical intraepithelial neoplasia: population based cohort
study. BMJ 2012;345:e6855.
4. Spence AR, Goggin P, Franco EL. Process of care failures in
invasive cervical cancer: systematic review and meta-analy-
sis. Prev Med 2007;45(2–3): 93–106.
5. Manhart LE, Koutsky LA. Do condoms prevent genital
HPV infection, external genital warts, or cervical neoplasia?
A meta-analysis. Sex Transm Dis 2002;29(11): 725–735.
6. CDC. Report to Congress: Prevention of Genital Human
Papillomavirus Infection. URL: http://www.cdc.gov/std/
HPV/2004HPV%20Report.pdf. Last accessed: 29 June 2013.
7. Morris K. FDA plans warning labels for condoms. Lancet
Infect Dis 2004;4(5): 257.
8. Hogewoning CJ, Bleeker MC, van den Brule AJ, et al.
Condom use promotes regression of cervical intraepithelial
neoplasia and clearance of human papillomavirus: a rando-
mized clinical trial. Int J Cancer 2003;107(5): 811–816.
9. Winer RL, Hughes JP, Feng Q, et al. Condom use and the
risk of genital human papillomavirus infection in young
women. N Engl J Med 2006;354(25): 2645–2654.
10. Thomas I, Wright G, Ward B. The effect of condom use on
cervical intraepithelial neoplasia grade I (CIN I). Aust N Z J
Obstet Gynaecol 1990;30(3): 236–239.
11. Sanchez-Aleman MA, Uribe-Salas FJ, Lazcano-Ponce EC,
Conde-Glez CJ. Human papillomavirus incidence and risk
factors among Mexican female college students. Sex Transm
Dis 2011;38(4): 275–278.
12. Shew ML, Fortenberry JD, Tu W, et al. Association of
condom use, sexual behaviors, and sexually transmitted
infections with the duration of genital human papilloma-
virus infection among adolescent women. Arch Pediatr
Adolesc Med 2006;160(2): 151–156.
13. Moscicki AB, Hills N, Shiboski S, et al. Risks for incident
human papillomavirus infection and low-grade squamous
intraepithelial lesion development in young females. JAMA
2001;285(23): 2995–3002.
14. Ho GY, Bierman R, Beardsley L, Chang CJ, Burk RD.
Natural history of cervicovaginal papillomavirus infection
in young women. N Engl J Med 1998;338(7): 423–428.
15. Munk AC, Gudlaugsson E, Ovestad IT, et al. Interaction of
epithelial biomarkers, local immune response and condom
use in cervical intraepithelial neoplasia 2–3 regression.
Gynecol Oncol 2012;127(3): 489–494.
16. Munk AC, Gudlaugsson E, Malpica A, et al. Consistent
condom use increases the regression rate of cervical intrae-
pithelial neoplasia 2–3. PLoS One 2012;7(9): e45114.
17. Munk AC, Ovestad IT, Gudlaugsson E, et al. Consistent
condom use increases spontaneous regression in high-risk
non-HPV16 but not in HPV16 CIN2–3 lesions, a prospect-
ive population-based cohort study. Infect Agent Cancer
2012;7(1): 30.
18. Lytle CD, Routson LB, Seaborn GB, Dixon LG, Bushar
HF, Cyr WH. An in vitro evaluation of condoms as barriers
to a small virus. Sex Transm Dis 1997;24(3): 161–164.
19. Frega A, Cenci M, Stentella P, et al. Human papillomavirus
in virgins and behaviour at risk. Cancer Lett 2003;194(1):
21–24.
20. Winer RL, Lee SK, Hughes JP, Adam DE, Kiviat NB,
Koutsky LA. Genital human papillomavirus infection: inci-
dence and risk factors in a cohort of female university stu-
dents. Am J Epidemiol 2003;157(3): 218–226.
49
21. Poljak M, Kocjan BJ, Potočnik M, Seme K. Anogenital
hairs are an important reservoir of alpha-papillomaviruses
in patients with genital warts. J Infect Dis 2009;199(9):
1270–1274.
22. Sanders SA, Yarber WL, Kaufman EL, Crosby RA,
Graham CA, Milhausen RR. Condom use errors and prob-
lems: a global view. Sex Health 2012;9(1): 81–95.
23. Crosby R, DiClemente RJ, Holtgrave DR, Wingood GM.
Design, measurement, and analytical considerations for
testing hypotheses relative to condom effectiveness
against non-viral STIs. Sex Transm Infect 2002;78(4):
228–231.
24. Ho L, Terry G, Londesborough P, Cuzick J, Lorenzato F,
Singer A. Human papillomavirus DNA detection in the
management of women with twice mildly abnormal cyto-
logical smears. J Med Virol 2003;69(1): 118–121.
25. Nielsen A, Iftner T, Munk C, Kjaer SK. Acquisition of high-
risk human papillomavirus infection in a population-based
cohort of Danish women. Sex Transm Dis 2009;36(10):
609–615.
26. Warner L, Newman DR, Austin HD, et al. Condom effect-
iveness for reducing transmission of gonorrhea and chla-
mydia: the importance of assessing partner infection
status. Am J Epidemiol 2004;159(3): 242–251.
27. Peterman TA, Lin LS, Newman DR, et al. Does measured
behavior reflect STD risk? An analysis of data from a ran-
domized controlled behavioral intervention study. Project
RESPECT Study Group. Sex Transm Dis 2000;27(8):
446–451.
28. Crosby R, Bounse S. Condom effectiveness: where are we
now? Sex Health 2012;9(1): 10–17.
29. Macaluso M, Demand MJ, Artz LM, Hook III EW. Partner
type and condom use. AIDS 2000;14(5): 537–546.
30. McCallum EB, Peterson ZD. Investigating the impact of
inquiry mode on self-reported sexual behavior: theoretical
considerations and review of the literature. J Sex Res
2012;49(2–3): 212–226.
31. Fenton KA, Johnson AM, McManus S, Erens B. Measuring
sexual behaviour: methodological challenges in survey
research. Sex Transm Infect 2001;77(2): 84–92.
32. Schroder KE, Carey MP, Vanable PA. Methodological chal-
lenges in research on sexual risk behavior: II. Accuracy of
self-reports. Ann Behav Med 2003;26(2): 104–123.
33. Noar SM, Cole C, Carlyle K. Condom use measurement in
56 studies of sexual risk behavior: review and recommenda-
tions. Arch Sex Behav 2006;35(3): 327–345.
34. Baer A, Saroiu S, Koutsky LA. Obtaining sensitive data
through the Web: an example of design and methods.
Epidemiology 2002;13(6): 640–645.
35. Wilson DP. Interpreting sexually transmissible infection pre-
vention trials by adjusting for the magnitude of exposure.
Clin Trials 2010;7(1): 36–43.
36. Grand Challenges in Global Health. Develop the Next
Generation of Condom. URL: http://www.grandchallenges.
org/Explorations/Topics/Pages/NextGenerationCondom
Round11.aspx. Last accessed: 7 July 2013.
37. IARC. IARC Handbooks of Cancer Prevention, Vol. 10:
Cervix cancer screening. International Agency for
Research on cancer Press: Lyon, 2005.
38. Ronco G, Dillner J, Elfström KM, et al. Efficacy of HPV-
based screening for prevention of invasive cervical cancer:
follow-up of four European randomised controlled trials.
Lancet 2013 (Epub ahead of print).
50
39. Rebolj M, Njor SH, Lynge E. Restriction of human papil-
lomavirus DNA testing in primary cervical screening to
women above age 30: systematic review. Eur J Cancer Prev
2012;21(1): 73–81.
40. Arbyn M, Kyrgiou M, Simoens C, et al. Perinatal mortality
and other severe adverse pregnancy outcomes associated
with treatment of cervical intraepithelial neoplasia: meta-
analysis. BMJ 2008;337:a1284.
41. Preisler S, Rebolj M, Untermann A, et al. Prevalence of
human papillomavirus in 5,072 consecutive cervical
SurePath samples evaluated with the Roche cobas HPV
real-time PCR assay. PLoS One 2013;8(3): e59765.
42. McCredie MR, Sharples KJ, Paul C, et al. Natural history of
cervical neoplasia and risk of invasive cancer in women with
cervical intraepithelial neoplasia 3: a retrospective cohort
study. Lancet Oncol 2008;9(5): 425–434.
43. Soutter WP, de Barros LA, Fletcher A, et al. Invasive cer-
vical cancer after conservative therapy for cervical intrae-
pithelial neoplasia. Lancet 1997;349(9057): 978–980.
Journal of Medical Screening 21(1)
Appendix
The following search was undertaken in PubMed in May
2013:
[((((‘‘humans’’[MeSH Terms] OR ‘‘humans’’[All Fields]
OR ‘‘human’’[All Fields]) AND (‘‘papillomaviridae’’
[MeSH Terms] OR ‘‘papillomaviridae’’[All Fields] OR
‘‘papillomavirus’’[All Fields])) OR ‘‘Papillomaviridae
’’[MeSH] OR ‘‘Papillomavirus Infections’’
[MeSH:noexp])) OR (HPV OR human papillomavirus)
OR (‘‘cervical intraepithelial neoplasia’’[MeSH Terms]
OR (‘‘cervical intraepithelial neoplasia’’[All Fields] AND
prevention) OR ‘‘uterine cervical neoplasms’’[MeSH
Terms] OR ((‘‘uterine cervical neoplasms’’[All Fields]
OR (‘‘cervical’’[All Fields] AND ‘‘cancer’’[All Fields]))
AND prevention))] AND [condoms[MeSH Terms] OR
condoms OR condom]