Vol.2, No.9, 1027-1032 (2010) Health
Copyright © 2010 SciRes. Openly accessible at http://www.scirp.org/journal/HEALTH/
Cervical cancer screening program based on HPV
testing and conventional Papanicolaou cytology
for jail inmates
Vincenza Fabiano1, Luciano Mariani2, Maria Rosaria Giovagnoli1, Salvatore Raffa1, Cristina
Vincenzoni2, Fausto de Michetti3, Francesco Bevere4, Deborah French1*
1Department Clinical and Molecular Medicine, “Sapienza” University of Rome, S. Andrea Hospital, Rome, Italy;
*Corresponding Author: deborah.french@uniroma1.it
2Department of Gynaecology, Regina Elena National Cancer Institute of Rome, Rome, Italy
3Medical Service, Female Jail “Rebibbia” of Rome, Rome, Italy
4General Direction, Regina Elena National Cancer Institute of Rome, Rome, Italy
Received 7 May 2010; revised 17 June 2010; accepted 20 June 2010.
Background: To assess the validity of Human
Papillomavirus (HPV) testing in a group of
women at high risk for developing cervical
cancer, a screening intervention was applied
to a population of jail inmates in Rome, Italy.
This cross-sectional study provided also new
insights on the risk factors and on the HPV
genotype distribution. Methods: We have in-
vited 350 inmates to the preliminary stage of
the screening program and 98 inmates de-
cided to participate to the study and filled out
a questionnaire for the history of attendance
to previous cervical screening and for the
known risk factors for cervical malignancies.
HPV DNA test, conventional Pap smear and
HPV genotyping were performed. Results: The
percentage of women with High Risk (HR) HPV
positivity were 19.3%. The inmates with LSIL/
HSIL status showed a significantly higher pre-
valence of HR-HPV positivity (100% vs. 16.3%;
p < 0.001) and of multiple HPV types (60% vs.
1.2%; p < 0.001) compared to women with
normal/ASCUS Pap smear. HPV16 was the
predominant genotype in either single or mul-
tiple infections. Conclusions: The results in-
dicated that HPV DNA-based approach is a
strategy useful for incarcerated women which do
not have the opportunity or the social and cul-
tural environment to receive preventive care.
Keywords: Cervical Cancer Screening; HPV;
During the last few years, cervical cancer screening pro-
grams for women in prison have been carried out in the
United States and in Canada [1-5]. Although the results
of such preventive care interventions are still not com-
plete and require further work and follow-up, these
studies have pointed out the interesting profile of a jail
inmate population as an high risk group for developing
cervical malignancies. In fact, several socio-demo-
graphic risk factors including race/ethnicity, lower level
of education and drug or alcohol abuse are responsible
for the higher incidence rates of cancer in prisoner
women [6,7].
Human papillomaviruses (HPVs) of the high risk types
are known to play a causative role in cervical cancero-
genesis [2]. HPV infection is correlated primarily with the
number of sex partners, but is positively associated also
with smoking and oral contraceptive use [8-10].
A number of randomized controlled trials have recently
shown that HPV testing for cervical cancer screening
shows a higher sensitivity compared with the conven-
tional Papanicolaou cytology [11-13].
These studies have indicated that the prevalence of
HPV infection in the general population is strictly re-
lated to the age of the women attending the screening
[14], with a peak incidence of HPV infection occurring
at the age of 16-20, as well as to their socioeconomic
status [6].
With the aim to contribute to the assessment of the va-
lidity of the HPV DNA testing for cervical cancer
screening and to increase the knowledge of the role of
the risk factors and on the distribution of the HPV types,
we have conducted a preventive care program by parallel
HPV DNA test and conventional cytology on a popula-
V. Fabiano et al. / HEALTH 2 (2010) 1027-1032
Copyright © 2010 SciRes. Openly accessible at http://www.scirp.org/journal/HEALTH/
tion of women prisoners in the “Rebibbia” Female Jail
of Rome.
This cross-sectional study was approved by the Second
Faculty of Medicine of “Sapienza” University of Rome,
by the Regina Elena National Cancer Institute of Rome
and by the “Rebibbia” Female Jail of Rome. The proto-
col was designated following the recommended guide-
lines of the following italian scientific societies: SICPCV
(Italian Society of Colposcopy and Cervico-Vaginal Pa-
thology) and GISCI (Italian Group of Cervical Cancer
Screening), adapted in accordance with the experimental
arm of the New Technologies for Cervical Cancer
(NTCC) [12].
2.1. Procedure and Questionnaire
In the preliminary stage of our study, to invite the in-
mates to participate to the screening program we first
organised three sequential meetings in the prison theatre
in order to describe the value of cervical cancer screen-
ing, the role of the HPV infection and the routes of viral
transmission. To explain the aims of the program and the
procedure of the gynecological control we used slides
with cartoons and figures to favour the comprehension
from a multi ethnical population.
98 out of 350 inmate women decided to participate
to the study and filled out a questionnaire by them-
selves. The questionnaire was written in italian and
was translated into English and Spanish. The questions
included those required for the history of attendance to
previous cervical screening as well as the willingness
to be screened in the prison setting and those for the
known risk factors for cervical malignancies such as
smoke, drug/alcohol and sexual behaviour (Table 1).
Written informed consent was obtained from all par-
2.2. Specimen Collection
The women then underwent a gynecological examina-
tion including three different cervical samples: 1) a sam-
ple of cervical cells taken by Cervical sampler, (Digene
Corporation, Gaitesburg, MD) and collect in standard
transport medium for HPV DNA test; 2) an eso-endo-
cervical scraping for conventional Pap Test; 3) a sample
of cervical cells taken by Ayre’s Spatula and Cytobrush
(Cytobrush DOC, Gardening, Genova, Italy) and collect
in Transport buffer for HPV DNA genotyping.
2.3. HPV Detection
HPV DNA test was performed by Hybrid Capture II
hybridization assay (HC2 Digene Corporation, Gaith-
Table 1. Questions for the inmates enrolled into the screening
Patient Code
Race/ethnicity (White, Latino/Hispanic, African, other)
Marital Status (Unmarried without current male partner, unmarried
with current male partner, married, widowed, separed-divorced)
How many sexual partners did you have in your life?
Which was the age of your first sexual intercourse?
Did you never practice oral sex?
Did you never practice anal sex?
Do you smoke? If yes, how many cigarettes/day?
Do you drink? If yes, how much?
Do you use contraceptive methods? If yes, you use condom?
Do you have carried out a PAP smear during the last three years?
ersburg, Maryland USA), according to the manufac-
turer’s instructions. HC2 test, was used with the “high-
risk” probes designed to detect HPV types 16, 18, 31, 33,
35, 39, 45, 51, 52, 56, 58, 59, 68 positivity. A cervical
smear was prepared for conventional Pap test and classi-
fied according to the Bethesda System 2001.
HPV genotyping test was performed using a line
probe assay for all cervical samples which were positive
at the HC2 test. Total DNA was extracted QIAamp®
DNA extraction (Qiagen, Hilden, Germany) and appro-
priate spin columns according to the manufacturer’s
protocol. The INNO-LiPA HPV Genotyping Extra is a
line probe assay designed for the identification of 28
different genotypes of the Human Papillomavirus by
detection of specific sequences in the L1 region of the
HPV genome. INNO-LiPA identified HPV types 6, 11,
16,18, 31, 33, 35, 39, 40, 42, 43, 44, 45, 51, 52, 53, 54,
56, 58, 59, 66, 68, 70, 74 (INNO-LiPA; Innogenetics
Gent, Belgium).
2.4. Cytological and Histological Diagnosis
All the lesions cytologically diagnosed, underwent col-
poscopic evaluation. The high grade lesions were imme-
diately treated, excisional procedures were performed by
a loop electrosurgical excisional procedure (LEEP), or
traditional cone-biopsy, in the day surgery of Regina
Elena National Cancer Institute of Rome. The histologi-
cal diagnosis for all treated cases was CIN III according
with cytology and colposcopic examination.
V. Fabiano et al. / HEALTH 2 (2010) 1027-1032
Copyright © 2010 SciRes. Openly accessible at http://www.scirp.org/journal/HEALTH/
2.5. Statistical Methods
Logistic regression analysis was performed to model the
association between sociodemographic characteristics,
sexual and health behaviours and human papillomavirus
(HPV) status or cervical cytology data. Odds Ratios
(ORs) was calculated for each potential risk factors. Chi
square and Fisher’s exact test was used to compare cate-
gorical variables and a P for trend was calculated for
ordinal categories.
As shown in Table 2, the epidemiological characteristics
of the jail inmates corresponded to those described for a
high risk population to develop cervical cancer. The
sexual behaviour of the inmate group was also at higher
risk because of the increased number of partners and the
earlier sex intercourse. In fact, the logistic regression
analysis showed that the OR for HR-HPV positivity was
significantly associated with lifetime number of sex
partners (OR = 2.00 for 5-9 partners; OR = 13.3 for >10
partners; p = 0.036).
Cervical samples from the 98 inmate participants to
the screening were analyzed by HPV DNA test using the
Hybrid Capture 2 hybridization assay to detect HR-HPV
positivity and by conventional cytology. As shown in
Table 3, the inmates with LSIL/HSIL status showed a
significantly higher prevalence of HR-HPV positivity
(100% vs. 16.3%; p < 0.001). In addition, the percentage
of subjects positive for both HPV DNA testing and cy-
tology was comparable to that reported in other screen-
ing programs [12,15], although a high prevalence of high
grade pre-neoplastic lesions (HSIL/LSIL) was found
among the inmates (Table 2). However, the superior
sensitivity of the HPV testing compared to cytology was
shown by the high percentage of cases positive for HPV
DNA but negative at the cytological exam (14.3%) in
agreement with several recent studies and new guide-
lines for cervical cancer prevention [15,16]. The OR for
LSIL/HSIL status was significantly associated with the
lifetime number of sex partners (OR = 1.8 for 5-9 part-
ners; OR = 4.1 for > 10 partners; p = 0.033) and for the
age of first sexual intercourse (OR = 2.0 for age < 15
years; p < 0.05) but not for none Pap smear performed
during the past 3 years (OR = 0.8; p = 0.78).
Regard to the distribution of the HR-HPV types in the
high risk inmate group and the amount of single and
multiple infections, the genotyping assay on the 19 HPV
DNA positive samples showed the much higher preva-
lence of HPV16 compared to the other types in either
single or multiple infections (total HPV16 prevalence:
65%; single prevalence: 35%; multiple prevalence: 30%;
Figure 1. Overview of HR HPV type distribution in the total
number of positive cases. HR HPV genotype distribution in order
of predominance: HPV 16 (n = 13; 65%), HPV 31 (n = 4; 20%),
HPV 52 (n = 4; 20%), HPV 33 (n = 3; 15%), HPV 45 (n = 3;
15%), HPV 18 (n = 2; 10%), HPV 58 (n = 1; 5%). Single HR
HPV type distribution: HPV 16 (n = 7; 35%), HPV 18 (n = 2;
10%), HPV 31 (n = 1; 5%), HPV 33 (n = 1; 5%), HPV 45 (n = 1;
5%), HPV 52 (n = 1; 5%). Multiple HR HPV type distribution:
HPV 16 (n = 6; 30%), HPV 31 (n = 3; 15%), HPV 52 (n = 3;
15%), HPV 33 (n = 2; 10%), HPV 45 (n = 2; 10%), HPV 58 (n =
1; 5%).
Figure 1), confirming that, as suggested, HPV16 is the
most persistent and aggressive HR HPV type [17] and is
able to promote secondary infections or co-infections
with other genotypes [11]. Moreover, the inmates with
LSIL/HSIL status showed a significantly higher preva-
lence of multiple HPV types (60% vs. 1.2%; p < 0.001)
respect to women with normal/ASCUS Pap smear (Ta-
ble 2).
Although the main objective of our study was to assess
the validity of the HPV DNA test in a high-risk popula-
tion, our program was designed also to train the partici-
pant inmates about the value of cervical cancer preven-
tion, because only a very low percentage of the incarcer-
ated women has attended for cytological Pap-test
screening previously. The number of participants to our
study out of the total prisoners (approximately 37%)
revealed a general interest to the prevention strategy.
The results of our screening appear to confirm the role
of the risk factors taken into account in our study, which
characterize the prison population, on the development
of higher grade lesions. In fact, although the number of
preneoplastic lesions diagnosed by our intervention was
comparable to those resulting from larger screenings on
the general populations [11,12], the increased percentage
of high grade lesions among the inmates confirm the
V. Fabiano et al. / HEALTH 2 (2010) 1027-1032
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Table 2. Association between the sociodemographic characteristics, sexual and health behaviours and the HPV status in the jail in-
Category Subjects total no HPVDNA + no (%) OR (95% CI) P for trend (chi square)
Age 0.0046
< 26 years 12 6 (50) Reference
26-35 years 25 4 (16) 0.19 (0.04-0.90)
36-45 years 42 9 (21.4) 0.273 (0.07-1.05)
> 45 years 19 0 -
Race/ethnicity 0.21
White 74 16 (21.6) Reference
Latino/Hispanic 11 2 (18.1) 0.71 (0.14-3.58)
African 13 1 (7.7) 0.35 (0.04-2.99)
Marital status 0.96
Unmarried without current male partner 30 6 (20) 1.25 (0.37-4.18)
Unmarried with current male partner 8 2 (25) 1.66 (0.27-10.02)
Married 42 7 (16.7) Reference
Widowed 8 2 (25) 1.66 (0.27-10.02)
Separated-divorced 10 2 (20) 1.25 (0.21-7.18)
Lifetime no of sex partners 0.033
0-1 24 3 (12.5) 0.83 (0.18-3.68)
2-4 41 6 (14.6) Reference
5-9 21 5 (23.8) 1.82 (0.48-6.86)
Over 10 12 5 (41.6) 4.16 (0.98-17.54)
Age of first sexual intercourse 0.34
< 15 years 26 7 (26.9) 2.00 (0.65-6.15)
15-19 years 58 9 (15.5) Reference
> 19 years 11 2 (18.1) 1.21 (0.22-6.55)
Oral intercourse 0.34
Never 64 14 (21.8) Reference
Ever 34 5 (14.7) 0.61 (0.20-1.88)
Anal intercourse 0.99
Never 81 16 (19.7) Reference
Ever 17 3 (17.6) 0.87 (0.22-3.39)
Tobacco consumption 0.60
Non smokers 23 5 (21.7) Reference
1-10 cigarettes 24 6 (25) 1.2 (0.31-4.65)
> 10 cigarettes 51 8 (15.6) 0.67 (0.19-2.32)
Alcohol consumption 0.65
Never 67 14 (20.8) Reference
Mild 23 3 (13.0) 0.56 (0.14-2.18)
Abuse 8 2 (25) 1.26 (0.22-6.94)
Condom use 0.57
Frequent 20 3 (15) Reference
Infrequent or never 78 16 (20.5) 1.46 (0.38-5.61)
Pap smear during the past 3 years 0.51
Yes 15 2 (13.6) Reference
No 83 17 (20.4) 1.67 (0.34-8.13)
V. Fabiano et al. / HEALTH 2 (2010) 1027-1032
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Table 3. Detection of HR-HPV DNA and accordance with cervical cytology in the inmates attending for the screening.
Characteristics Overall
no = 98
Normal/ASCUS Pap
smear no = 86
LSIL/HSIL Pap smear
no = 5 Unsatisfactory no = 7 P value
HR-HPV Positive 19 (19.4) 14 (16.3) 5 (100)* 0 < 0.001
Prevalence of multiple HPV
types 4 (4.1) 1 (1.2) 3 (60) 0 < 0.001
P values are from Fisher’s exact test; ASCUS, atypical squamous cells of undetermined significance; LSIL, low grade squamous intra-epithelial lesions; HSIL,
high grande squamous intraepithelial lesions; * Pap smear: 1 LSIL, 4 HSIL.
validity of the risk factors analyzed through our ques-
Moreover, it is well know that most HPV infections
spontaneously regress: however, if the infection is per-
sistent, the risk of cervical cancer substantially increases
[18]. In natural or organized screening programs, about
80% of the detected low grade lesions spontaneously
regressed [18,19], while in a population as the jail in-
mates that never attended to a screening program or that
had not more than a Pap test during the life the lesions
are believed to persist and progress to high grade.
Our study was designed evaluating all the cytological
scrapings after HR-HPV testing and our results are in
accordance with those obtained by the experimental arm
of the New Technologies for Cervical Cancer (NTCC)
[12]. Since in HPV DNA by HC2 screening strategies it
is possible to increase the length of follow up respect to
Pap-test based programs (3-5 years if HPV DNA test is
negative twice) [20], our approach will be very useful
for incarcerated women which do not have the opportu-
nity or the social and cultural environment to receive
preventive care.
The results on the distribution of the HR-HPV geno-
types among the inmates revealed the much higher preva-
lence of HPV16 compared to the other types in either
single or multiple infections, as expected [11,17]. It is
currently known that more than 40% of HR HPV positive
cases display multiple viral types [21], although the pos-
sible impact of these co-infections on the progression of
cervical malignancies has not been determined yet. It is
also well recognized that HPV16 represents the pre-
dominant genotype [19]. In contrast, the very low per-
centage of cases positive for HPV18 (10%) in our popu-
lation is somehow surprising, although Clifford et al.
have reported heterogeneity in the prevalence of HPV18
in the general population from 11 countries [22]. How-
ever, it is known that HPV18 is under-represented in high
grade lesions at the time of diagnosis and that the
HPV18 associated lesions rapidly progress [23].
We found a much higher rate of unsatisfactory Pap-
smears (7.1%) compared to that reported by Prandi et al.
(1.99%) in a screened population in Italy [24], possibly
due to the more frequent occurrence of vaginal/cervi-
cal infections in inmate women. Because one out of the
7 unsatisfactory cytological tests was HR- HPV positive,
we may conclude that HPV DNA testing allows to do
not repeat an unsatisfactory cervical sample [20], further
assessing the value of the addition of HPV DNA testing
for screening of a high-risk population.
Finally, in groups of women do not attending to cer-
vical cancer screenings, such as the population studied in
this program, the potential benefit of HPV vaccines are
enormous. In fact, it is now well recognized that impor-
tant additional effects of the vaccines are the cross pro-
tections against infections and diseases caused by 16/18
related HPV types, specially against HPV31 and HPV45,
which are the other genotypes causally attributed to cer-
vical cancer [25].
This work was partially supported by grants from MIUR, from Minis-
tero della Salute and from Italian Association for Cancer Research
(AIRC), Italy. The Digene Italia kindly provided STM collection media
and kits for HPV High Risk detection. The Innogenetics kindly pro-
vided INNO-LiPA kits for HPV genotyping.
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