World Journal of AIDS, 2011, 1, 37-42
doi:10.4236/wja.2011.12007 Published Online June 2011 (http://www.SciRP.org/journal/wja)
Copyright © 2011 Sc iR es. WJA
37
Screening for Anal Dysplasia in HIV-Infected Men
Who Have Sex with Men by Anal Cytology,
Human Papillomavirus Testing and Anoscopy
Eefje Jong1,2*, Jan Willem Mulder2, Anne Catherina Theresia Maria Depla3,
Eric Cornelis Maria van Gorp4, Jo han Westerga5, Claudie Flohil5, Anja Johanna Heijne-Tol6,
Paulus Henricus Marinus Smits6
1Themba Lethu Clinic, Helen Joseph Hospital, Johannesburg, South Africa; 2Department of Internal Medicine, Slotervaart Hospital,
Amsterdam, the Netherlands; 3Department of Gastroenterology, Slotervaart Hospital, Amsterdam, the Netherlands; 4Department of
Virology, Erasmus Medical Centre, Rotterdam, the Netherlands; 5Department of Pathology, Slotervaart Hospital, Am sterdam, the
Netherlands; 6Department of Molecular Biology, Slotervaart Hospital, Amsterdam, the Netherlands.
Received April 2nd, 2011; Revised April 25th, 2011; Accepted May 25th, 2011.
ABSTRACT
The incidence of anal cancer in HIV-infected men who have sex with m en (MSM) is increasing and screening is advo-
cated. In a cross-sectional study anal cytology specimens from 58 HIV-infected MSM were analyzed for adequacy, cy-
tology and HPV DNA testing results and compared to findings on anoscopy. The adequacy of cytology specimens was
high. In 34 (63%) of anal swab samples any grade of dysplasia was observed compared to 41 (71%) of biopsy speci-
mens. The cytology specimens revealed high-grade dysplasia in 4 (7%) compared to 29 (50%) of biopsy specimens. The
prevalence of high-risk HPV types was 90% by using the SPF10 PCR and 81% by using the Hybrid Capture II assay.
Because of the high HPV prevalence, HPV DNA testing alone is not a suitable diagnostic screening tool for detecting
anogenital lesions in this specific MSM population. Screening should include both anal cytology and anoscopy.
Keywords: HIV, Men, Human Papillomavirus, Anal Cancer, Screening
1. Introduction
The incidence of anal cancer in HIV-infected and HIV-
negative men who have sex with men (MSM) is increas-
ing [1-3]. The occurrence of high-grade anal dysplasia
and anal cancer is strongly associated with HIV infection,
a history of receptive anal intercourse and anogenital
human papillomavirus (HPV) infection [3-9].
Introduction of the cervical cancer screening program
resulted in a decrease in cervical cancer in cidence rates in
Western countries from 45 per 100,000 person-years to 8
per 100,000 person-years [10]. It is because of this suc-
cessful methodology that screening programmes for anal
dysplasia are advocated. The hallmark of cervical cancer
screening is the Pap smear, which enables cytological
examination of exfoliated cells [11]. Patients with abnor-
mal cervical cytology are referred for further evaluation
with cervical colposcopy. However, sensitivity of cytolo-
gy is not optimal. The sensitivity of atypical squamous
cells of undetermined significance (ASCUS) cervical cy-
tology can be greatly improved with the introduction of
HPV DNA testing using the Hybrid Capture II (HCII)
assay for the detection of high-risk HPV strains [12-15].
Although HCII testing is not yet FDA approved for use in
the anal canal, it has been shown to improve the ability to
predict high-grade dysplasia in MSM with ASCUS cy-
tology. Referring only those with ASCUS and high-risk
HPV genotypes for anoscopy prevents unnecessary diag-
nostic procedures i n this group [16].
We investigated the prevalence of anal dysplasia in a
group of HIV-infected MSM using clinician-collected
anal cytology and HPV DNA testing compared to find-
ings on anoscopy with biopsy. The adequacy of the dif-
ferent screening methods was determined. The findings
of this study could be used to determine the best future
screening strategy for anal dysplasia in HIV-infected
MSM.
2. Study Design
A cross-sectional study was conducted at the HIV outpa-

38 Screening for Anal Dysplasia in HIV-Infected Men Who Have Sex with Men by Anal Cytology, Human Papillomavirus
Testing and Anoscopy
tient clinic of the Slotervaart Hospital, Amsterdam, the
Netherlands. HIV-infected MSM were asked to partici-
pate. All patients provided written informed consent be-
fore inclusion in the study. Inclusion started in March
2008. Demographic and clinical information was col-
lected by using a standardized questionnaire or was re-
trieved from the patient’s medical file. In each patient
who consented with anoscopy a clinician-collected anal
swab was taken for cytological examination and HPV
DNA testing. The study was approved by the Institution-
al Review Board.
2.1. Anal Cytology
The clinician-collected anal cytology sample was ac-
quired through inserting a cytobrush 5 cm into the anal
canal. The cytobrush was removed while rotating 360
degrees and pressing to the wall of the anal canal. The
collected sample was fixed in 1.5 ml of Surepath pre-
servative fluid (Becto n Dickinson, USA) for liquid-based
cytology and HPV testing. Preparations were produced
analogous to thin layer liquid based cervical cytology
using Autocyte (Autocyte, Tripath Imaging Inc, Burling-
ton, USA) .
2.2. Anoscopy
Anoscopy was done with the use of a conventional gy-
naecologic colposcope. All exams were performed by or
under direct supervision of one single experienced gas-
troenterologist during the whole study period. At first a
digital anorectal examination was performed. An anal
cytology sample was collected as described in the pre-
vious paragraph. Thereafter a 3% acetic acid solution
was locally applied by inserting and rotating a soaked
wooden cotton-tipped swab. A second swab with acetic
acid was inserted and left in place for one minute. Next,
the proctoscope was introduced to inspect the anal canal.
The acetowhite areas and the areas with a suspicious ap-
pearance were biopsied. In case of no suspected area, no
biopsies were taken.
2.3 Biopsy and Anal Swab Sample Preparation
All cytological and histological preparations and speci-
mens were examined by two experienced pathologists.
Cellular changes were determined using standard criteria
for gynaecologic cytology in accordance with the Be-
thesda system [17]. Cytological specimens were classified
as normal, ASCUS, low-grade squamous intraepithelial
lesion (LSIL), or high-grade squamous intraepithelial
lesion (HSIL). Histological specimens were classified as
normal, anal intraepithelial neoplasia (AIN) grade 1, AIN
grade 2, AIN grade 3, or squamous cell carcinoma (SCC).
2.4. HPV DNA Testing
After processing the anal swab sample for cytological
examination the remainder of the sample was sent to the
Molecular Biology Department for HPV DNA testing.
All samples were stored at 5°C until further processing.
After DNA isolation, HPV DNA was amplified by the
SPF10 PCR primer set (Innogenetics, Gent, Belgium).
Test characteristics and reaction conditions have been
described
Before, [18] from 43 patients enough material was
available to be analyzed on the presence of high risk
HPV DNA using the HCII test (Qiagen, Hilden, Germa-
ny).
3. Results
The results of 58 HIV-infected MSM are presented here.
The patient characteristics are shown in Table 1. The
mean age was 44.8 years (± 9.4), 85% was using com-
bined antiretroviral therapy, 71% had a HIV viral load
below 40 copies/ml, and 57% reported receptive anal
intercourse in the last 6 months.
Table 2 outlines the results of the clinician-collected
anal swab samples as compared to the findings on anos-
copy. Specimen adequacy for cytological specimens was
high (53/58, 91%). In 34 (63%) of anal swab samples
any grade of dysplasia was observed compared to 41
(71%) of biopsy specimens. The cytology specimens
revealed high-grade dysplasia in 4 (7%) participants
compared to 29 (50%) of biopsy specimens. The agree-
ment between findings on cytology and histology was
poor (kappa 0.20). No significant association between
CD4 cell count, HIV viral load, receptive anal inter-
course in the last 6 months, treatment for sexually trans-
mitted diseases in the last year or smoking and any grade
of anal dys pl a sia was o bse rved.
The high-risk HPV prevalence in the cytology speci-
mens was 90%. All patients infected with HPV DNA
harboured a median number of 2 (range 0 - 7) high-risk
HPV types (data not shown). In the 43 samples that were
analyzed with both the SPF10 PCR and the HCII assay
identical test results for the presence or absence of
high-risk HPV types were found in 35 patients (81%).
4. Discussion
In the study presented here we evaluated different as-
pects of a screening programme for anal dysplasia in
HIV-infected MS M. Cytological findings and HPV DNA
testing results on clinician-collected cytology specimens
were compared to histological find ing s .
The HPV prevalence in our study population was high
and infections with multiple high-risk HPV types were

Screening for Anal Dysplasia in HIV-Infected Men Who Have Sex with Men by Anal Cytology, Human Papillomavirus
Testing and Anoscopy
Copyright © 2011 Sc iR es. WJA
39
Table 1. Baseline characteristics of HIV-infected MSM (n = 58).
Characteristic
Mean age in years (± SD)
Ethnicity
Caucasian
Latino
Other
CD4 cell count (cells/mm3)
< 200
200 - 500
> 500
HIV viral load (copies/ml)
< 40
40 - 100.000
> 100.000
Use of ART
Type of ART
NRTI + NNRTI
NRTI + PI
NRTI
Other
Duration of ART use (months, IQR)
Receptive anal intercourse in last 6 months
Frequency of receptive anal intercourse in last 6 months
0
1 - 5
6 - 20
21 - 40
Number of sex pa rt ners in last 6 months
0
1
2 - 10
11 - 20
21 - 30
> 30
Received treatment for sexually transmitted disease in last year
Gonorrhoea
Chlamydia
Syphillis
Current sm oker
44.8 (± 9.4)
51 (86%)
4 (7%)
4 (7%)
1 (2%)
25 (42%)
33 (56%)
42 (71%)
14 (24%)
3 (5%)
50 (85%)
36 (72%)
8 (16%)
2 (4%)
4 (8%)
106 (24 - 137)
57%
43%
36%
18%
3%
19%
34%
24%
12%
7%
4%
11%
11%
18%
39%
MSM, men who have sex with men; ART, antiretroviral therapy; NRTI, nucleoside reverse transcriptase inhibitor; NNRTI, non-nucleoside
reverse transcriptase inhibitor; PI, protease inhibitor; IQR, interquartile range.
common. The high HPV prevalence and detection of
multiple HPV genotypes is in accordance with previous
studies in HIV-infected MSM [19-23]. Due to the very
high HPV prevalence found with both the SPF10 PCR
and HCII assay as HPV DNA testing methods, HPV
DNA testing lacks specificity to detect anal dysplasia in
this specific patient population.
A high prevalence of any grade of dysplasia was ob-
served in both cytology and histology specimens. No
data on sensitivity and specificity were calculated be-
cause biopsies were not done in every patient and the
patient number is too low to perform any statistical anal-
ysis on. The observed agreement between findings on
cytology and histology was poor. Cytological testing w as
complicated by a generally low cell yield. Furthermore,
inadequate sampling of the transformation zone due to
blind sampling could lead to an incorrect classification of
dysplasia on cytology. This is also reflected in the high
proportion of ASCUS cytology. In 44% of clini-
cian-collected cytological samples ASCUS was reported.

Screening for Anal Dysplasia in HIV-Infected Men Who Have Sex with Men by Anal Cytology, Human Papillomavirus
Testing and Anoscopy
40
Table 2. Comparison of findings for clinician-collected anal cytology specimens with biopsy specimens (n = 58).
Histology
No biopsy
Normal
AIN1
AIN2
AIN3
SCC
Ulcer
Total
Cytology
Inadequate
Normal
ASCUS
LSIL
HSIL
Total
0
5
4
1
0
1
1
4
1
0
1
7
1
3
6
1
0
11
1
8
6
1
2
18
0
1
8
1
0
10
0
0
0
0
1
1
0
0
1
0
0
1
3
21
26
4
4
58
AIN, anal intraepithelial neoplasia grade 1; AIN2, anal i ntraepithelial neoplasia grade 2; AIN3, anal intraep ithelial neoplas ia grade 3; SCC, squ amous cell
carcinoma; ASCUS, atypical squamous cells of undetermined significance; LSIL, low-grade intraepithelial lesion, HSIL, high-grade intraepithelial lesion.
Other studies showed incidence rates of ASCUS cytolo-
gy in the anal canal of 14% - 78% in HIV-infected MSM.
These studies indicated that the incidence of ASCUS
cytology in the anal canal is higher than in the cervix [16,
23,24]. Adding the HCII assay in case of ASCUS cytol-
ogy, as is currently done for ASCUS on cervical cytolo-
gy, could improve the clinical sensitivity to detect anal
dysplasia [25-27]. However, in this study the HPV pre-
valence when using the HCII assay was still 81% so
adding this assay would not improve clinical sensitivity.
In two large studies on anal cancer screening in
HIV-infected patients, in a predominantly male HIV-
infected population, anal cytology and HPV DNA detec-
tion have high sensitivity but low specificity for detect-
ing high-g rade anal dysplasia [23,28].
In the study presented here patients with high-grade
dysplasia were referred for treatment to a surgeon with
experience in the field of anal surgery. If patients refused
referral for treatment a follow-up anoscopy was sche-
duled in a year. All patients without a treatment indica-
tion were scheduled to repeat anal cytology and HPV
testing in two years followed by anoscop y. A more strict
screening algorithm was suggested by Goldstone et al.
[29]. The guidelines from the European AIDS Clinical
Society (EACS) recommend a digital rectal exam with or
without Pap smear testing with a screening interval of 1 -
3 years [30].
The considerable prevalence of high-grade dysplasia
on anoscopy with biopsy calls for a routine screening
program for anal dysplasia in HIV-infected MSM. How-
ever, the optimal screening strategy to limit the amount
of patients requiring anoscopy needs to be determined
still. Testing for HPV DNA using the HCII assay lacked
clinical sensitivity as over 80% of participants were
HPV-infected. Self-collected anal cytology could be a
promising sampling method, but the availability of
anoscopy and trained physicians is a prerequisite in the
implementation of a screening program on anal dysplasia,
because as it currently stands almost all patient require
anoscopy. In agreement with our results, a study has bee n
done assessing cost-effectiveness of high-resolution anos-
copy (HRA), anal cytology, and anal HPV detection in
screening for AIN2/3 in HIV-positive MSM. The direct
use of HRA is the most cost-effective strategy for de-
tecting AIN2/3 in HIV-infected MSM [31].
In conclusion, the prevalence of anal HPV infection
and anal dysplasia on cytological and histological sam-
ples in HIV-infected MSM is high. The agreement be-
tween cytology and histology results is poor. Given the
high HPV prevalence HPV DNA testing should not be
routinely applied in this specific patient population of
MSM. Screening should include anoscopy. Finally, fol-
low-up is essential to improve our knowledge on the nat-
ural course of anal dysplasia and to determine the optim-
al screening interval.
5. Acknowledgements
We would like to thank Mrs. H. Paap, Mrs. M. Stroomer
and Mr. D.J. Vlasblom, HIV nurse consultants, for their
great help with including patients and their logistical
support. Many thanks to Ms. C. Wientjes, MD, Ms. S.
Willemse, MD, and Mr. P. Smit, MD, for their practical
support with anosc o py.
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