2019, Volume 35, Number 2, Page(s) 102-106
Two-Year Results of Community-Based Screening Program for Human Papilloma Virus DNA in Çorum Province
Güven GÜNEY1, Emine ARSLAN2, Yılmaz BAŞ1, Ebru TURGAL3
1Department of Pathology, Hitit University, Faculty of Medicine, ÇORUM, TURKEY
2Department of Obstetric and Gynecology, Hitit University, Faculty of Medicine, ÇORUM, TURKEY
3Department of Biostatistics, Hitit University, Faculty of Medicine, ÇORUM, TURKEY
Keywords: Uterine cervical neoplasm, HPV DNA test, Turkey, Diagnostic Screening Programs
The Turkish Ministry of Health started a community-based screening program using Human Papilloma Virus (HPV) DNA in 2014.
In our study, we aimed to investigate the results of this survey in Çorum province between the years of 2016-17 to determine the shortcomings
and deficiencies in practice.
Material and Method: All of the women between the ages of 30 and 65 years who had undergone High risk HPV DNA screening in Çorum
province between 2016 and 2017 were included in the study. High risk HPV types were divided into three categories as type 16, 18 and others. The
target group of patients to be screened were compared with the numbers reached in the survey. After colposcopic biopsy, the clinicopathological
correlation of the patients who underwent colposcopic biopsy was determined via pathology reports.
Results: HPV DNA was detected in 817 women (3.5%). HPV types 16, 18 and others were found to be positive in 216, 32 and 569 individuals,
respectively. Cervical biopsy was performed with colposcopy in 212 (26%) women. As the result of colposcopy, LSIL and HSIL were detected in
63 and 56 patients, respectively. 34.5% of patients with the diagnosis of any kind of dysplasia received treatments.
Conclusion: It was determined that 44% of HPV DNA-positive patients were not subjected to the appropriate processes according to the national
guidelines. This shows that despite the screening, the desired therapeutic effect could not be achieved.
Cervical cancer is the third most common cancer in women
all over the world, leading to considerable morbidity and
. A number of epidemiological and molecular
studies have shown that Human Papilloma Virus (HPV) is
the main cause of cervical cancer and more than 90% of all
cervical cancers are positive for HPV DNA 2-5
Invasive carcinogenesis of HPV is found to be related to
precancerous lesions and this process takes a long time
6. Therefore, necessary precautions can be taken before
invasive cancer develops by means of HPV screening
programs. It has also been possible to provide prophylaxis
with improved HPV vaccines against this virus since 2006
7,8. The effective use of HPV screening programs in
developed countries has led to a decline in the incidence
of cervical cancer when compared to developing countries
The Turkish Ministry of Health launched a communitybased
screening program using cervical smears in 2004 10-15. However, the result was far below expectation, and only
1-2% of the targeted population could be detected 14. As a result, a new strategy was set in 2014 and a communitybased
screening program using HPV DNA was introduced.
In our study, we aimed to present the results of this survey
in Çorum province between the years of 2016-2017 to
determine the shortcomings and deficiencies in the practice.
All of the women between the ages of 30 and 65 years who
had undergone high risk HPV DNA screening in Çorum
province within the scope of the National Screening
Program by the Çorum provincial health directorate
between the years of 2016 and 2017 were included in the
study. Within the scope of the screening, two samples were
taken from each woman by the family physicians. The first
sample was collected with a brush and transferred to a glass
slide for conventional cytology. The second was taken with
a different brush and put into 5 ml of Standard Transport
Medium for HPV DNA analysis. For women who were
HPV positive by Hybrid Capture 2 (Qiagen), genotyping
was performed with the CLART kit (Genomica).
The high risk HPV types detected in these patients and
the ages of the patients were obtained from the relevant department in the Health Directorate by official application.
High risk HPV types were divided into three categories as
type 16, 18 and others (type 31,33,34,35,39,45,51,52,56,58,5
9,66,68 and 70). If more than one type of HPV was detected
in a patient and one of them was HPV type 16 or 18, this
case was evaluated as HPV type 16 or 18.
The HPV DNA positive patients who were referred to
the Hitit University Erol Olcok Education and Research
Hospital, the only hospital where colposcopy can be
performed in Çorum, and who were examined by
colposcopy were determined via the hospital automation
system. The clinicopathological correlation of the patients
who underwent colposcopic biopsy was determined via
pathology reports. The pathology results of the colposcopic
biopsy materials were classified as Normal / Low grade
squamous intraepithelial lesion (LSIL) and high grade
squamous intraepithelial lesion (HSIL). Patients who
underwent conization/loop electro surgical excision
(LEEP)/ hysterectomy after colposcopic biopsy were again
determined through the system and the results of the
procedures were determined from the pathology reports.
The target group of patients to be screened were divided
into age ranges according to Turkish Statistical Institute
(TSI) data and the number of women in each age range
was determined. Within the national cancer screening
program, this population was planned to be screened in 5
years. So, the number of people to be screened for 2 years covering the years of 2016-2017 was determined as the
target population to be reached and compared with the
numbers reached in the survey.
Within the scope of the national cancer screening program,
HPV DNA screening was performed in a total of 23,010
women in Çorum province, 12,144 in 2016 and 10,866 in
2017 (Figure 1
). Based on TSI data, the targeted number
for the two years of the screening program was 47,557.
The total number of the women reached at the end of two
years screening program was 23,010, which corresponds
to 48.3% of the targeted number. The number of the
patients reached in the screening program closest to the
target number of patients was in 50-59 years group (59%).
However, the lowest number of patients reached compared
to the number of targeted patients was in the 30-39 years
group (38%) (Figure 1
As a result of screening, HPV DNA was detected in 817
women. This number corresponds to 3.5% of the entire
female population screened. When distributed according
to HPV types; HPV types 16, 18 and others were found
to be positive in 216 (0.9%), 32 (0.1%) and 569 (2.5%)
individuals, respectively. The ratios of the entire screening
population were evaluated: HPV positivity rate was highest
in 30-39 years group (%4.2) and lowest in 60-65 years
group (% 2.9) (Table I).
Click Here to Zoom
|Table I: Distribution of HPV types and percentages of positivity according to age.
Two hundred and twelve out of 817 (26%) women with
HPV DNA positivity underwent colposcopic biopsy.
When this number was distributed according to HPV
types, colposcopic biopsy was performed for patients with
HPV types 16, 18 and others at a rate of 126/216 (58%),
13/32 (40%) and 73/569 (13%), respectively. According
to the algorithm determined by the national guidelines,
colposcopic biopsy should have been performed for HPV
type 16 and 18 positive cases. Colposcopy was performed
for 56% of the women in this group (139/248) (Table II).
When the results of colposcopic biopsies were evaluated,
63 patients (30%) had LSIL, 56 patients had HSIL and 93
patients (44%) had no dysplasia. When this evaluation was
performed according to HPV types, LSIL was detected in 32
(28%), 3 (24%) and 20 (28%) cases for type 16, 18 and other
types of HPV, respectively. HSIL was found in 39 (31%),
6(46%) and 11(15%) cases for type 16,18 and other types of
HPV respectively. The dysplasia (LSIL + HSIL) detection
rate was 79 (62.6%), 9 (69.2%) and 31 (42%) cases in HPV
type 16, 18 and other types of HPV groups, respectively
Ten of 63 patients with LSIL (%16), 31 of 56 patients
with HSIL (55%), and a total of 41 of 119 patients with
the diagnosis of any kind of dysplasia (34.5%) underwent treatment (LEEP, conization or hysterectomy). Two
patients with LSIL had conization, 7 patients with LSIL had
LEEP and 1 patient with LSIL underwent hysterectomy
while 26 of 31 patients with a diagnosis of HSIL had
conization and 5 had LEEP (Table III).
Click Here to Zoom
|Table III: Distribution of the patients who had treatment after
HPV DNA testing in cervical cancer screening is now the
first line screening test recommended by the European
Union, the International Agency for Research On Cancer
(IARC) and the World Health Organization (WHO)
. Although the sample collection methods are
similar for both HPV DNA and cytology based screening
programs, more patients can be screened by HPV DNA
screening as screening with HPV DNA test requires less
labor force and organization.
The number of women screened with HPV DNA screening
in Turkey has been more than 5-6 times the number
screened with cytology-based screening programs 14,18.
In Turkey, the Ministry of Health set national standards for
a community-based cervical cancer screening program in
2014. The aim of this program was to screen the women
between 30 and 65 years of age in the community every 5
years. It was predicted that 20% of the target population
would be screened every year according to this program.
Between 2016 and 2017, a total of 23,010 women were
screened in Çorum province, accounting for 48.3% of
the total target population. According to age groups, the
highest screening rate was in the age range of 50-59 years
(59%), and the lowest screening rate was in the age range
of 30-39 (38%) years. In a study by Gültekin et al. which
included the screening results of 1 million women all over
Turkey, it was stated that the highest screening rate was in
the 40-44 years age range, the lowest was in the 60-65 years
age range and the second lowest was in the 30-34 years
age range 18. In our study, it was determined that there
were difficulties in reaching the young female population in
Of the screened population. 817 (3.5%) patients were
positive for HPV DNA in Çorum. This ratio was found to be
3.5% in the study by Gultekin et al. 18. Kulhan et al. found
that ratio was 2.79% in their study conducted in Erzincan
province 19. Our positivity rate was largely similar to the
screening results found in other parts of Turkey. In our
study, 26.4% of all HPV DNA positive cases were detected
as HPV type 16, 4% as HPV type 18, and 69.6% as other
types of HPV. In the study by Gultekin et al., this ratio was
20.7% for HPV 16, and 5.1 % for HPV 18 18. Kulhan et
al. found 11.25% HPV 16 and 2.27 % HPV 18 positivity in their study 19. The most common type in Çorum was
HPV 16 and compatible with the findings in other regions.
In our study, the group with the highest rate of HPV DNA
positivity was the 30-39 age group (4.2%). This was followed
by 40-49, 50-59 and 60-65 years of age, respectively (Table
I). Gultekin et al. and Kulhan et al. found that the HPV
DNA incidence was the highest in the 30-39 years age
group 18-19. HPV positivity decreases with age and goes
down to 2.9% in the age range of 60-65 years.
According to national guidelines, patients who are
positive for HPV 16 and 18 should be directly referred to
colposcopy. However, the patients who are positive for
HPV other than 16 or 18 should be referred to colposcopy
in case of squamous cell anomaly in cervicovaginal smear
taken at the time of HPV DNA sampling. Colposcopic
biopsy was performed in 212 (26%) out of 817 women
with HPV positivity in our hospital (Table II). When HPV
type 16 and 18 were evaluated together, 109 of 248 patients
(44%) did not undergo colposcopy, which was required
according to national guidelines. Gultekin et al. also stated
that approximately 40.1% of women in the whole country
were not followed according to the appropriate procedure,
similar to our study (18). In that study, it was found that the
pathological evaluation results of 1985 (56%) of the 3499
patients who underwent colposcopic biopsy were normal,
708 (20%) were LSIL, 721 (20%) were HSIL and 85 (2.5%)
were invasive cancer (18). In our study, it was revealed
that, 44% of the cases had non-SIL, 30% had LSIL and 26%
had HSIL according to colposcopic biopsy results. In our
study, the HSIL and LSIL rates were significantly higher
than that of the results of Gultekin et al. The reason for
this difference may be that the young population between
the ages of 30 and 39 could not be screened sufficiently. If
this age group could be screened adequately, the number
of cases with HPV positivity and the correlation with
the histomorphological lesions (LSIL/HSIL) could be
established more reliably. However, the patient group who
could not be further examined could also adversely affect
the rates. Furthermore, no invasive tumor was detected
as the result of colposcopic biopsies in our hospital. This
may be due to the fact that patients who were suspected
of invasive tumor during colposcopy might have been
referred to advanced centers without taking a biopsy.
According to the national guideline, treatment (LEEP
/ Conization / Hysterectomy) should be performed
especially for patients with HSIL. According to our results,
31 of the 56 (55%) patients with HSIL underwent one of
these procedures but no hospital records were found for the remaining 45% of the patients. Although some of
these patients might have gone to advanced centers for
treatment, some of the patients were thought to have
remained untreated for reasons such as being unaware, too
many patients, and not being able to make an appointment.
The percentage of women who were reached within the
scope of national cancer screening program in Çorum
province over two years shows similarities with the
results all over Turkey. However, it is noteworthy that the
percentage of the reached people was the lowest in the 30-
39 years age group, in which HPV DNA was expected to be
most common, as in seen throughout Turkey. It is obvious
that special programs and methods should be developed
to reach this age group within the scope of screening. It
was determined that 44% of HPV DNA-positive patients
were not subjected to the appropriate processes according
to national guidelines. The data were collected from a
single center which was the only one where colposcopy
was performed in Çorum province. It is possible that, a
small number of these patients received their treatments in
hospitals outside the province. However, when the sociocultural
and economic aspects of Çorum are evaluated, this
ratio will be very low and it is thought that a significant
portion of this 44% section may not have received the
appropriate treatment. It was also found that 45% of
the patients with HSIL, who were the main target of all
these screening programs and who were also at risk for
developing invasive cancer, did not receive the necessary
treatment. This shows that despite the screening, the desired
therapeutic effect could not be achieved. This patient group
needs to be directed to institutions performing colposcopy
and to be followed by the institutions in order to ensure the
necessary treatment after colposcopy.
CONFLICT of INTEREST
The authors declare no conflict of interest.
1) Ferlay J, Shin HR, Bray F, Forman D, Mathers C, Parkin DM.
Estimates of worldwide burden of cancer in 2008: GLOBOCAN
2008. Int J Cancer. 2010;127:2893-917.
2) Wardak S. Human Papillomavirus (HPV) and cervical cancer.
Med Dosw Mikrobiol. 2016;68:73-84.
3) Zhang L, Bi Q, Deng H, Xu J, Chen J, Zhang M, Mu X. Human
papillomavirus infections among women with cervical lesions
and cervical cancer in Eastern China: Genotype-specific
prevalence and attribution. BMC Infect Dis. 2017;17:107.
4) Sasaki Y, Iwanari O, Arakawa I, Moriya T, Mikami Y, Iihara K,
Konno R. Cervical cancer screening with human papillomavirus
DNA and cytology in Japan. Int J Gynecol Cancer. 2017;27:
5) Fernandez AF, Rosales C, Lopez-Nieva P, Graña O, Ballestar
E, Ropero S, Espada J, Melo SA, Lujambio A, Fraga MF,Pino I,
Javierre B, Carmona FJ, Acquadro F, Steenbergen RD, Snijders
PJ, Meijer CJ, Pineau P, Dejean A, Lloveras B, Capella G, Quer
J, Buti M, Esteban JI, Allende H, Rodriguez-Frias F, Castellsague
X, Minarovits J, Ponce J, Capello D, Gaidano G, Cigudosa JC,
Gomez-Lopez G, Pisano DG, Valencia A, Piris MA, Bosch FX,
Cahir-McFarland E, Kieff E, Esteller M. The dynamic DNA
methylomes of double-stranded DNA viruses associated with
human cancer. Genome Res. 2009;19:438-51.
6) Ghosh S, Seth, Paul J, Rahman R, Chattopathyay S, Bhadra D.
Evaluation of Pap smear, high risk HPV DNA testing in detection
of cervical neoplasia with colposcopy guided or conventional
biopsy as gold standard. Int J Healthcare Biomed Res. 2014;2:
7) Walboomers JM, Jacobs MV, Manos MM, Bosch FX, Kummer
JA, Shah KV, Snijders PJ, Peto J, Meijer CJ, Muñoz N. Human
papillomavirus is a necessary cause of invasive cervical cancer
worldwide. J Pathol. 1999;189:12-9.
8) Harper DM, DeMars LR. HPV vaccines ‐ a review of the first
decade. Gynecol Oncol. 2017;146:196-204.
9) Catarino R, Petignat P, Dongui G, Vassilakos P. Cervical cancer
screening in developing countries at a crossroad: Emerging
technologies and policy choices. World J Clin Oncol. 2015;6:
10) Ferlay J, Soerjomataram I, Dikshit R, Eser S, Mathers C, Rebelo
M, Parkin DM, Forman D, Bray F. Cancer incidence and
mortality worldwide: Sources, methods and major patterns in
GLOBOCAN 2012. Int J Cancer. 2015;136:E359-86.
11) Açikgöz A, Ergör G. Cervical cancer risk levels in Turkey and
compliance to the national cervical cancer screening standard.
Asian Pac J Cancer Prev. 2011;12:923-7.
12) Sevil S, Kevser O, Aleattin U, Özlem D. The frequency of having
pap‐smear tests among women between 15-64 years old and
the evaluation of the level of their knowledge. J Pak Med Assoc.
13) Daloglu FT, Karakaya YA, Balta H, Eren A,Aslıhan D. Cervical
cytological screening results of 8,495 cases in Turkey-common
inflammation but infrequent epithelial cell abnormalities? Asian
Pac J Cancer Prev. 2014;15:5127-31.
14) Mehmetoglu HC, Sadikoglu G, Ozcakir A, Bilgel N. Pap smear
screening in the primary health care setting: A study from
Turkey. N Am J Med Sci. 2010;2:467-72.
15) Demirhindi H, Nazlican E, Akbaba M. Cervical cancer screening
in Turkey: A community‐based experience after 60 years of pap
smear usage. Asian Pac J Cancer Prev. 2012;13:6497-500.
16) European Guidelines for Quality Assurance in Cervical Cancer
Screening. 2nd ed. Supplements. Anttila A, Arbyn M, Vuyst de
H, Dillner J, Dillner L, Franceschi S, Patnick J, Ronco G, Segnan
N, Suonio E, Törnberg S, von Karsa L, editors. Luxembourg:
European Union Publications; 2015. 194.
17) Huh WK, Ault KA, Chelmow D, Davey DD, Goulart RA, Garcia
FA, Kinney WK, Massad LS, Mayeaux EJ, Saslow D, Schiffman M,
Wentzensen N, Lawson HW, Einstein MH. Use of primary highrisk
human papillomavirus testing for cervical cancer screening:
Interim clinical guidance. Gynecol Oncol. 2015;136:178-82.
18) Gultekin M, Zayifoglu Karaca M, Kucukyildiz I, Dundar S, Boztas
G, Semra Turan H, Hacikamiloglu E, Murtuza K, Keskinkilic
B, Sencan I. Initial results of population based cervical cancer
screening program using HPV testing in one million Turkish
women. Int J Cancer. 2018;142:1952-8.
19) Kulhan M, Kulhan NG, Seven Y, Nayki UA, Nayki C, Ata N,
Ulug P. Estimation of the prevalence and distribution of HPV
genotypes and identification of related risk factors among
Turkish women. Contemp Oncol (Pozn). 2017;21:218-23.