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Year : 2012  |  Volume : 55  |  Issue : 1  |  Page : 52-55
Evaluation of cervical cytological abnormalities in Turkish population

Obstetrics and Gynecology Division, Maltepe University Medicine Faculty Hospital Atatürk Cad. Maltepe Istanbul, Turkey

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Date of Web Publication11-Apr-2012


Introduction: Cervical cancer is one of the most common female malignancy with high mortality rates in developing countries. Our purpose was to determine the prevalence of cervical cytologic abnormalities in population (strict Islamic religious area) and the detection rate of epithelial abnormalities by cervical cytology (CC). Materials and Methods: A total of 32,026 conventional pap smear tests collected between January 2006 and January 2010 from three hospitals are retrospectively analyzed. Results: Total of 900 (2.8%) cases had epithelial abnormalities. The numbers and rates of epithelial abnormalities were as the followings: Atypical squamous cell of undetermined significance (ASCUS; n=615 [1.9%]); atypical squamous cell suspicious for high-grade squamous intraepithelial lesion (ASC-H; n=27 [0.1%]); atypical glandular cell of undetermined significance (AGUS; n=73 [0.2%]); low- grade squamous intraepitelial lesion (LSIL; n=147 [0.5%]); high- grade squamous intraepithelial lesion (HSIL; n=35 [0.1%]); and squamous cell carinoma (SCC; n=3 [0.0%]). Conclusion: The prevalence of cervical cytological abnormality in our study was 2.8%. Recently, some conflicting results from the same population were published. More prospective studies with larger numbers are needed.

Keywords: Cervical cancer, cytology, PAP smear

How to cite this article:
Atilgan R, Celik A, Boztosun A, Ilter E, Yalta T, Ozercan R. Evaluation of cervical cytological abnormalities in Turkish population. Indian J Pathol Microbiol 2012;55:52-5

How to cite this URL:
Atilgan R, Celik A, Boztosun A, Ilter E, Yalta T, Ozercan R. Evaluation of cervical cytological abnormalities in Turkish population. Indian J Pathol Microbiol [serial online] 2012 [cited 2022 Dec 1];55:52-5. Available from:

   Introduction Top

Cervical cancer is one of the most common female malignancies with high mortality rates in developing countries. The five-year survival is 50% in developing countries where it is 66% in developed ones. All over the world, estimated new cases of cervical (uterine cervix) cancer was 493 000 and deaths were 274 000 in 2002. [1]

The impact of cervical cytology (CC) screening has been demonstrated by steadily reduced rates of incidence and mortality due to invasive cervical cancer in the developed countries over the last decades. In the past 60 years, the mortality from cervical cancer has decreased 70 to 80% in developed countries. The incidence was decreased from 32/100 000 in 1940's to 8.3/100 000 in 1980. The  Pap smear More Details test is a simple, non-invasive, and a cost-effective method for the diagnosis of cervical and vaginal precancerous, cancerous lesions. [2]

According to a study made by the International Agency for Research on Cancer in 2002, the cervical cancer incidence rate in Turkey was 4.5/100 000, it was estimated to encounter 1 364 new cervical cancer cases and 726 of the reported deaths were associated with cervical cancer in the same year. [1] In 2003, the results of studies performed by the Turkish Ministry of Health, department of cancer control in eight cities were published. [3] This study showed that cervical cancer ranks the 10 th among all women's cancers and its incidence rate is 4.76/100 000.

Similar results were found throughout Europe. Nearly four million cervical screening tests are performed every year in the United Kingdom and the age-standardized incidence and mortality rates for cervical cancer were 9 and 3.7 per 100,000, respectively. [4] There are some differences between Western and Eastern Europe. Every year, nearly 13 000 women were diagnosed as cervical cancer in the West, whereas the number was higher in the Eastern Europe (31 000) and more than half of these women were lost due to the cervical cancer. [1],[5]

Our purpose was to determine the prevalence of cervical cytological abnormalities in the strict religious part of Turkish population and the detection rate of epithelial abnormalities by CC.

   Materials and Methods Top

A total number of 32 026 conventional pap smear tests were collected between January 2006 and January 2010 from three hospitals located in the east of the country consisting approximately six devout cities and the results were retrospectively analyzed. Local ethical comity approval has been taken for the study. Conventional samples (CC) were collected and smeared into the slide and immediately fixed with polyethylene glycol. The samples were evaluated by five different pathologists. The results were assessed as satisfactory and unsatisfactory. Satisfactory results were based on the 2001 Bethesda system and subdivided as "negative" (including "atypia, favors reactive"), "squamous cell atypia" (atypical squamous cells of undetermined significance [ASCUS] and atypical squamous cells, cannot exclude high-grade lesions [ASC-H]), "atypical glandular cells" (AGUS), "low-grade squamous intraepithelial lesion" (LSIL), "high-grade squamous intraepithelial lesion" (HSIL), "squamous cell carcinoma" (SCC), and "adenocarcinoma." The statistical analyses were performed by SPSS software vs. 13. 0 (SPSS Inc., Chicago, USA) statistical program.

   Results Top

A total number of 32 026 samples were retrospectively analyzed. The mean age of the participants was 38 ± 1 years (16 to 92 years). Cytological findings of the smear results are listed in [Table 1].
Table 1: Cytological findings of 32026 conventional smear samples

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These data show that the unsatisfactory rate for the CC technique was 2.1% (n=659). The main causes for CC inadequacy were sample obscured by red blood cells and inflammation. Benign cytology results were seen in 30 467 (95%) of the samples. The most common reported benign result was chronic cervicitis with 23 846 cases (74.5% of all samples).

The numbers and rates of other normal results detected by CC were as the followings, respectively: Normal benign results, n=3 078 (9.6%); atrophy, n=2 332 (7.3%); squamous metaplasia, n=1 211 (3.8%).

A total number of 900 (2.8%) cases had epithelial abnormalities. The numbers and rates of epithelial abnormalities were as the follows: ASCUS (n=615/1.9%) [Figure 1]; ASC-H (n=27/0.1%); AGUS (n=73/0.2%); LSIL (n=147/0.5%) [Figure 2]; HSIL (n=35/0.1%) [Figure 3]; and SCC (n=3/0.0%).
Figure 1: Atypical squamous cells of undetermined significance (PAP, ×400)

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Figure 2: Low-grade squamous intraepithelial neoplasia (PAP, ×400)

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Figure 3: High-grade squamous intraepithelial neoplasia (PAP, ×400)

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One patient with chronic cervicitis had undergone colposcopy due to suspicious findings. The colposcopic biopsy result was reported as SCC. Moreover, six patients with epithelial abnormalities (1 ASCUS, 1 LSIL, and 4 HSIL) had been diagnosed as SCC by the histological confirmation during the colposcopic examination.

   Discussion Top

According to 2002 and 2005 researches, the highest incidence rates of cervical cancer are observed in sub-Saharan Africa, Melanesia, Latin America, the Caribbean, south central Asia, and Southeast Asia. Currently, the incidence rates in developed countries were generally low, with age-standardized rates less than 14.5/100 000. The incidence for Turkey is as low as 4.5/100 000. [1] Also, the studies made by the Turkish Ministry of Health, Department of Cancer Control in 2003 supported the rates reported for cervical cancer. [3] However, this pattern is relatively recent; before the introduction of screening programs in the 1960s and 1970s, the incidence rates in most of the European countries, North America, and Australia/New Zealand were similar to those in the developing countries today. [6] The incidence was 38.0/100 000 in the Second National Cancer Survey of the United States. [7] Also, very low rates are observed in China (6.8/100 000) and Western Asia (5.8/100 000); the lowest recorded rate is 0.4/100 000 in Ardabil, northwest Iran. [8]

The major cause of cervical cancer is Human papilloma virus (HPV) are a large family of small double-stranded DNA viruses that infect squamous epithelia. Genital HPV infections are very common, sexually transmitted, and have peak prevalence between ages 18 and 30 years. The most important subtypes for cancer are HPV 16, found in 50 to 70% of cases, and HPV 18, found in 7 to 20% of cases. [9]

This paper highlights the abnormalities seen in CC in the Turkish population. Abnormal CC prevalence rate in Turkey is lower than that in India and Europe and North America. This might be due to sociocultural differences, lack of population-based studies or a lower HPV prevalence. Further studies are required to fully assess the above mentioned factors, especially the role of HPV.

The other cervical cancer risk factors are having first sexual intercourse before 16 years old, having more than four sexual partners, smoking, oral contraceptive use, and genital condyloma history. [10] One of the most important risk factor for cervical cancer is the absence of screening with the pap smear test which was first introduced in 1942 by Papanicolaou. Cancer is more common among the women who do not have regular pap tests. SCC is seen 3.9 and 13 times more in a woman screened once in three years and 10 years, respectively, compared with ones screened annually. [11] In developed countries such as USA, 85% of women had at least one pap test through their lifetime, but this rate is only 5% in the developing countries. [12]

American Cancer Society recommends initiating cervical cancer screening about 3 years after the first vaginal intercourse, but no later than 21 years old. Women who have had three normal Pap test results in a row may get screened every two to three years after their 30s. Recommendations point that women at 70 years of age or older might choose to discontinue the screening with the Pap tests if they have had three or more normal Pap tests in a row and had no abnormal Pap test results in the last 10 years. [13]

We demonstrated that 659 (2.1%) of 32 026 CC examinations were unsatisfactory. The main causes for CC inadequacy were sample obscured by red blood cells and inflammation. Previously, Beerman et al. [14] (0.89%) found lower rates of unsatisfactory samples.

Of all, 615 cases (1.9%) were classified as ASCUS in this study. Recently, Davey et al. [15] reviewed 56 studies and found higher detection rates (3.8%) of ASCUS with the CC examination. Moreover, Lawson et al. [16] found the ASCUS rate among low-income women as 5.2%. On the other hand, Beerman et al. [14] (0.87%) and Abdullah [17] (0.45%) found lower detection rates of ASCUS.

In the present study, the detection rates for ASCUS and over lesions were found to be 2.8% (n=900). Previous results from Turkey were lower which were reported by Inal et al. [18] (0.7%) and Coskun et al. [19] (1.7%), except a study designed by Colgan et al. [20] in which the lesions rate were 3.8%. Our results were also significantly lower than those multi-centered studies reported from Europe and U.S.A (7% - 3.6%). [21]

Turkish Cervical Cancer And Cervical Cytology Research Group (TCC and CCRG) published 140 334 cervical smear results from 33 centers of Turkey in 2007. [22] Overall, the prevalence of cervical cytological abnormalities was 1.8%; the prevalence of preinvasive cervical neoplasia was 1.7% and the prevalence of cytologically diagnosed invasive neoplasia was 0.06%. Our results were similar to TCC and CCRG and some other previous reports from Turkey. [22],[23],[24] Celik et al. [25] reported a higher prevalence for almost all epithelial abnormalities (ASC and ASC-H - 4.8%; LSIL - 1.8%; HSIL - 1.1%; AGUS - 0.9%; and cancer - 0.07%) [Table 2]. Previous foreign studies reported higher prevalence of ASC-US, LSIL, HSIL, and AGC in the USA (3.9%, 2.1%, 0.5%, and 0.2%, respectively). [26] Lower prevalence in our study among the very strict Islamic population compared with Christian countries may be due to the low prevalence of HPV, which might be a result of Islamic religion belief on sexual attitude and the conservative culture of population. [24]
Table 2: Comparison of Turkish population prevalence of cervical cytological abnormalities detected in pap smear screening test

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In conclusion, the prevalence of cervical cytological abnormalities in our study was 2.8%. Recently, some conflicting results from the same population were published. More prospective studies with larger numbers are needed to determine the real prevalence of the cervical epithelial abnormalities in a Muslim country, to generate more reliable policies.

   References Top

1.Ferlay J, Bray F, Pisani P, Parkin DM. Cancer incidence, mortality and prevalence worldwide [database]. Lyon, France: International agency for research on cancer (IARC); Cancer Base 2002;5:2.  Back to cited text no. 1
2.Roohi M, Sahi SC. Incidence of cervical intraepithelial neaplasia in Faisalabad. Pak J Med Res 1997;32:164-5.  Back to cited text no. 2
3.Yilmaz H.H, Yazihan N, Tunca D, Sevinç A, Olcayto E.Ö, Özgül N, et al. Cancer trends and Incidence and mortality patterns in Turkey. Jpn J Clin Oncol 2010;41:10-6.  Back to cited text no. 3
4.Karnon J, Peters J, Platt J, Chilcott J, Mc Googan E, Brewer N. Liquid-based cytology in cervical screening: An updated rapid and systematic review and economic analysis. Health Technol Asses 2004;8:20.  Back to cited text no. 4
5.Boyle P, Ferlay J. Cancer incidence and mortality in Europe 2004. Ann Oncol 2005;16:4818.   Back to cited text no. 5
6.Gustafsson L, Pontén J, Bergström R, Adami HO. International incidence rates of invasive cervical cancer before cytological screening. Int J Cancer 1997;71:159-6.  Back to cited text no. 6
7.Dorn HF, Cutler SJ. Morbidity from cancer in the United States: Public health monograph, Washington, DC: US Department of Health, Education, and Welfare; 1959.  Back to cited text no. 7
8.Sadjadi A, Malekzadeh R, Derakhshan MH, Sepehr A, Nouraie M, Sotoudeh M, et al. Cancer occurrence in Ardabil. Results of a population - based cancer registry from Iran. Int J Cancer 2003;107:113-8.  Back to cited text no. 8
9.Stanley M. Pathology and epidemiology of HPV infection in females. Gynecol Oncol 2010;117:5-10.  Back to cited text no. 9
10.Kjellberg L, Hallmans G, Ahren AM, Johansson R, Bergman F, Wadell G, et al. Smoking, diet, pregnancy and oral contraceptive use as risk factors for cervical intra-epithelial neoplasia in relation to human papillomavirus infection. Br J Cancer 2000;82:1332-8.  Back to cited text no. 10
11.IARC Monographs on the evaluation of carcinogenic risks humans. Human Papillomaviruses. Lyon: IARC; 2005.  Back to cited text no. 11
12.Kuo DY, Goldberg GL. Screening of cervical cancer: Where do we go from here? Cancer Invest 2003;21:157-61.  Back to cited text no. 12
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14.Beerman H, van Dorst EB, Kuenen-Boumeester V, Hogendoorn PC. Superior performance of liquid-based versus conventional cytology in a population-based cervical cancer screening program. Gynecol Oncol 2009;112:572-6.  Back to cited text no. 14
15.Davey E, Barratt A, Irwig L, Chan SF, Macaskill P, Mannes P, et al. Effect of study design and quality on unsatisfactory rates, cytology classifications, and accuracy in liquid-based versus conventional cervical cytology: A systematic review. Lancet 2006;367:122-32.  Back to cited text no. 15
16.Lawson HW, Lee NC, Thames SF, Henson R, Miller DS. Cervical cancer screening among low-income women: Results of a national screening program, 1991-1995. Obstet Gynecol 1998;92:745-52.  Back to cited text no. 16
17.Abdullah LS. Pattern of abnormal pap smears in developing countries: A report from a large referral hospital in Saudi Arabia using the revised 2001 Bethesda system. Ann Saudi Med 2007;4:268-72.  Back to cited text no. 17
18.Inal MM, Köse S, Yildirim Y, Ozdemir Y, Töz E, Ertopçu K, et al. The relationship between human papillomavirus infection and cervical intraepithelial neoplasia in Turkish women. Int J Gyneacol Cancer 2007;17:1266-70.  Back to cited text no. 18
19.Coskun A, Köstü B, Kiran G, Arikan DC, Analan A. Pap smear screening result in Kahramanmaras. Gynecol Obstet Reprod Med 2008;14:182-5.  Back to cited text no. 19
20.Colgan TJ, McLachlin CM, Cotterchio M, Howlett R, Seidenfeld AM, Mai VM. Results of the implementation of liquid-based cytolog. Cancer 2004;102:362-7.  Back to cited text no. 20
21.Stany MP, Bidus MA, Reed EJ, Kaplan KJ, McHale MT, Rose GS, et al. The prevalence of HR-HPV DNA in ASC- US pap smears: A military population study. Gynecol Oncol 2006;101:82-5.  Back to cited text no. 21
22.Turkish Cervical Cancer and Cervical Cytology Research Group.Prevalence of cervical cytological abnormalities in Turkey. Int J Gyneacol Obstet 2009;106:206-09.  Back to cited text no. 22
23.Karabulut A, Alan T, Ekiz MA, Iritaº A, Kesen Z, Yahºi S. Evaluation of cervical screening results in a population at normal risk. Int J Gyneacol Obstet 2010;110:40-2.   Back to cited text no. 23
24.Yalti S, Gürbüz B, Bilgiç R, Cakar Y, Eren S. Evaluation of cytologic screening results of the cervix. Int J Gynecol Cancer 2005;15:292-4.  Back to cited text no. 24
25.Celik C, Gezginç K, Toy H, Findik S, Yilmaz O. A comparison of liquid-based cytology with conventional cytology. Int J Gyneacol Obstet 2008;100:163-6.  Back to cited text no. 25
26.National Cancer Institute, surveillance epidemiology and end results. Available from:  Back to cited text no. 26

Correspondence Address:
Aygen Celik
Obstetrics and Gynecology Division, Maltepe University Medicine Faculty Hospital Atatürk Cad. Çam Sok No. 3, 34843 Maltepe Istanbul
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Source of Support: None, Conflict of Interest: None

DOI: 10.4103/0377-4929.94856

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  [Figure 1], [Figure 2], [Figure 3]

  [Table 1], [Table 2]

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