Year : 2009 | Volume
: 52 | Issue : 1 | Page : 34--37
A comparative study of cervical smears in an urban Hospital in India and a population-based screening program in Mauritius
Kaustubh Mulay1, Meenakshi Swain1, Sushma Patra2, Swarnalata Gowrishankar1,
1 Department of Anatomic Pathology and Cytology, Apollo Hospitals, Jubilee Hills, Hyderabad - 500033, India
2 Department of Pathology, Global Hospitals, Hyderabad, India
Department of Anatomic Pathology and Cytology, Apollo Hospitals, Jubilee Hills, Hyderabad - 500 033
Objective: To study cervical smear abnormalities in urban women in India and women in Mauritius and to compare the results in the two groups. Study Design: An analysis of 6010 cervical smears taken as part of routine check-ups in an urban hospital was done and an analysis of 10,000 cervical smears taken from women participating in a National Cancer Screening Program in Mauritius was done. Emphasis was put on cervical epithelial cell abnormalities and the results in the two populations are compared with that of similar studies in other parts of the world. Results: Non specific inflammation formed 19.6% and 25.34% of the smears in the Indian and Mauritian groups, respectively (with specific infection forming 6.05% and 15.08%). The epithelial abnormalities constituted 1.392% of the Indian group and 0.47% of the Mauritian group. The difference was statistically significant in the atypical squamous cells of uncertain significance (ASCUS) and atypical glandular cells of uncertain significance (AGUS) group. Conclusions: The prevalence of low-grade squamous intraepithelial lesions (LSIL) and high-grade squamous intraepithelial lesions (HSIL) is similar to that in the developed world.
|How to cite this article:|
Mulay K, Swain M, Patra S, Gowrishankar S. A comparative study of cervical smears in an urban Hospital in India and a population-based screening program in Mauritius.Indian J Pathol Microbiol 2009;52:34-37
|How to cite this URL:|
Mulay K, Swain M, Patra S, Gowrishankar S. A comparative study of cervical smears in an urban Hospital in India and a population-based screening program in Mauritius. Indian J Pathol Microbiol [serial online] 2009 [cited 2023 May 29 ];52:34-37
Available from: https://www.ijpmonline.org/text.asp?2009/52/1/34/44959
Cervical cancer is one of the leading cancers in women with an estimated 500,000 new cases every year, of which 80% occur in developing countries.  In India it is estimated, that the number of cases are over 140,000. 
The role of the pap smear as a cancer screening tool for the cervix has been substantiated by several studies in the last 50 years , and the method has resulted in falling incidence and mortality rates of cervical cancer in the developed world. ,, In India, a publicly funded regular cervical cancer screening program does not exist. Therefore, the data on the prevalence of cervical epithelial abnormalities in various populations in this country is not known. This study was initiated to analyse the findings on cervical smears of urban women in India, mostly from a higher socio-economic status, taken as part of a preventive health check-up and compare that data with data from cervical smears of women in Mauritius, taken as part of a National Cervical Cancer Screening program and compare this data with similar studies done in other parts of the world.
Materials and Methods
This study, conducted at the department of Anatomic Pathology and Cytology, included 16,010 cervico-vaginal smears. The Indian population formed one study group of 6,010 cervico-vaginal smears while the Mauritian population formed the other study group with 10,000 cervical smears.
Mauritius: The Mauritian study group comprised of 10,000 cervical smears from Mauritian women who participated in the National Screening program. These smears were sent to this hospital for screening in October 2002 and the reports were dispatched in sets and completed by February 2003. This was a populations screening with no selection of cases. The smears were taken by qualified gynecologists.
India: The Indian study group comprised of 6,010 cervico-vaginal smears from women who attended the hospital-based health check-up program between January 2003 and June 2004, which included cervical smear screening apart from other screening investigations. All smears were taken by trained gynecologists.
Selection criteria: There were no exclusion criteria in this study, so all 16,010 cases were included. The cases had either one or two smears. All the smears received in the period mentioned above were included in the study.
Specimen collection and handling: The samples from both the study groups were collected using Ayer's spatula or an endocervical brush. The smears were then fixed in alcohol and stained using the Papanicolaou's technique. The slides from Mauritius were labeled, fixed in alcohol and subsequently air-dried, packed in boxes and transported by air. The smears from both the groups were stained in the department. All the smears from both study groups were conventional cervico-vaginal smears.
Reporting: All the smears from both study groups were reported by pathologists with a minimum of 5 years experience in cytopathology using the 1991 Bethesda System. 
Analysis and comparison: The smears were categorized into different age groups and results compared for the adequacy of specimen, prevalence of normal smears, non specific infections, specific infections, other reactive changes and epithelial abnormalities.
The epithelial abnormalities were classified according to the 1991 Bethesda system  as atypical squamous cells of uncertain significance (ASCUS), atypical glandular cells of uncertain significance (AGUS), low-grade squamous intraepithelial lesion (LSIL), high-grade squamous intraepithelial lesion (HSIL), or invasive carcinoma.
Quality assurance: Every tenth case in both series was reviewed by a second pathologist and any difference in opinion was settled by a consensus opinion of a minimum of four pathologists. All cases with epithelial cell abnormalities were reviewed by a minimum of three pathologists.
Statistical analysis: The statistical significance, i.e., the P -value for each parameter in each of the age groups was calculated using the Chi-square test or the Fisher's test.
Ethical issues: There were no ethical issues involved in the study, as all the cases were cervico-vaginal smears taken for routine screening and appropriate diagnosis.
The results of the analysis are summarized in [Table 1],[Table 2],[Table 3],[Table 4], 84.4% of the smears were satisfactory according to the Bethesda system (TBS) in the Indian group and 43.79% in the Mauritian group. "Satisfactory but limited by" formed 14.85% and 55.5% of the Indian and Mauritius groups, respectively. Most of the latter were due to a non mention of the age of the women in the request form in the Mauritian group. A total of 0.73% of the smears were unsatisfactory in the Indian group and 1.16% of the smears were unsatisfactory in the Mauritian group.
Specific infections that included trichomonas, candida, bacterial vaginosis, herpes simplex virus (HSV), actinomycosis and mixed infections (a combination of two or more of the above infections) constituted 6.05% of the Indian group and 15.08% of the Mauritian group. This difference was statistically significant and the difference was striking in the groups with trichomonas, bacterial vaginosis and mixed infections [Table 2].
There was also a higher number of non specific inflammations in the Mauritian group (25.34%) as compared with the Indian group (19.61%).
The epithelial abnormalities (including ASCUS, AGUS, LSIL, HSIL and squamous cell carcinoma) constituted 1.392% of the Indian group and 0.47% of the Mauritian group [Table 3]. ASCUS formed the largest number with 0.64% and 0.26%, respectively. LSIL constituted 0.216% and 0.07%, respectively while HSIL was a lower number with 0.16% and 0.08%, respectively. Four cases of invasive cervical carcinoma in the Indian group and one case in the Mauritian group were also detected. The difference was statistically significant in the ASCUS and AGUS group.
The Republic of Mauritius is an island nation in the southwest Indian Ocean off the southeast coast of Africa with a population of a little over 1.3 million. The health system is a free public health service with four public health hospitals and eight private clinics. In recent years, the government has laid greater emphasis on health promotion and preventive medicine. In 2002, 10,000 women were screened and pap smears were taken; these smears were sent to the hospital in India for reporting.
The routine health check-up offered by the hospital includes a gynecologic examination and a pap smear among other tests. A total of 6,010 smears taken from consecutive women coming for this test (5350 cervical smears and 610 vaginal smears) between January 2003 and June 2004 were selected for this study. Only 44 smears (0.73%) of the smears from the Indian group were unsatisfactory contrasting with 116 (1.16%) from the Mauritian group. The proportion of inadequate smears in other similar studies have ranged from 0.2% to 5%. [9-13] It may be noted that in both groups, the smears were taken by trained gynecologists.
Non specific inflammation formed 19.6% and 25.34% of the smears in the Indian and Mauritian group, respectively. Studies in populations in rural Zimbabwe  and Pakistan  have observed inflammation in 37% and 59.3%, respectively. It is likely that the higher socio-economic status of the women in our study was responsible for the lower percentage. With reference to the detection of epithelial abnormalities, which is the main reason for advocating routine cervical smear examinations, the prevalence in studies around the world has shown a wide range from as low as 0.98%  to as high as 15.5%.  [Table 4] gives the details of these studies in various countries. No consistent pattern has emerged in these studies in the developed and developing countries. Hence, within countries such as the US, rates have ranged from 2.3 to 6.6%, , in the Middle East from 1.6% to 7.9%, ,,, in Israel from 0.98% to 4.41%, ,,, and in India from 1.87% to 5.9%. , The reasons for this could be many including criteria employed for diagnosis, the quality checks used, intrinsic differences in the population studied including prevalence of risk factors and the numbers studied which have ranged from as few as 419  to as large as 796, 337. 
The figure of 1.92% of epithelial abnormalities in the Indian group in this study is similar to that reported in the study from Gujarat, India  and the neighboring country of Pakistan.  The figure of 0.47% for the Mauritian group is among the lowest so far. The reasons for this low prevalence is not clear but it is unlikely to be a subjective error of interpretation as the same group of 4 pathologists similarly trained were involved in the reporting of all cervical smears in this study and also, a quality check of double-checking one in 10 smears and a consensus reporting of all abnormal smears was done.
A more detailed analysis showed that the biggest difference in the various studies is recorded in the ASCUS group where the prevalence ranged from 0.6% to 4.5%. This could be due to a subjective difference, where minor changes are probably not recorded because ASCUS had an overall low prevalence in the studies. ,,, It may also be mentioned that no cytotechnologists were employed in the initial screening of this study. The initial screening, reviews and comparisons were all done by trained pathologists with a minimum of 5 years experience in reporting routine pap smears. It is interesting that in the majority of the studies, including ours, HSIL formed less than 1% of the abnormal smears. Studies in a high-risk population in Zimbabwe and China with a high incidence of cervical cancer are those which have reported rates of HSIL as high as 3.7%. ,
Though cervical cancer is a leading cause of cancer related morbidity and mortality in India,  our hospital-based study of relatively affluent women shows a prevalence of LSIL and HSIL similar to that in the developed world. It is possible though that there could be invasive cervical cancer preceded by negative screening as occurred in high-risk Alaskan native women. 
Health Statistics in Mauritius are not available in published medical literature but from the above study it appears that though cervical inflammations are not uncommon, the prevalence of cervical epithelial abnormalities is low.
The study has shown a relatively low prevalence of epithelial abnormalities in cervical smears in the urban, relatively affluent population studied and in the population from Mauritius, representing a country between the developing and developed nations.
In comparison to similar studies in other parts of the world, the greatest difference was seen in the ASCUS group.
|1||Tristen C, Bergstrom S. Cancer in developing countries: A threat to reproductive health. Lakartidningen 1996;93:3374-6.|
|2||Juneja A, Sehgal A, Sharma S, Pandey A. Cervical cancer screening in India: Strategies revisited. Indian J Med Sci 2007;61:34-47.|
|3||Miller AB, Chamberlain J, Day NE, Hakama M, Prorok PC. Report on a workshop of the UICC project on Evaluation of Screening for Cancer. Int J Cancer 1990;46:761-9.|
|4||Walton RJ. The task force on cervical cancer screening programs. Can Med Assoc J 1976;114:981.|
|5||Hakama M, Rasanen-Virtanen U. Eftect of a mass screening program on the risk of cervical cancer. Am J Epidemiol 1976;103:512-7.|
|6||LγγrγE, Day NE, Hakama M. Trends in mortality from cervical cancer in the Nordic countries: Association with organized screening programs. Lancet 1987;1:1247-9.|
|7||Anderson GH, Boyes DA, Benedet JL, Le Riche JC, Matisic JP, Suen KC, et al . Organization and results of the cervical cytology screening program in British Columbia. 1955-85. Br Med J (Clin Res Ed) 1988;296:975-8.|
|8||Kurman RJ, Solomon D. The Bethesda system for reporting cervical/vaginal diagnosis. New York: Springer-Verlag 1994.|
|9||Pan Q, Belinson JL, Li L, Pretorius RG, Qiuo YL, Zhang WH, et al . A thin layer, liquid based pap test for mass screening in an area of China with high incidence of cervical carcinoma: A cross sectional, comparative study. Acta Cytol 2003;47:45-50.|
|10||Tuncer ZS, Basaran M, Sezgin Y, Firat P, Mocan Kuzey G. Clinical results of a split sample liquid based cytology (Thin Prep) study of 4,322 patients in a Turkish institution. Eur J Gynaecol Oncol 2005;26:646-8.|
|11||Kapila K, George SS, Al-Shaheen A, Al Ottibi MS, Pathan SK, Sheikh ZA, et al . Changing spectrum of squamous cell abnormalities observed on papanicolaou smears in Mubarak Al Kabeer Hospital, Kuwait, over a 13 year period. Med Princ Pract 2006;15:253-9.|
|12||Insinga RP, Glass AG, Rush BB. Diagnoses and outcomes in cervical cancer screening: A population based study. Am J Obstet Gynaec 2004;191;105-13.|
|13||Fonn S, Bloch B, Mabina M, Carpenter S, Cronje H, Maise C, et al . Prevalence of pre-cancerous lesions and cervical cancer in South-Africa: A multicentre study. S Afr Med J 2002;92:148-56.|
|14||Tbistle PJ, Chirenje ZM. Cervical cancer screening in a rural population of Zimbabwe. Cent Afr J Med 1997;43:246-51.|
|15||Wasti S, Ahmed W, Jafri A, Khan B, Sohail R, Hassan S. Analysis of cervical smears in a Muslim population. Ann Saudi Med 2004;24:189-92.|
|16||Sadan O, Schejter E, Ginath S, Bachar R, Boaz M, Menczer J, et al . Premalignant lesions of the uterine cervix in a large cohort of Israeli Jewish women. Arch Gynecol Obstet 2004;269:188-91.|
|17||Sadeghi SB, Hsieh EW, Gunn SW. Prevalence of cervical intraepithelial neoplasia in sexually active teenagers and young adults: Results of data analysis of mass papanicolau screening of 796, 337 women in the United States in 1981. Am J Obstet Gynecol 1984;148:726-9.|
|18||Daney DD, Woodhouse S, Styer P, Statsney J, Mody D. Atypical epithelial cells and specimen adequacy: Current laboratory practices of participants in the college of American Pathologists Inter laboratory comparison program in cervicovaginal cytology. Arch Pathol Lab Med 2000;124:203-11.|
|19||Jamal A, Al-Maghrabi JA. Profile of Pap smear cytology in Western region of Saudi Arabia. Saudi Med J 2003;24:1225-9.|
|20||Altaf FJ. Cervical cancer screening with pattern of pap smear. Review of multicenter studies. Saudi Med J 2006;27:1498-502. |
|21||Bar-Am A, Niv J, Yavetz H, Jaffa AJ, Peyser RM. Are Israeli women in a low risk group for developing squamous cell carcinoma of the uterine cervix? Acta Obstet Gynecol Scand 1995;74:472-7.|
|22||Baram A, Galon A, Schachter A. Premalignant lesions and microinvasive carcinoma of the cervix in Jewish women: An epedemiological study. Br J Obstet Gynecol 1985;92:4-8.|
|23||Suprun HZ, Schwartz J, Spira M. Cervical intraepithelial neoplasia and associated condylomatous lesions: A preliminary report on 4764 women from Northern Israel. Acta Cytol 1985;29:334-40.|
|24||Misra JS, Singh U. Results of long term hospital based cytological screening in asymptomatic women. Diagn Cytopathol 2006;34:184-7.|
|25||Patel TS, Bhullar C, Bansal R, Patel SM. Interpreting epithelial cell abnormalities detected during cervical smear screening: A cytohistologic approach. Eur J Gynaecol Oncol 2004;25:725-8.|
|26||National Cancer Registry Program. Annual Report. ICMR : New Delhi; 1990-1996.|
|27||Davidson M, Bulkow LR, Lanier AP, Smith RA, Hawkins I, Jensen H, et al . Incidence of invasive cervical cancer preceded by negative screening in high - risk Alaska Native women. Int J Epidemiol 1994;23:238-45.|
|28||Caprara L, Monari F, De Bianchi PS, Amadori A, Bondi A. ASCUS in screening. Pathologica 2001;93:645-50.|
|29||Robyr R, Nazeer S, Vassilakos P, Matute JC, Sando Z, Halle G, et al . Feasibility of cytology-based cervical cancer screening in rural: Cameroon. Acta Cytol 2002;46:1110-6.|
|30||Nance KV. Evolution of pap testing at a community hospital: A ten year experience. Diagn Cytopathol 2007;35:148-53.|