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Table of Contents
ORIGINAL ARTICLE
Year : 2020  |  Volume : 3  |  Issue : 4  |  Page : 692-697

The spectrum of cytologic patterns in cervical smears of a high-risk group: Retrospective analysis of a cancer detection camp experience


1 Department of Clinical Laboratory Services and Translational Research, Division of Pathology, Malabar Cancer Centre, Thalassery, Kerala, India
2 Department of Community Oncology, Malabar Cancer Centre, Thalassery, Kerala, India
3 Department of Cancer Registry and Epidemiology, Malabar Cancer Centre, Thalassery, Kerala, India

Date of Submission28-May-2020
Date of Decision27-Jul-2020
Date of Acceptance10-Sep-2020
Date of Web Publication25-Dec-2020

Correspondence Address:
Sangeetha Keloth Nayanar
Department of Clinical Laboratory Services and Translational Research, Division of Pathology, Malabar Cancer Centre, Thalassery, Kerala
India
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Source of Support: None, Conflict of Interest: None


DOI: 10.4103/CRST.CRST_213_20

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  Abstract 


Background: Cervical cancer is a major public health concern, especially among women in developing countries like India. The human papillomavirus (HPV) is a widely recognized etiological factor for cervical carcinogenesis. There is an increased risk of the development of cervical cancer among certain groups of women, particularly the sex workers due to high HPV exposure.
Objectives: This study was conducted to analyze the spectrum of epithelial cell abnormalities and the cytomorphology in the cervical smears of the high-risk groups of women in the North Malabar region of Kerala, India.
Materials and Methods: This retrospective study was conducted at the Malabar Cancer Center, in Thalassery, India, between December 2011 and December 2015. Women who attended the Early Cancer Detection Camps organized for high-risk groups were included in the study. Pap smears were collected from all the women to study the spectrum of changes in their cervical smears to determine a possible correlation between high-risk behaviors and the occurrence of precancerous lesions. Descriptive statistics were used to describe the qualitative variables and Chi-square test was used to determine the association between the abnormalities and demographic variables. A P < 0.05 was considered statistically significant.
Results: Out of 289 women enrolled in the study, 277 had satisfactory smears. The median age of the women was 40 years (range, 20–69 years), with majority (44%) in the age group of 30–39 years. Epithelial abnormalities were reported in 53 (19.1%) women. Nonspecific inflammation was observed in 56.6% of the women who were negative for intraepithelial lesion/malignancy (NILM), Candidiasis was seen in 13 (4.7%) women and bacterial vaginosis in 8 (2.9%). Younger women had a significantly higher number of epithelial abnormalities than older (P = 0.01). The highest prevalence of intraepithelial lesions was observed in women in the childbearing age group.
Conclusions: The high frequency of epithelial abnormalities emphasizes the need for cervical cancer awareness and prevention campaigns. Periodic cervical smear examination for these vulnerable groups could be a feasible option for the early detection of cervical cancer. The Pap smear test is a rapid, noninvasive, simple, low-cost, and effective diagnostic method for the early detection of cervical cancer in high-risk groups.

Keywords: Bethesda system, cervical cancer, cervical cytology, epithelial cell abnormalities, high-risk groups


How to cite this article:
Sahadevan Kanthimathy SD, Kizhakkebhagam NG, Aravind S, Parambil NA, Therayangalath B, Nayanar SK. The spectrum of cytologic patterns in cervical smears of a high-risk group: Retrospective analysis of a cancer detection camp experience. Cancer Res Stat Treat 2020;3:692-7

How to cite this URL:
Sahadevan Kanthimathy SD, Kizhakkebhagam NG, Aravind S, Parambil NA, Therayangalath B, Nayanar SK. The spectrum of cytologic patterns in cervical smears of a high-risk group: Retrospective analysis of a cancer detection camp experience. Cancer Res Stat Treat [serial online] 2020 [cited 2021 Jan 20];3:692-7. Available from: https://www.crstonline.com/text.asp?2020/3/4/692/304948




  Introduction Top


Invasive cancers of the cervix are preceded by cytomorphological changes in the cervical epithelium that can persist for many years.[1] Since the introduction of conventional cytology screening by George Papanicolaou in the late 1940s, a drastic reduction has been noticed in the incidence of and mortality due to invasive cervical cancers in many developed nations.[2] However, despite the fact that cervical cancer is now considered a preventable disease, it is still a major cause for cancer-related mortality among women in the Third World countries. According to GLOBOCAN 2018, there are over 5 lakh new cases of cervical cancer in different regions of the world, and nearly half of these are reported from Asia.[3] The human papillomavirus (HPV) is a known etiologic agent for the development of carcinoma of the cervix and is mainly transmitted by sexual contact.[4] About 90% of all HPV infections resolve within 2 years. However, the persistent infections lead to an increased risk of pre-cancerous lesions, thereby increasing the risk of development of invasive cancers, typically within 10–15 years. This time gap renders many opportunities for early detection.[5] The cervical smear test is a globally accepted screening procedure for the early detection of cervical cancer and its precursors. It has an excellent specificity of around 95% and a sensitivity of 44%–78%.[6] Ample training in smear collection, the use of Cervex-Brush, and newer techniques like liquid-based cytology (LBC) reduce the rate of unsatisfactory results.[7] Either a conventional pap smear or an LBC can be used to detect premalignant lesions from the cervix.[8]

Research has established that having multiple sexual partners can increase the risk of acquiring an HPV infection.[9],[10],[11] Therefore, certain high-risk groups such as female sex workers (FSWs) are at an increased risk of developing cervical malignancies, that are attributable not only to the high prevalence of the associated risk factors but also to the lack of effective screening measures. To the best of our knowledge, no trials for cervical cancer screening have been conducted among the FSWs in Kerala, a south Indian state. Therefore, the present study was conducted to explore the prevalence and cytomorphological features of both non-neoplastic and neoplastic lesions in the cervical smears of FSWs from the North Malabar region of Kerala.


  Materials and Methods Top


General study details

This is a retrospective analysis of the cervical smear reports of women who attended the community-based Early Cancer Detection Camps, conducted at the Malabar Cancer Center, a tertiary cancer center in Thalassery, India, between December 2011 and December 2015. The study was approved by the Institutional Review Board and Institutional Ethics Committee [Supplementary Appendix 1]. An informed consent was obtained from all participants prior to enrollment in the study. The study was conducted according to the various ethical principles as stated in the Declaration of Helsinki.

Participants

All consecutive FSWs who attended the camps during 4 years and for whom a Pap smear test was performed were included in the analysis. Cases with unsatisfactory smear reports were excluded. The smears were considered unsatisfactory if the number of squamous cells was inadequate, if most of the epithelial cells were obscured by blood or inflammatory debris, or in the presence of air-drying artefacts.

Variables

Our primary aim was to study the prevalence and characterize the spectrum of cytomorphologic features in the cervical smears of women with high-risk behaviors. The secondary objective was to evaluate for any correlation between the presence of epithelial abnormalities on cervical cytology and clinicodemographic features.

Study methodology

A series of camps were organized by the Division of Community Oncology of our tertiary care center as part of its cancer awareness and outreach programs and funded by local charitable societies. A few cases were screened as a part of a funded project with multicenter participation. The camps were set up on site, and the smears were collected by trained cytotechnologists using the conventional method for all the cases. For 166 cases, in addition to the conventional method, a smear was also collected using the LBC technique (Sure Path, BD Diagnostics). In the conventional method, smears were sampled with an Ayre spatula, spread on a glass slide, fixed in 95% isopropyl alcohol, and stained according to the standard Papanicolaou technique. For the LBC technique, samples were collected in preservative containing vials using the Cervex-Brush as per the manufacturer's instructions. Sure Path slides were prepared using the Prep Stain Slide Processor and stained using an automated stainer (BD Diagnostics-Tripath, Burlington, NC, USA). The smears were screened by cytotechnologists and verified by pathologists. The reports were generated according to the Bethesda 2001 guidelines for cases registered between 2011 and 2014 and according to Bethesda 2014 guidelines for the cases registered in 2015.

Data collection

Demographic data and clinical details were retrieved from the case files obtained from the Division of OncoPathology and the Department of Community Oncology of our institution. Relevant information including the age, details of the last menstrual period, signs and symptoms, per speculum findings, and cytology results were entered into a proforma for analysis.

Statistics

A sample size calculation was not performed for this study; we included all persons who fulfilled the inclusion and exclusion criteria within the study period. The statistical software, IBM SPSS Statistics for Windows, Version 20.0. Armonk, NY, USA: IBM Corp., was used for statistical analysis. Descriptive statistical methods such as frequencies and percentages were used for qualitative variables, and the Chi-square test was used to determine the relation between cytological abnormalities and demographic variables.


  Results Top


Between December 2011 and December 2015, Pap smears were collected from a total of 289 consecutive women from the high-risk groups for cytological examination. In 12 (4.15%) women, the smears were unsatisfactory and hence they were excluded from the analysis. Thus, 277 (95.84%) women, in whom the smears were satisfactory as per the definition, were included in the analysis [Figure 1]. The cytological interpretation of their smears is summarized in [Table 1]. The human immunodeficiency virus (HIV) status of the study cohort was not known, and screening tests for HIV were not performed as a part of this study.
Figure 1: Flow diagram of the retrospective analysis of the cervical smears of female sex workers who underwent cytologic screening at community screening camps in Thalassery, India

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Table 1: Cytologic interpretation of the cervical smears of female sex workers who underwent cytologic screening at community screening camps in Thalassery, India (n=277)

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The median age of our study cohort was 40 years (range: 20–69 years). The majority of the women (44%) were in the age group of 30–39 years [Table 2]. Out of 277 women, 40 (35%) had multiple complaints such as leukorrhea, itching, abdominal pain, lower abdominal pain, and vaginal burning [Figure 2]. However, of the 53 women with reported epithelial abnormalities, 30 (56%) had various clinical symptoms.
Table 2: Cytologic spectrum of non-neoplastic and neoplastic lesions in the different age groups of female sex workers who underwent cytologic screening at community screening camps in Thalassery, India

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Figure 2: Distribution of symptoms in the study to evaluate the pattern of cytologic abnormalities in female sex workers who underwent cytologic screening at community screening camps in Thalassery, India

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Epithelial abnormalities were reported in a total of 53 (19.1%) women, of which 30 (10.8%) had atypical squamous cells of undetermined significance (ASCUS), 9 (3.2%) had high-grade squamous intraepithelial lesions (HSILs), and 2 (0.7%) had atypical glandular cells-not otherwise specified (AGC-NOS).

Among those who were negative for intraepithelial lesion/malignancy (NILM), the majority (56%) showed non-specific inflammatory changes with features such as squamous epithelial cells with focal cytoplasmic vacuolation, mild karyomegaly, margination of chromatin, and plenty of polymorphonuclear leukocytes in the background [Figure 3]a. There were 13 women with candidiasis (4.7%) and 8 with bacterial vaginosis (2.9%).
Figure 3: A panel of microphotographs of cervical lesions: (a) inflammatory smear (liquid based cytology Pap smear, ×40); (b) liquid-based cytology smear showing bacterial vaginosis (Pap, ×100); (c) low-grade squamous intraepithelial lesion depicting koilocytes (Pap, ×400); (d) high-grade squamous intraepithelial lesion (Pap, ×400)

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Women with per speculum examination signs such as discharge, bulky and hypertrophied cervix, and erosion and bleeding on touch were considered to have an unhealthy cervix. Of the 139 women with an unhealthy cervix based on the per speculum findings, 34 had epithelial abnormalities (P = 0.024). Of these, 17 women had ASCUS, 9 had HSIL, and 8 had low-grade squamous intraepithelial lesions (LSILs).

A comparative analysis of the age groups based on the presence of epithelial abnormalities showed that women belonging to the younger age groups had a significantly higher number of epithelial abnormalities than those belonging to the older age groups, and the difference was statistically significant (P = 0.01).

The cases with epithelial abnormalities were managed according to the institutional protocols. Women with ASCUS and LSIL were advised to repeat the Pap smear after 6 months, and if positive for similar findings to undergo the loop electrosurgical excision procedure. Those with ASC-H and HSIL were advised colposcopic biopsy for confirmation and if confirmed by biopsy were advised a hysterectomy.

A histopathologic correlation was available for 11 cases. Out of the seven cases of HSIL on cytology, two were reported as squamous cell carcinomas, three as cervical intraepithelial neoplasia (CIN) III, one as CIN II, and one as hyperplastic stratified squamous epithelium. Out of three cases of ASC-H on cytology, one was reported as CIN II on biopsy and the remaining two as chronic cervicitis, one with and the other without squamous metaplasia.


  Discussion Top


In our study, evaluating the cervical smears of 277 FSWs who attended the community-based Early Cancer Detection Camps, we found that more than half of the screened smears showed evidence of inflammation. Out of 139 women who were considered to have an unhealthy cervix, 34 had epithelial abnormalities (P = 0.024). There was a high prevalence of epithelial abnormalities in women aged<39 years (P = 0.01). The most common abnormality was ASCUS, which was observed in 30 (10%) women. There was not a single case of invasive malignancy, but HSIL was detected in nine (3.2%) smears. To the best of our knowledge, ours is the first study to assess the spectrum of changes in the cervical smears of women with high-risk behaviors in the rural setting in India.

Similar findings have been reported by other researchers. [Table 3] shows an overview of the results from various studies including ours. Singh et al. showed that FSWs had a higher incidence of inflammatory changes than the healthy controls (51.7% vs. 34.7%).[12] Similarly, Patel et al. reported the presence of inflammatory features on the smears of 57.5% of the women who had complaints such as vaginal discharge and bleeding per vagina.[13] Candidiasis comprised the majority of the vaginal infections (4.6%). It is known to induce mucosal swelling, eczema, and cell exfoliation.[14] Vafaei et al. and Madan et al. reported the incidence of candidiasis to be 3.5% in sex workers and 2.5% in the HIV-positive women, respectively.[15],[16] Hitherto, there are no studies that provide a conclusive evidence for the association between vaginal mycosis and an increased risk of CIN.[17] Bacterial vaginosis is one of the most common vaginal imbalances that occur during the reproductive age of a woman.[18] We reported a 2.9% incidence of bacterial vaginosis, characterized by the presence of “clue cells” in the smears [Figure 3]b. Gillet et al. have reported an apparent association between bacterial vaginosis and cervical HPV infection.[19] In our study, we observed one case of bacterial vaginosis that was associated with ASCUS and another with AGC-NOS. Surprisingly, there were no cases of infection with trichomonas vaginalis on cytology.
Table 3: Comparison of the other studies performed to evaluate the epithelial abnormalities detected by cervical cytological examinations in high-risk groups with the present study

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In our study, the prevalence of cervical epithelial cell abnormalities was 19.1%, which is similar to that reported by Vafaei et al. (16.5%) and Leung et al. (12.46%).[5],[15] The most frequently observed pattern of epithelial abnormalities was ASCUS (10.8%), and similar findings have been reported by Manghani et al. and Leung et al.[5],[20] Atypical squamous cells, in the presence of which high-grade intraepithelial lesions cannot be excluded (ASC-H) were observed in 1.4% of the cases in our study; these findings are comparable to those reported by Jha et al. (0.73%) and Madan et al., (1.68%) in HIV-positive women.[16],[21] The incidence of LSIL was 2.9%, which is in agreement with the incidence observed in the study by Jha et al.[21] Koilocytes along with squamous pearls depicting the pathognomonic effect of HPV infection were seen in four out of eight cases of LSIL [Figure 3]c. We found cytological changes suggestive of HSIL in nine (3.2%) cases. Such smears showed clusters and singly scattered squamous cells with a high nuclear-to-cytoplasmic ratio, hyperchromatic nucleus, marked pleomorphism with coarse or granular chromatin, and scant to moderate cytoplasm [Figure 3]d. Madan et al. and Chakravarty et al. in their studies have shown that the high prevalence of HPV and HIV among FSWs resulted in a high rate of cervical epithelial cell abnormalities.[16],[22],[23] Only two cases of AGC-NOS (0.7%) were observed in our study, which is similar to the findings from the study by Devi and Priya (0.8%).[24] Cytological abnormalities were more common among the HPV-positive FSWs than HPV-negative ones (54.3% vs. 20%).[25]

Biopsy is the gold standard for the validation of the abnormalities detected in cervical smears.[26] We had 11 cervical biopsies available for histologic correlation. Agreement between biopsy and cervical smears was observed in six cases of HSIL, with one case being false-positive on cytologic screening. This biopsy discordant case was possibly over diagnosed on cytology due to low cellularity, hemorrhagic background, or air-drying artefacts.

Various studies have suggested that the Pap smear test is one of the most cost-effective options for screening and the availability of trained personnel such as cytotechnologists and cytotechnicians is an added asset to the cervical cancer prevention and screening strategies.

Our study had a few limitations. First, our sample size was small. This is attributable to factors such as social stigma and the inhibition experienced by the subjects during the recruitment process. Second, as our study cohort comprised women who participated in the screening campaign, demographic data were limited to routinely collected information at the time of screening. Therefore, confounding risk factors such as smoking and alcohol consumption were not assessed. Finally, molecular assays for the detection of high-risk strains of HPV in the LBC samples were not performed due to financial constraints.


  Conclusions Top


The findings from our study depict a panoramic image of a positive correlation between women with high-risk behavior and the rate of occurrence of precancerous lesions. The high frequency of lesions highlights the need for more awareness and prevention campaigns for cervical cancer. The provision of performing periodic examinations and prompt follow-up is essential. Policies can be devised for low-cost cervical cytology screening programs with technical assistance from non-governmental organizations. We also advocate testing for HPV DNA, primarily because the actual incidence of HPV infection may be significantly higher than that estimated from cytological abnormalities. These measures can go a long way in reducing the morbidity and mortality in the high-risk group as well as in the general population.

Financial support and sponsorship

Nil.

Conflicts of interest

There are no conflicts of interest.


  Supplementary Appendix Top


Supplementary Appendix 1: IEC approved protocol

Spectrum of cervical cytologic patterns in high-risk groups: Experience from early cancer detection camps by a cancer center in north Malabar region of South India

Sabna Dev Sahadevan Kanthimathy, Nimi G. Kizhakkebhagam, Sithara Aravind, Neethu Ambali Parambil1, Bindu Therayangalath2, Sangeetha Keloth Nayanar

Department of Clinical Laboratory Services and Translational Research, Division of Pathology, Departments of1 Community Oncology and2 Cancer Registry and Epidemiology, Malabar Cancer Centre, Thalassery, Kerala, India

Keywords: Cervical cancer, human papilloma virus, pap smear


  Introduction Top


Cervical cancer is a leading cause of cancer mortality among women in developing countries. It kills around 72000 women annually in India, accounting for nearly one-third of the global cancer deaths.[1] Persistent infection with oncogenic human papilloma virus (HPV) is a well-established risk factor for invasive cervical carcinoma.[2] Meta-analysis carried out on the correlation between HIV, HPV, and squamous intraepithelial lesion have shown that HIV infected women have a higher prevalence of HPV infection and cervical intraepithelial neoplasia that tend to increase in proportion with the degree of immunodeficiency.[3] Hence, high-risk groups like female sex workers have an increased risk of developing cervical carcinoma when compared to others. The identification of precancerous lesions in cervical screening programs is primarily and successfully done by cytologic screening with PAP Test.[4] Our study intends to explore the prevalence rate and cytomorphology of nonneoplastic and neoplastic findings in cervical smears in high-risk groups.

Aims and objectives

  • To determine the prevalence and patterns of the cytologic lesions in cervical smears of high-risk groups
  • To correlate cytologic findings with histopathologic features wherever available.



  Materials and Methods Top


  • Study design: Retrospective descriptive study
  • Study population: December 2011 to December 2015
  • Study period: March 2012 to July 2012
  • Study sample: Cervical samples collected through Early Cancer Detection Camps for high–risk groups (female sex workers). Expected sample size: Around 350 cases
  • Study place: Division of Oncopathology in Malabar Cancer Centre
  • Demographic data and clinical details: From patients requisition forms archived in the Departments of Community Oncology and Oncopathology
  • Cytological evaluation: All samples were taken by conventional Pap smear collection method and liquid-based cytology technique was also done in around 50%. All nonneoplastic and neoplastic lesions will be included and reported according to Bethesda System 2001
  • Histopathological evaluation: High-grade lesions in pap test will be correlated with corresponding biopsy reports wherever available.


Statistical analysis

  1. Prevalence of cervical lesions will be calculated
  2. Chi-square test will be used to compare determine the statistical significance of the parameters.



  Expected Results Top


Prevalence rate of infections and epithelial abnormalities will be higher in the high-risk groups.


  References Top


  1. Kaarthigeyan K. Cervical cancer in India and HPV vaccination. Indian J Med Paediatr Oncol 2012;337-12.
  2. McGraw SL, Ferrante JM. Update on prevention and screening of cervical cancer. World J Clin Oncol 2014;5744-52.
  3. Madeddu G, Mameli G, Capobianco G, Babudieri S, Maida I, Bagella P, et al. HPV infection in HIV-positive females The need for cervical cancer screening including HPV-DNA detection despite successful HAART. Eur Rev Med Pharmacol Sci 2014;181277-85.
  4. Cristina Aparecida T.S. Mitteldorf. Cervical cancer screenihg: From Pap smear to future strategies. J Bras Patol Med Lab 2016;52.




 
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McGraw SL, Ferrante JM. Update on prevention and screening of cervical cancer. World J Clin Oncol 2014;5:744-52.  Back to cited text no. 4
    
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Leung KM, Yeoh GP, Cheung HN, Fong FY, Chan KW. Prevalence of abnormal Papanicolaou smears in female sex workers in Hong Kong. Hong Kong Med J 2013;19:203-6.  Back to cited text no. 5
    
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    Figures

  [Figure 1], [Figure 2], [Figure 3]
 
 
    Tables

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