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  Table of Contents  
ORIGINAL ARTICLE
Year : 2014  |  Volume : 51  |  Issue : 2  |  Page : 124-128
 

A comparative study of cervical cancer screening methods in a rural community setting of North India


Departments of Epidemiology and Biostatistics and Cyto Pathology, Institute of Cytology and Preventive Oncology, Noida, Uttar Pradesh, India

Date of Web Publication7-Aug-2014

Correspondence Address:
S Asthana
Departments of Epidemiology and Biostatistics and Cyto Pathology, Institute of Cytology and Preventive Oncology, Noida, Uttar Pradesh
India
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Source of Support: Supported by grant from Indian Council of Medical Research under funding IRIS No. 3390., Conflict of Interest: None


DOI: 10.4103/0019-509X.138172

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 » Abstract 

Context: Pap smear testing as a conventional cervical screening approach has limitations for implementation and aided visual cervical testing has varying results in different regions. Aims: The aim of this study is to demonstrate the performance of aided visual cervical screening tests as against conventional Pap smear testing in a rural community setting of North India. Settings and Design: This was a rural community based cross-sectional study. Materials and Methods: All 7603 ever married women of age 30-59 years surveyed in a pocket of Dadri Tehsil, Uttar Pradesh, India were targeted for screening by Pap, visual inspection of cervix using acetic acid (VIA) and visual inspection of cervix using Lugol's iodine (VILI) methods. Screen positives were referred to colposcopy and confirmation by histology. Statistical Analysis Used: Detection of histological cervical intraepithelial neoplasia (CIN) II + and CIN III + assessed separately by sensitivity, specificity and likelihood ratio's and predictive values. Analysis of data was performed by using IBM SPSS statstics software version 16.0. Results: A total of 65.6%(4988/7604) eligible women of 30-59 years age group in the target population were screened. Out of 4988, further analysis was performed on 4148 after excluding those who did not complete all screenings, who lost to follow-up and had missing histology results. Screen positivity rates by Pap (ASCUS and above), VIA and VILI were 2.6%, 9.7% and 13.5% respectively. Sensitivity and specificity of detecting the CIN III+ lesions were 87.5 and 98.8% for Pap, 50.0% and 96.7% for VIA and 50.0% and 95.7% for VILI respectively. Conclusions: VIA screening demonstrated as a feasible primary screening test for detecting high grade CIN and as to perform better when the Pap test is not feasible.


Keywords: Cervical cancer screening, cytology, rural community, visual inspection of cervix using acetic acid


How to cite this article:
Satyanarayana L, Asthana S, Bhambani S, Sodhani P, Gupta S. A comparative study of cervical cancer screening methods in a rural community setting of North India. Indian J Cancer 2014;51:124-8

How to cite this URL:
Satyanarayana L, Asthana S, Bhambani S, Sodhani P, Gupta S. A comparative study of cervical cancer screening methods in a rural community setting of North India. Indian J Cancer [serial online] 2014 [cited 2019 Aug 21];51:124-8. Available from: http://www.indianjcancer.com/text.asp?2014/51/2/124/138172



 » Introduction Top


Cancer of the uterine cervix is leading cancer in India. In different regions of India highest risks among women were observed for breast cancer followed by cervical cancer and gall bladder cancer with a cumulative risk of one in 35, one in 61 and one in 123 likely develop the cancer of the respective site in their life-time. [1] The estimated 134,420 new cases of cervical cancer that was a one-fourth load of total cancer cases for the year 2008 in India. [2] A review study observed cervical cancer is relatively neglected disease in terms of advocacy and indicated cytology, human papilloma virus (HPV) testing, visual inspection of cervix using acetic acid (VIA) and visual inspection of cervix using Lugol's iodine (VILI) are known to be accurate and effective methods to detect cervical intraepithelial neoplasia (CIN) or cervical cancer and could contribute to the reduction of disease in low resource setting. [3] Another review on the subject from India stated that cervical screening by VIA or VILI is acceptable alternative for low resource setting. [4] A cluster randomized control trial (RCT) conducted at Osmanabad district in India [5] demonstrated VIA as a useful alternative with careful monitoring and HPV testing and cytology was similar in detection rates despite heavy investments.

A RCT conducted in south India showed VIA screening as an effective method to prevent cervical cancer in developing country. [6] A pooled analysis of 11 studies from Africa and India showed the possibility of over diagnosis of CIN II + with overestimated sensitivity and specificity of VIA and VILI. [7] A cluster (RCT) from Osmanabad District observed no significant reduction of advanced cancer or deaths in Pap screening and VIA screening groups as compare to control group. [8] Various studies on evaluation and feasibility of cervical screening methods from different low resource regions are still on progress and continue to be reported. There are several studies in recent 5 years reported on evaluation of various screening methods including VIA and cytology. [9],[10],[11],[12],[13],[14],[15],[16] As there was no large scale cervical cancer screening demonstration in the region of rural Uttar Pradesh, a study was initiated in the year 2009 with an aim to evaluate the demonstration of aided visual tests in a rural setting. Thus the present study reports screening demonstration results of VIA and VILI tests for detection of high CIN in comparison with conventional Pap testing.


 » Materials and Methods Top


The selected study area of a tehsil of Gautham Budha Nagar District (UP) had a population of 1.5 lacs covered by community health center (CHC), along with the attached four primary health centers (PHC) with their 34 sub-centers. The estimated population of the selected 36 villages covered under the project was 75000. Eligible women between 30 and 60 years age were enumerated by a base-line survey. All the eligible target group women were invited for screening and no further selection of women was done. Most of the screening centers were established at PHC and sub centers or at a convenient place. Exclusion criterion was women who had undergone a total hysterectomy and previously diagnosed with cancer or pre-cancer. Women who were menstruating at the time of the study visit were excluded temporarily. Pregnant women were eligible to participate in study 12 weeks after the end of pregnancy. The Duration of the study was 3 years from November 2009 to July 2012.

Motivation of eligible women was done by auxiliary nurse midwives (ANMs) and Accredited Social Health Activist (ASHAs) through community group talks and personal communication with the help of health education material. Flip chart, handouts and posters were the material. Project staffs and community health workers were trained to use that material. Motivational training was imparted for ASHA's and social workers through workshops. Women who came to screening center were again counseled and explained about the procedure of screening, informed consent was taken and screening pro forma was filled up. Screening was done by different modes viz., Pap, VIA and VILI in sequence. Any screened women detected as positive was referred to CHC for colposcopic examination and biopsy collection for confirmation of diagnosis. The details of women contained in proforma were women's name, age, address, socio-demographic and screen result etc.

Visual inspection of the cervix after applying 5% acetic acid was done with a cotton swab on the cervix and by allowing sufficient time (1 min) to see for color change on transformation zone. VIA is considered to be positive if it became conspicuous with white color against the pinkish background of normal epithelium others and else considered to be negative. VILI is similar to VIA except the application of Lugol's iodine instead of acetic acid. VILI is considered positive if yellow iodine non-uptake areas were visualized close to the squamocolumnar junction or a growth on the cervix turned yellow. In a normal cervix, normal Squamous epithelium will be strongly stained as mahogany brown due to iodine uptake. However, the columnar epithelium of central endocervical areas does not take the iodine stain and remain pale. [17] Bethesda system was followed for cytology in reading Pap smear [18] Women with a report of ASCUS or more were considered to be positive and referred for colposcopy-directed biopsy.

Woman found to be screen positive by aided visual test was informed about the test immediately with brief counseling. A card (referral card) was issued to her and asked to report at CHC for colposcopy. Women with negative VIA and VILI result were asked to come back at the center to collect pap report after 15 days. Report was distributed to women by our project staff or by ASHA's or ANMs of the area depending on availability and convenience in case they failed to return to collect the report. Withdrawal of participants at any stage during the study was monitored and withdrawal reason was noted. Colposcopy directed biopsy was taken wherever necessary. The biopsy samples sent to cytopathology for diagnosis. The treatment of precancerous lesions was done as per IARC guidelines. [18] CIN I cases were treated with cryotherapy where eligible at CHC by doctor else referred to tertiary care hospital for surgical procedures and radiotherapy.

Statistical analysis

The formulae used for computation of test characteristics for VIA VILI and cytology are as follows:

  • Sensitivity = true positives/disease +
  • Specificity = true negatives/disease −ve
  • Positive predictive value = true +/test +
  • Negative predictive value = true -/test -
  • The likelihood ratio positive (LR+) is calculated
  • The likelihood ratio negative (LR-) is calculated.


Detection of histological CIN II + and CIN III + assessed separately by sensitivity, specificity and likelihood ratio's and predictive values. Analysis of data was performed by using SPSS software version 16.0.


 » Results Top


Nearly 65.6% (4988/7604) eligible women surveyed reported at screening center. The response rate for all the age group was good, i.e., at least about 60% or more. [Figure 1] shows the flow chart of cervical screening by VIA, VILI and Pap test along with the outcome of confirmatory diagnosis.
Figure 1: Cervical screening by visual inspection of cervix using acetic acid, visual inspection of cervix using Lugol's iodine and PapaNacolau test along with outcome of confirmatory diagnosis

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Socio-demographic information of screened women is given in [Table 1]. Of the total women, 63.2% were illiterate and 23.9% were having primary education. About 13% women had education up to high school and above. Ever married and widowed women were 92.7% and 2.8% respectively. Most women (90.9%) screened were Hindu and the rest were Muslim and others communities. Around 78% (3908) women were pre-menopausal and rest 1080 (21.6%) post-menopausal, 69.0% of women had normal menstrual cycle and 12% women had irregular menstrual cycles.
Table 1: Socio demographic information of screened women

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Distribution of clinical symptoms and signs are presented in [Table 2]. Only 16.9% women were asymptomatic. The common presenting symptom was abnormal vaginal discharge and present in 60% women followed by 36.5% lower abdominal pain and 22% backache. Few women (0.6%) presented with post coital bleeding. On per speculum vaginal examination by ANM, 50.0% women had normal looking cervix. Cervical erosion was present in 38.8% women, whereas hypertrophy of cervix in 25.5% of women. Two women were found with suspicious for malignancy. The percent screen positivity for VIA, VILI and Pap was 9.7, 13.5 and 2.6 respectively.
Table 2: Clinical (Gynae) symptoms and signs present in screened women

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After excluding those who did not complete all screenings, who lost to follow-up and had missing histology results the sample size arrived at 4198 from 4988. Further analysis is performed on data of 4198 women screened. [Table 3] shows percent positivity of VIA, VILI and Pap by severity of histological diagnosis. The detection rates for CIN I and CIN II by VIA and VILI were higher than Pap while the detection rate for CIN III was 100% for Pap. [Table 4] and [Table 5] depict clinical performance with the help of sensitivity, specificity, predictive values and likelihood ratios for VIA, VILI and Pap screening tests for detecting CIN II + and CIN III + respectively. Sensitivity of all the three screening tests was comparable with little lower for VIA in the detection of CIN II +. Sensitivity was highest (87.5%) for Pap followed by VIA (50.0%) and VILI (50.0%) for CIN III + detection. Very high specificity was observed for all the three tests. Positive predictive values were highest for Pap and lower for VIA and VILI respectively.
Table 3: Percent positivity of VIA, VILI and Pap by severity of histological diagnosis

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Table 4: Performance of various screening modalities for detecting CIN-II+

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{Table 5}


 » Discussion Top


VIA screening demonstrated as a sole feasible primary screening test due to non-feasibility of Pap and HPV tests for detecting CIN though there was an expected sacrifice of missed cases due to VIA screening. Better performance of Pap was observed in our study as compared to other studies. In a study of accuracy of five cervical cancer screening tests assessed in eleven studies in Africa and India in a pooled analysis showed lowest sensitivity (57%) for Pap test in the detection of CIN II + but specificity (93%) was high. [7] Our Pap results were not blinded with other screening test results and in addition the Pap smear reading was done by senior pathologists in our setup. The pooled analysis showed sensitivity of VIA was higher (79% and 83%) for the outcomes of CIN II + and CIN III + respectively when compared with the present study.

There are varying screen positivity rates across the different studies. In a cross-sectional study at Angola, 8851 women screened positivity rates for VIA and VILI found to be 6.6 and 32% respectively. [19] Another study conducted on 5519 Indian rural women aged 30-49 years positivity for VIA, VILI and Pap was found to be 16.9%, 15.65 and 6.1% respectively. [20] In a cross-sectional study on 10378 women at Tanzania low positivity rates were found 3.8% for VIA and 4.8% for VILI. [21] VIA positivity rate varied in the different countries of Africa in a demonstration project observed from as high as 28.0% in Zambia to as low as 5.7% in Nigeria with an overall average VIA positivity of 10.1%. [22] In a population-based cervical screening in Mongolia, 2009 women underwent both VIA and Pap tests. VIA was abnormal in 254 (12.6%); Pap smear showed atypical squamous cells of undetermined significance or worse in 3%. [23] In a cross-sectional study among 4957 women of Columbia, positivity rates were 1.3% and 4.3% for HSIL and LSIL in cytology, 7.4% for VIA and 10.1% for VIA-VILI. [24] In a large population based RCT at Tamil Nadu, India, total screen positivity by VIA was found to be 9.9%. [6] In 42 villages of Andhra Pradesh among 2295 women screened VIA positivity was 12.9%, whereas Pap positivity was 14.7%. This pap positivity is unusually high. [25] In our study, VIA and VILI positivity are 9.5% and 13.2% respectively with a very low rate of 2.6% for Pap test.

The test characteristics of various screening modes are well-documented, but there are variations in the performance of tests. In a study of concurrent evaluation of visual and cytology screening in rural India, sensitivity of VIA, VILI and cytology to detect high grade CIN were 64.5%, 64.5% and 67.7% respectively, specificity were 84.2, 85.5 and 95.4 respectively. [20] Present study showed 59% sensitivity for VIA, lower than VILI but more specific. This lower pickup might be due to lower case detection rate as such in our rural community. In a community based study at Angola, sensitivity and specificity for VIA 70.7% and 94.5% and for VILI 88.0% and 68.9% respectively. [19] In a study at Tanzania, sensitivity for VIA and VILI were 60.6 and 93.4% respectively, specificity for VIA and VILI were 98.2% and 97.3% respectively. [21] The estimated sensitivity and specificity were 81.3% and 87.3% respectively for VIA, 91.5% and 86.9% for VILI and 92.9% and 83.5% for the combined test. [26] A recent study of the effectiveness of VIA and VILI in 1 time and annual follow up screening in rural china detected half of CIN II cases and most CIN III + cases and 1 year follow-up of CIN I lesion also detected significant number of CIN II lesion at the end of 1 year. [27] A study on providing updated estimation of accuracy of VIA based on meta-analysis reported an 80% sensitivity (range 79-82%) and a 92% specificity (range 91%-92%) and positive predictive value of 10% (range: 9-10%). [28]

A cluster randomized controlled trial demonstrated the importance of visual method (VIA) with high screening participation rates, good compliance for clinical management and significant down staging. [29] A recent report indicated that the realistic sensitivity of a quality assured single visual inspection with acetic acid is around 50% and is associated with a 25-35% reduction in cervical cancer incidence and the frequency of cervical intraepithelial neoplasia grade 2 or worse lesions in randomized controlled trials. [30] The present study in a realistic rural community demonstration the observed sensitivity was low. In the absence of HPV screening due to cost consideration and cytology being not practical to implement universal screening, VIA screening implementation to reduce the burden of the disease is the currently available alternative in low resource settings. VIA screening demonstrated as a feasible primary screening test for detecting high grade CIN in a north Indian rural community. The implementation of visual screening at district level is likely to reduce the burden of disease to some extent. In India, Tamil Nadu government has already initiated district level VIA and VILI screening on a pilot basis to demonstrate that VIA/VILI is an appropriate cost-effective screening tool in low resource settings. The pilot program was demonstrated to be conducive for scaling up across the state. [31] In the long run implementation of VIA screening can reduce the incidence of the disease.


 » Acknowledgments Top


We thank Dr. BC Das, Ex-director, Dr. A Sehgal Ex-director-in-charge, Dr. Ravi Mehrotra Director, ICPO for their administrative support and also thank Dr. Veena Singh for aided visual training to the project staff and Dr S. Batra, LNH Delhi and Dr G K Rath AIIMS, Delhi from collaborating hospitals and MS, community health center, Dadri.

 
 » References Top

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10.Li R, Zhou Q, Li M, Tong SM, He M, Qiu H, et al. Evaluation of visual inspection as the primary screening method in a four-year cervical (pre-) cancer screening program in rural China. Trop Doct 2013;43:96-9.  Back to cited text no. 10
    
11.Dasgupta S, Bhattacharya S. Is visual inspection with acetic acid better than cervical cytology to screen women ≥40 years of age for carcinoma cervix? A cross-sectional study on proportion of screen-positive women (by VIA and cervical cytology) having CIN II/III lesion on cervical biopsy: Difference between two age groups and among screening methods. Arch Gynecol Obstet 2012;285:1731-6.  Back to cited text no. 11
    
12.Consul S, Agrawal A, Sharma H, Bansal A, Gutch M, Jain N. Comparative study of effectiveness of Pap smear versus visual inspection with acetic acid and visual inspection with Lugol′s iodine for mass screening of premalignant and malignant lesion of cervix. Indian J Med Paediatr Oncol 2012;33:161-5.  Back to cited text no. 12
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15.Sahasrabuddhe VV, Bhosale RA, Kavatkar AN, Nagwanshi CA, Joshi SN, Jenkins CA, et al. Comparison of visual inspection with acetic acid and cervical cytology to detect high-grade cervical neoplasia among HIV-infected women in India. Int J Cancer 2012;130:234-40.  Back to cited text no. 15
    
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18.Sellors JW, Sankaranarayanan R. Colposcopy and treatment of cervical intraepithelial neoplasia: A beginners′ manual. Lyon, France: IARC Press, 2003.  Back to cited text no. 18
    
19.Muwonge R, Manuel Mda G, Filipe AP, Dumas JB, Frank MR, Sankaranarayanan R. Visual screening for early detection of cervical neoplasia in Angola. Int J Gynaecol Obstet 2010;111:68-72.  Back to cited text no. 19
    
20.Deodhar K, Sankaranarayanan R, Jayant K, Jeronimo J, Thorat R, Hingmire S, et al. Accuracy of concurrent visual and cytology screening in detecting cervical cancer precursors in rural India. Int J Cancer 2012;131:E954-62.  Back to cited text no. 20
    
21.Ngoma T, Muwonge R, Mwaiselage J, Kawegere J, Bukori P, Sankaranarayanan R. Evaluation of cervical visual inspection screening in Dar es Salaam, Tanzania. Int J Gynaecol Obstet 2010;109:100-4.  Back to cited text no. 21
    
22.Prevention of cervical cancer through screening using visual inspection with acitic acid (VIA) and treatment with cryo therapy. A demonstration project in six African countries (Malawi, Madagascar, Nigeria, Uganda, The United Republic of Tanzania and Zambia). Available from: http://www.who.int/reproductive-health/publications/cervical_cancer_gep/index.htm. [Last accessed on 2013 May 7].  Back to cited text no. 22
    
23.Elit L, Baigal G, Tan J, Munkhtaivan A. Assessment of 2 cervical screening methods in Mongolia: Cervical cytology and visual inspection with acetic acid. J Low Genit Tract Dis 2006;10:83-8.  Back to cited text no. 23
    
24.Murillo R, Luna J, Gamboa O, Osorio E, Bonilla J, Cendales R, et al. Cervical cancer screening with naked-eye visual inspection in Colombia. Int J Gynaecol Obstet 2010;109:230-4.  Back to cited text no. 24
    
25.Gravitt PE, Paul P, Katki HA, Vendantham H, Ramakrishna G, Sudula M, et al. Effectiveness of VIA, Pap, and HPV DNA testing in a cervical cancer screening program in a peri-urban community in Andhra Pradesh, India. PLoS One 2010;5:e13711.  Back to cited text no. 25
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26.Muwonge R, Walter SD, Wesley RS, Basu P, Shastri SS, Thara S, et al. Assessing the gain in diagnostic performance when two visual inspection methods are combined for cervical cancer prevention. J Med Screen 2007;14:144-50.  Back to cited text no. 26
    
27.Li R, Lewkowitz AK, Zhao FH, Zhou Q, Hu SY, Qiu H, et al. Analysis of the effectiveness of visual inspection with acetic acid/Lugol′s iodine in one-time and annual follow-up screening in rural China. Arch Gynecol Obstet 2012;285:1627-32.  Back to cited text no. 27
    
28.Sauvaget C, Fayette JM, Muwonge R, Wesley R, Sankaranarayanan R. Accuracy of visual inspection with acetic acid for cervical cancer screening. Int J Gynaecol Obstet 2011;113:14-24.  Back to cited text no. 28
    
29.Mittra I, Mishra GA, Singh S, Aranke S, Notani P, Badwe R, et al. A cluster randomized, controlled trial of breast and cervix cancer screening in Mumbai, India: Methodology and interim results after three rounds of screening. Int J Cancer 2010;126:976-84.  Back to cited text no. 29
    
30.Sankaranarayanan R, Nessa A, Esmy PO, Dangou JM. Visual inspection methods for cervical cancer prevention. Best Pract Res Clin Obstet Gynaecol 2012;26:221-32.  Back to cited text no. 30
    
31.Tamil Nadu Health Systems Project. Available from: http://www.tnhsp.org/screening-cervical-cancer-and-breast-cancer. [Last accessed on 2013 Apr 27].  Back to cited text no. 31
    


    Figures

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    Tables

  [Table 1], [Table 2], [Table 3], [Table 4]



 

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