|Ahead of print
Evaluating the feasibility of utilizing Gynocular-triage-to-diagnose application with VIA (Visual inspection with Acetic acid) in community cervical cancer screening programs in rural Mysore, India
Vijaya Srinivas1, Holly M Nishimura2, Poornima Jayakrishna1, Karl Krupp3, Purnima Madhivanan4, SubbaRao V Madhunapantula5
1 Public Health Research Institute of India, Mysore, Karnataka, India
2 School of Public Health, Johns Hopkins University, Baltimore, Tucson, USA
3 Public Health Research Institute of India, Mysore, Karnataka, India; Department Health Promotion Sciences, Mel and Enid Zuckerman College of Public Health, Tucson, USA
4 Department of Medicine, Division of Infectious Diseases; Department of Family & Community Medicine, College of Medicine, University of Arizona, Tucson, USA
5 Department of Biochemistry, Center of Excellence in Molecular Biology and Regenerative Medicine (CEMR) Laboratory, Mysore, Karnataka, India
|Date of Submission||21-Feb-2019|
|Date of Decision||16-May-2019|
|Date of Acceptance||28-Mar-2020|
SubbaRao V Madhunapantula,
Department of Biochemistry, Center of Excellence in Molecular Biology and Regenerative Medicine (CEMR) Laboratory, Mysore, Karnataka
Source of Support: None, Conflict of Interest: None
Background: Cervical cancer is the third most common cancer among women in India. The aim of the study is to determine the feasibility of using the Gynocular-triage-to-diagnose (Gynocular T2D/GT2D) in conjunction with visual inspection with acetic acid (VIA) in community-based cervical cancer screening programs in rural Mysore, India.
Methods: Between November 2015 and August 2016, the Public Health Research Institute of India (PHRII) implemented a mobile cervical cancer-screening in Mysore district using VIA and GT2D. Women underwent speculum exams and VIA positive cases were identified. Swede score was assessed using GT2D and a score >4 indicated further monitoring or referral for treatment. Papanicolaou (Pap) smears were conducted for selected cases. Statistical analysis was performed using Chi-square and Fisher's exact tests.
Results: Among 199 women registered in the camp, 176 were included in the final analysis. 23 women were excluded due to vaginal bleeding. The average age of women was 39 years (range = 27-59 years). Among the 176 cases, 38 (21.6%) were VIA positive and 138 (78.4%) were VIA negative. Swede score of >4 was observed in 6 VIA positive and 7 VIA negative women. Two cases among VIA negative with a score of >4 were suggested biopsy.
Conclusion: Gynocular triaging prevented overtreatment of 32 (18.1%) participants, and identified 7 subjects with >4 Swede score even in VIA negative cases, which would have been ignored if VIA alone was used. In summary, our study demonstrates that Gynocular triaging is feasible in community cervical cancer screening programs.
Keywords: Cervical cancer, Gynocular T2D, VIA, swede score, Pap test
Key Message: Gynocular TM Triage-to-Diagnose application can be combined with Visual Inspection with Acetic acid (VIA) for the better diagnosis of cervical cancers in a community-screening program.
|How to cite this URL:|
Srinivas V, Nishimura HM, Jayakrishna P, Krupp K, Madhivanan P, Madhunapantula SV. Evaluating the feasibility of utilizing Gynocular-triage-to-diagnose application with VIA (Visual inspection with Acetic acid) in community cervical cancer screening programs in rural Mysore, India. Indian J Cancer [Epub ahead of print] [cited 2021 Jan 20]. Available from: https://www.indianjcancer.com/preprintarticle.asp?id=297014
| » Introduction|| |
Cervical cancer is the third leading cause of cancer-related deaths among females in low- and middle-income countries (LMICs). According to recent global statistics, about 5,70,000 new cervical cancer cases and 3, 11, 000 deaths were attributed to cervical cancer in the year 2018. Incidence and mortality rates are much higher in developing countries compared to developed countries, which could be due to differences in the access to screening tests, patient education, and availability of appropriate resources for effective immunization and treatment.,
In high-income countries, where population-based screening programs were introduced several decades ago, cervical cancer incidence decreased by as much as 4% annually, and 70% overall. Incidence rates also decreased in high-incidence areas, including India and Brazil, possibly due to improved socioeconomic conditions and screening coverage. Despite modest improvement in decreasing the incidence of cervical cancer in India, every year about
96,922 new cases and 60,078 cancer-related deaths are being reported. In addition, India has the highest age-standardized incidence of cervical cancer in South Asia (i.e. 22), compared to 19.2 in Bangladesh, 13 in Sri Lanka, and 2.8 in Iran.
Implementation of cytology-based screening programs has been difficult in many low-resource settings because of expensive laboratory-based infrastructure and equipment, need for skilled personnel to prepare and analyze Papanicolaou (Pap) smear slides. Therefore, LMICs where cervical cancer remains one of the main causes of cancer deaths among women, require an affordable, easy-to-use, reliable point-of-care screening method(s), which can be used in low-resource settings. The World Health Organization (WHO) recommends low-cost screening methods such as visual inspection with acetic acid (VIA) or visual inspection with Lugol's iodine (VILI) for limited-resource settings. Although these methods are cost-effective and produce immediate results, they are subjective and depend highly on the provider, who is performing the test. A pooled analysis of cross-sectional studies in India and Africa reported sensitivity and specificity of 92% and 85%, respectively, for VILI, versus 77% and 86% for VIA to detect high-grade Cervical Intraepithelial Neoplasia (CIN)., The low specificity of VILI and VIA (85% and 86%, respectively) can lead to unnecessary referrals, investigation (s), over-treatment, and psychological stress (associated with false-positive screening tests) to the individuals., Hence, a more accurate and confirmatory test is urgently needed.
To address the above concerns, a mobile colposcope triaging method was developed and tested for its feasibility to use in cervical cancer screening programs. In principle, the colposcope triaging method involved observing the aceto-white lesions from the VIA test under magnification, followed by harvesting a biopsy of the suspected lesion, when necessary.
Triaging with Gynocular has following advantages: (a) convenience and convincing. Since the photographs could be shared through cloud system and the expert opinion can be obtained, the diagnosis of cervical cancer is more accurate compared to VIA, where the decision is made only by the observer. In addition, the patients appeared to be more convinced when the Gynocular photographs are shown to them; (b) better visualization. Unlike regular VIA procedure where the vessel patterns are not fully visible, in the Gynocular, vessel patterns are better visualized with accuracy and at higher magnification; and (c) cost. Other than the initial investment, the Gynocular needs no additional expenses. Hence, it is more convenient and cost-effective compared to VIA, where a laboratory and reagents are required. However, the feasibility of using a standard colposcope triaging is limited due to low-resources and community-based settings. To overcome these limitations, a Gynocular, a pocket-sized monocular colposcope, (which can be mounted on a camera tripod), with 5× to 12× magnification, Light Emitting Diode (LED) illumination, green filter, and a rechargeable battery, was developed by Gynius, A.B. Stockholm, Sweden. The optics, resolution, and illumination of the Gynocular [Table 1] are comparable with those of the traditional colposcope. The previous studies have shown the accuracy of the Gynocular to be comparable with traditional colposcopy., In the present study, we examined the feasibility of using Gynocular with VIA testing in cervical cancer screening programs using a mobile clinic model in rural hard-to-reach settings in India.
| » Materials and Methods|| |
The study was approved by the Institutional Review Board of the Public Health Research Institute of India (PHRII), Mysore, Karnataka, India (IRB approval # 2016-08-20-34).
This cross-sectional study was conducted in rural Mysore Taluk of Mysore District. Mysore district has a population of 3,001,127 persons, of which 1,489,527 are female. About 58.6% of residents live in 1,332 rural villages. Annual per capita income and literacy for rural residents was INR 16,086 (USD 322), and 63.3%, respectively, which are much lower when compared to all-India annual per capita income of INR 38,005 (USD 760) and literacy rate (74.0%). The majority of rural residents belong to Hindu (87.7%) religion and the remaining 12.3% were Muslim or other religions.
A team of outreach workers and counselors were used to create awareness about cervical cancer and counsel women to get screened. The team used the existing networks in the community to spread awareness, provided general reproductive health education, and encouraged health care seeking. Local gatekeepers including Auxillary Nurse Midwives (ANMs), Accredited Social Health Advocates (ASHAs), and Anganwadi workers (maternal and child health outreach workers) helped in implementing the program. The Anganwadi workers are community-based employees working for Government of India's Child Development project (for more details please visit the website http://www.wcd.nic.in/). A training program for Anganwadi workers in Hunsur Taluk of Mysore district was organized on the request of Child Development Project Officer. This training was conducted in 17 batches with 338 Anganwadi workers. The one-day training program included presentations about women's reproductive health, cervical cancer prevention, and treatment of precancerous lesions. The training program was organized with pre- and post-test questionnaires to assess the change in knowledge after the training. All the women were given awareness about the newly introduced Gynocular and its benefits in community-based screening program.
Participants were recruited by the outreach workers of PHRII, as well as by Anganwadi workers from the villages in Hunsur Taluk of Mysore district. Women were counseled by trained counselors and enrolled in the study after they underwent informed consent process. In total, 199 women consented to participate in the study. To be eligible for screening, women had to be above 30 years of age, not pregnant, willing to undergo a pelvic examination, and visit PHRII clinic if a follow-up examination was necessary. Exclusion criteria included a history of hysterectomy, vaginal bleeding, or history of cervical cancer, and not willing to participate. Written informed consent was obtained for completing VIA as well as Gynocular procedures.
Demographic details such as age, education, religion, and marital status were collected from all the study participants. Eligible women who provided written informed consent were assigned a study identification number. In addition to demographic data, information about their reproductive health and healthcare-seeking behavior was collected. Following the questionnaire, each woman received one-on-one counseling to understand the cervical cancer screening procedures that would be performed in detail and answer any questions that the woman may have had. All communication was in the local languages of Kannada or Urdu.
Screening by VIA and Gynocular
To assess women for precancerous cervical lesions, a physician conducted a clinical examination. The examination was performed in lithotomy position on a gynecological table using a self-retaining Cusco speculum. The cervix was visualized and examined for unusual vaginal discharge or other abnormalities (warts, growth, and uterine prolapse). A cotton swab was inserted to collect some vaginal fluid to assess the vaginal pH and odor. During speculum examination, the cervix was visualized and observed for any abnormalities such as inflammation, hypertrophy, erosion, polyps, and leukoplakia. VIA was carried out by squirting 4–5 ml of 5% acetic acid into the vagina using a needleless syringe. The solution was bathed over the entire cervix using a cotton swab for a minute. The VIA screening was classified as positive when a sharp, distinct, well-defined, dense aceto-white area on the cervix, with or without raised margins, close to the squamo-columnar junction (SCJ) in the transformation zone was observed. The examination was described “adequate” only if SCJ was visible. In cases where SCJ was not fully visible, the examination was considered “inadequate.” Pap tests were performed for subjects with inadequate SCJ. A set of adequate positive cases were also tested by Pap to rule out false-positive findings. Women with VIA adequate result and negative in Pap test were recommended to visit the center after 3 years for a follow-up. However, VIA adequate women with Pap test positive findings were suggested for a biopsy or cryotherapy or loop electrosurgical excision procedure ( LEEP) examinations based on mild or moderately positive or high-grade lesions found in Pap smear More Detailss [Flowchart 1] and [Flowchart 2].
In summary, the screening procedure involves identification of individuals with clear/nonclear SCJ (adequate/inadequate) followed by examination for positive or negative response to VIA. Once identified, the individuals with VIA positive result were subjected to Pap test followed by biopsy examination.
On completion of VIA, the Gynocular mounted on a camera tripod along with the smartphone and having a T2D clinical software application was used to record high definition (HD) images of the cervix to document cervical abnormalities [Features of Gynocular system are described in [Table 1]. The Gynocular results were represented in Swede score. The Swede score consisted of four variables that included: (1) aceto-whiteness; (2) margin plus surface; (3) vessel pattern; and (4) lesion size. Next, the cervix was swabbed with Lugol's iodine solution and the 5th Swede score was assigned for iodine staining. A Swede score ranged from 0 to 10. A score ≤4 excluded high-grade disease or cancer, while a score >4 was indicative of a high-grade lesion (Cervical Intraepithelial Neoplasia - CIN2 and CIN3).
The T2D software has an option to refer images to a colposcopic specialist. The Gynocular images of the cervix for each participant were referred to an expert who examined and provided the final scores. Participants with negative VIA with score ≤4 and with normal Pap report were scheduled for a follow-up visit after 3 years. Those cases with abnormal Pap results and Gynocular score >4 were referred for cryotherapy services or LEEP. The VIA positive cases with score ≤4 were also referred to the nearest government hospital for second opinion. In addition, the VIA positive cases with score ≤4 were closely monitored by the outreach staff and advised for follow-up for re-screening after 6 months to rule out false positivity or confirm positivity.
Data management and statistical analysis
Data entry was done using Microsoft Access 2000 software. Statistical analysis was carried out using SPSS 20 software. Proportions were compared for categorical variables using Chi-square and Fisher's exact tests where appropriate, and 95% confidence intervals (CIs) were calculated.
| » Results|| |
Of the 199 cases eligible, 23 cases were excluded due to bleeding, incomplete procedures, including 2 women who were unwilling to participate. Acceptability of the procedure in the community setting was very high as 197 women out of 199 eligible subjects had agreed to undergo the procedure. The final analysis included a total of 176 cases. Among these 176 women, the mean age was 39 years (range = 27-59 years, Standard Deviation (SD) ±7.6). Most women were Hindu (79.5%), married (96.9%), and parous (96%). The demographic details are given in [Table 2]. Examination of these 176 individuals for the visibility of squamocolumnar junction (SCJ) showed the presence of clear SCJ boundaries in 153 individuals (86.93%; considered as “Adequate”). However, the remaining 23 individuals (13.07%) had poor SCJ margins or SCJ was not visible (considered “inadequate”). Further examination showed that 33 out of 153 individuals (with clear SCJ margins) were positive for VIA. Similar analysis in individuals with poorly distinguished SCJ showed positive VIA in 5 cases [Flowchart 1]. In summary, among the 176 women, who were first screened by VIA, 38 (21.6%; 33 with clear SCJ margins and 5 with relatively poor SCJ margins) were positive for VIA, while remaining 138 (120 individuals with clear SCJ and 18 from individuals with poor SCJ margins) were negative [Flowchart 1]. The 38 VIA positive women with deep dense acetowhite area and sharp margins adjacent to squamocolumnar junction (SCJ) were referred to a tertiary hospital for a second opinion.
Examination of VIA positive (38 cases) and negative (138 cases) subjects using Gynocular showed that 163 individuals (145 from clear SCJ group and 18 from poor SCJ group) had a Swede score <4 and 13 individuals had Swede score >4 (6 from clear SCJ group and 7 from poor SCJ group).
Pap smears were carried out only when the identification of SCJ is difficult and not conclusive (referred as inadequate VIA). A total of 47 Pap tests were performed, among which 23 were VIA positive and 24 were VIA negative. Of these 23 VIA positive cases selected for Pap testing, 18 individuals were with Swede score ≤4 and 5 were with Swede score >4 [Flowchart 2]. Likewise, among the 24 VIA negative cases, from whom Pap smears were collected, 21 were with Swede score ≤4 and three with Swede score >4. Biopsies were obtained for (a) one participant with positive VIA and Swede score of ≤4 due to prominent dense acetowhite lesion and (b) two individuals with negative VIA but Swede score of >4. Analysis of tissue biopsies of these 3 subjects showed the presence of Koilocytic atypia in one of the two individuals with negative VIA but scored >4 in Swede scores. Koilocytic atypia is characterized by the presence of Koilocytes and demands frequent cancer screening.
Analysis of the Pap test results, by a pathologist, with Swede score >4 showed normal Pap result for 5 cases, one woman had atypical glandular cells of endocervical origin–reactive (which is benign but inflammatory), one woman had atrophic smear, and one had a high-grade squamous intraepithelial lesion (HSIL) [Table 3] and [Table 4]. Among the 39 cases with Swede scores of ≤4, 19 (48.7%) had normal Pap results, while 4 (10.2%) had atypical glandular cells of endocervical origin–reactive, 2 (5.1%) had atrophic smear, and 2 (5.1%) had a low-grade squamous intraepithelial lesion and 1 (2.5%) had a high-grade squamous intraepithelial lesion (HSIL). Among the remaining cases, 6 (15.3%) were inflammatory and 5 (12.8%) had inadequate cell number [Table 3] and [Table 4]. Cryotherapy was performed for two women whose Swede score was >4.
| » Discussion|| |
VIA is considered as a preferred cost-effective method compared to Pap tests and Human Papilloma Virus (HPV) DNA-based tests for cervical cancer screening in low- and middle-income countries. In general, VIA positive cases are treated on the same visit with cryotherapy. However, recent studies have raised a concern about the ability of VIA examination alone for conclusively identifying precancerous lesions. One possible reason is the identification of false-positive cases with VIA. Therefore, there is a need to identify cost-effective methods to further confirm VIA test results. One such method was Gyocular T2D, which has no additional expense except the initial investment of purchase of the instrument. In our program, the acceptability to undergo these tests was encouraging as only two women were not willing to participate. Economically, VIA continues to be cost effective provided a single visit “screen and treat” approach is used; however, chances of overtreatment are high. The issue of overtreatment can be avoided by improving the specificity of screening methods or by combining with other methods such as the use of Gynocular to ensure that women who need further follow-up are only recommended for biopsy-based test. Moreover, the concept of VIA and preventive measures for cervical cancer is not adequate in government hospitals, creating a problem for referral system. Hence, programs such as continued medical education (CME) might strengthen the referral system.
In the present study, we have assessed the feasibility and potential for use of Gynocular T2D in a community-based setting to detect precancerous lesions based on the Swede score. While the Gynocular T2D system helped in detecting precancerous cases even among VIA negative subjects, it needs to be confirmed. In addition, examination with Gynocular helped in preventing unnecessary treatment of subjects who otherwise would have been exposed to various diagnostic and treatment methods due to their VIA positive result. In our study, the majority of VIA positive cases had Swede scores of ≤4 when assessed with Gynocular. Therefore, triaging VIA positive women using Gynocular would be a feasible and cost-effective way in community-based mobile screening programs to reduce not only the number of false positives but also to decrease the burden on healthcare. However, further studies examining the biopsies of all Gynocular positive and VIA positive cases are required to demonstrate the sensitivity and specificity of Gynocular over VIA in detecting precancerous lesions.
Gynocular was used as a screening tool along with VIA to avoid any inconvenience in community. Although the sample size of our study was relatively low, a recent crossover, randomized clinical trial at the colposcopy clinic of Bangabandhu Sheikh Mujib Medical University in Dhaka, Bangladesh, with 540 VIA-positive women revealed that Swede score identified more CIN+ lesion than VIA testing and liquid-based cytology analysis, therefore, offering more accurate screening and selection for immediate treatment of cervical lesion in low-resource setting. Another randomized crossover clinical trial evaluating the ease of Swede score system showed no significant differences in the scores between the values reported by a trained VIA nurse and a doctor in detecting cervical lesions by Gynocular. Hence, Gynocular T2D would be a likely option for community-based cervical cancer screening in low-resource setup. Supporting this, a recent screening study in India, conducted by Chittaranjan National Cancer Institute (CNCI) in 6883 women, recommended the GT2D application for VIA screening. This study highlighted the importance of Gynocular for effective triaging to detect precancerous lesions with more accuracy.
Although the results of our study reported the benefits of utilizing Gynocular T2D, there are limitations in this study. For instance, Pap test was carried out only for randomly selected VIA negative participants to compare the Swede score of Gynocular. Similarly, biopsies were collected only for selected individuals among 38 VIA positive cases, hence, failed to assess the efficacy of Gynocular in detecting with conformity. Therefore, future studies should consider performing these tests among all participants and comparing the results of Gynocular T2D to conclusively establish whether triaging with Gynocular is a potential way of screening individuals for precancerous lesion during cervical cancer screening program.
| » Conclusion|| |
Our study found Gynocular T2D with VIA screening is acceptable and convenient to use in community programs. However, there is a need for training healthcare workers who are involved in VIA screening. If optimally utilized, triaging with Gynocular T2D can help in detecting early cervical lesions, which otherwise might progress into advanced cancer.
Authors would like to thank all the women who participated in this study. Our sincere thanks to AOGIN-India. Thanks to Dr. Abraham P., CMC Vellore for his support and editorial inputs. Our thanks to Rashmi, P., Fazilla, B., Rani, C., Chandramani, Nandini Urs, Savitha Counselor of PHRII for their help in completing the study. Our thanks to Dr. Elisabeth Shemmer for assisting in analyzing the Gynocular image. Karl Krupp and Purnima Madhivanan would like to acknowledge the support by the National Institutes of Health/Fogarty International Center (FIC), National Heart Lung and Blood Institute (NHLBI), National Institute of Neurological Disorders and Stroke (NINDS) Award # D43 TW010540. Purnima Madhivanan was also partly funded by National Institutes of Health/National Institute of Allergy and Infectious Diseases (NIAID) #1R15AI128714-01
Declaration of patient consent
The authors certify that they have obtained all appropriate patient consent forms. In the form, the patients have given their consent for their images and other clinical information to be reported in the journal. The patients understand that their names and initials will not be published and due efforts will be made to conceal their identity, but anonymity cannot be guaranteed.
Financial support and sponsorship
Conflicts of interest
There are no conflicts of interest.
| » References|| |
Arbyn M, Weiderpass E, Bruni L, de Sanjose S, Saraiya M, Ferlay J, et al
. Estimates of incidence and mortality of cervical cancer in 2018: A worldwide analysis. Lancet Glob Health 2020;8:e191-e203.
Bruni L, Diaz M, Castellsague X, Ferrer E, Bosch FX, de Sanjose S. Cervical human papillomavirus prevalence in 5 continents: Meta-analysis of 1 million women with normal cytological findings. J Infect Dis 2010;202:1789-99.
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;6:281-90.
Bray F, Loos AH, McCarron P, Weiderpass E, Arbyn M, Moller H, et al
. Trends in cervical squamous cell carcinoma incidence in 13 European countries: Changing risk and the effects of screening. Cancer Epidemiol Biomarkers Prev 2005;14:677-86.
Gustafsson L, Ponten J, Zack M, Adami HO. International incidence rates of invasive cervical cancer after introduction of cytological screening. Cancer Causes Control 1997;8:755-63.
Bobdey S, Sathwara J, Jain A, Balasubramaniam G. Burden of cervical cancer and role of screening in India. Indian J Med Paediatr Oncol 2016;37:278-85.
] [Full text]
Sreedevi A, Javed R, Dinesh A. Epidemiology of cervical cancer with special focus on India. Int J Womens Health 2015;7:405-14.
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.
] [Full text]
Haney K, Tandon P, Divi R, Ossandon MR, Baker H, Pearlman PC. The role of affordable, point-of-care technologies for cancer care in low- and middle-income countries: A review and commentary. IEEE J Transl Eng Health Med 2017;5:2800514.
Huchko MJ, Sneden J, Zakaras JM, Smith-McCune K, Sawaya G, Maloba M, et al
. A randomized trial comparing the diagnostic accuracy of visual inspection with acetic acid to Visual Inspection with Lugol's Iodine for cervical cancer screening in HIV-infected women. PLoS One 2015;10:e0118568.
Sankaranarayanan R, Gaffikin L, Jacob M, Sellors J, Robles S. A critical assessment of screening methods for cervical neoplasia. Int J Gynaecol Obstet 2005;89(Suppl 2):S4-S12.
Sankaranarayanan R. Screening for cancer in low- and middle-income countries. Ann Glob Health 2014;80:412-7.
Arbyn M, Sankaranarayanan R, Muwonge R, Keita N, Dolo A, Mbalawa CG, et al
. Pooled analysis of the accuracy of five cervical cancer screening tests assessed in eleven studies in Africa and India. Int J Cancer 2008;123:153-60.
Lewis KC, Tsu VD, Dawa A, Kidula NA, Chami IN, Sellors JW. A comparison of triage methods for Kenyan women who screen positive for cervical intraepithelial neoplasia by visual inspection of the cervix with acetic acid. Afr Health Sci 2011;11:362-9.
Nessa A, Wistrand C, Begum SA, Thuresson M, Shemer I, Thorsell M, et al
. Evaluation of stationary colposcope and the Gynocular, by the Swede score systematic colposcopic system in VIA positive women: A crossover randomized trial. Int J Gynecol Cancer 2014;24:339-45.
Ghosh I, Mittal S, Banerjee D, Singh P, Dasgupta S, Chatterjee S, et al
. Study of accuracy of colposcopy in VIA and HPV detection-based cervical cancer screening program. Aust N
Z J Obstet Gynaecol 2014;54:570-5.
Nessa A, Roy JS, Chowdhury MA, Khanam Q, Afroz R, Wistrand C, et al
. Evaluation of the accuracy in detecting cervical lesions by nurses versus doctors using a stationary colposcope and Gynocular in a low-resource setting. BMJ Open 2014;4:e005313.
Adsul P, Srinivas V, Gowda S, Nayaka S, Pramathesh R, Chandrappa K, et al
. A community-based, cross-sectional study of hrHPV DNA self-sampling-based cervical cancer screening in rural Karnataka, India. Int J Gynaecol Obstet 2019;146:170-6.
Fuenmayor A, Fernandez C, Perez V, Coronado J, Avila M, Fernandes A, et al
. Detection of precancerous lesions in the cervix and HPV infection in women in the region of Maniapure, Bolivar State. Ecancermedicalscience 2018;12:884.
Vedantham H, Silver MI, Kalpana B, Rekha C, Karuna BP, Vidyadhari K, et al
. Determinants of VIA (visual inspection of the cervix after acetic acid application) positivity in cervical cancer screening of women in a peri-urban area in Andhra Pradesh, India. Cancer Epidemiol Biomarkers Prev 2010;19:1373-80.
Ngonzi J, Bajunirwe F, Wistrand C, Mayanja R, Altman D, Thorsell M, et al
. Agreement of colposcope and gynocular in assessment of cervical lesions by swede score: A randomized, crossover pilot trial. J Low Genit Tract Dis 2013;17:372-7.
Ferlay J, Soerjomataram I, Dikshit R, Eser S, Mathers C, Rebelo M, et al
. Cancer incidence and mortality worldwide: Sources, methods and major patterns in GLOBOCAN 2012. Int J Cancer 2015;136:E359-86.
Basu P, Meheus F, Chami Y, Hariprasad R, Zhao F, Sankaranarayanan R. Management algorithms for cervical cancer screening and precancer treatment for resource-limited settings. Int J Gynaecol Obstet 2017;138(Suppl 1):26-32.
Basu P, Banerjee D, Mittal S, Mandal R, Ghosh I, Das P, et al
. Evaluation of a compact, rechargeable, magnifying device to triage VIA and HPV positive women in a cervical cancer screening program in rural India. Cancer Causes Control 2016;27:1253-9.
[Table 1], [Table 2], [Table 3], [Table 4]