Abstract
Introduction
Cervical cancer is the second common cancer among Indian women, with incidence of 17.7 per 100,000 women and a national screening coverage of less than 2%. HPV-Self Sampling (SS) offers a promising opportunity to expand screening coverage. However, understanding the feasibility of this method within the local context is crucial before implementing it as a large-scale intervention.
Objective
To assess the feasibility of HPV self-sampling (HPV-SS) by exploring the determinants of participation, user experiences and care trajectory among screen positive women on HPV-SS from urban non slum, urban slum, rural and tribal settings in India.
Methodology
Eligible women in age group of 30–69 years were invited to participate in the study. Women enrolled in the study were delivered in-depth education on cervical cancer. In post education session, women were invited to participate in cervical cancer screening, using HPV-SS.
Results
The initial participation rate in the study was 66%. The acceptance of HPV-SS was 98.2% after health education among enrolled women. The prevalence of oncogenic HPV ranged from 4.4% to 11.2%, with the highest rates observed in tribal population.
Compliance with referral among screen-positive women was 82% in urban non-slum areas and 89% from urban slum settings. In rural and tribal settings, compliance rates were 67% and 89%, respectively, following the organization of community camp. Perception of self-confidence in the accuracy of collecting self-samples and preference for HPV-SS over provider-collected samples varied across the settings.
Conclusion
The study highlights HPV-SS as a key driver for scaling up cervical cancer screening coverage. However, initial low participation rates for cervical cancer screening, underscores the need for continuous community awareness efforts and capacity-building among grass root healthcare personnel. Though HPV-SS appears promising, challenges such as limited access to designated laboratories and accessibility to treatment facilities remain significant barriers of widespread implementation.
Keywords: Cervical cancer, Screening, Feasibility, HPV-Self sampling, HPVDNA test, Marginalised women, Health disparities
Background
Cervical cancer is an important public health issue in low and middle income countries (LMICs), contributing substantially to the overall disease burden [1]. Many women in LMICs succumb to the disease because of advance stage presentation. Cervical cancer has precancerous stage that can be detected by cost-effective screening methods [2, 3]and can be treated with simple and effective procedures, thus preventing avoidable deaths. There are however disparities in regards to cervical cancer incidence and mortality rates between and within the countries. The screening rates remain substantially low in many developing countries [4–6]. These disparities are often related to markedly inadequate health systems especially with regards to availability of good quality cervical cancer screening and treatment facilities. Low awareness, due to poor literacy levels and low socioeconomic status further complicates the elimination of this preventable disease [7].
In India, cervical cancer is the second leading cause of cancer deaths among women. In 2022, 127,526 new cervical cancer cases were reported from India with age adjusted incidence (AAI) rate of 17.7 per 100,000. Increase in Incidence rates are projected by 4.9% by year 2030 [4]. Factors such as early age of sexual debut, multiple sexual partners, and increasing smoking rates among younger generations contribute to higher risk of persistent HPV infections [6]. Without an organized screening program, this rising burden of cervical cancer poses a serious public health concern.National cervical cancer screening guidelines in India were updated under National Program for Prevention and Control of Cancer, Diabetics, Cardiovascular diseases and Stroke (NPCDCS) in year 2017 and again more recently in 2023 under National Programme for Prevention of Non-Communicable Diseases (NP-NCD). Despite the presence of these policies, the cervical cancer screening rates remain substantially low at < 2%, and primarily conducted through opportunistic screening [8]. As a country with vast population and significant sociocultural diversity, where majority of the population still resides in rural areas, access to screening and healthcare services is uneven [9]. Women from rural, tribal and low income settings are particularly marginalised with limited knowledge of cervical cancer and restricted access to essential health care facilities.
Some of the key population level barriers that have been identified with regards to screening uptake among women are poor literacy levels, low socioeconomic status, lack of knowledge about the disease, unavailability of cervical cancer screening facilities at an accessible distance and psychological stress associated with screening [10, 11]. Due to low level of education, undertaking screening in absence of symptoms, is perceived as an unnecessary process. Spending the day participating in screening may also lead to loss of daily wages, thus pushing down the priority for screening in preference of job or household chores [12–14]. The critical structural barriers identified includethe time required for women to travel to screening facilities, long waiting times at the clinics, preference for gender concordance between patients and healthcare providersand financial constrains associated with accessing quality treatment [13]. The affordability and accessibility issues associated with cervical cancer screening and prevention services are also some of the important challenges associated with poor uptake of cervical cancer screening.
Among the screening tests, there is good evidence for primary screening with visual inspection with acetic acid (VIA) to be an effective screening tool in countries with low resources [3]. Despite this, VIA still has major disadvantage of having high false positivity rates. Hence women screened positive need to be further triaged. This adds to inconvenience, as it includes travelling to diagnostic care centers, which may be far away. This modality of screening remains a challenge to sustain and scale up programs at National level. Currently there are rapid developments in molecular Human Papillomavirus (HPV) testing platforms. WHO supports molecular HPV-DNA based tests, as primary screening modality, for its advantage of high sensitivity and high negative predictive value, thus translating into requirement of lesser number of screening rounds [3]. The HPV test has a potential to leverage the resources at national level, because of lesser requirement of manpower and less subjectivity. There are two modalities proposed with HPVDNA testing- Physician collected sampling and Self collected sampling. Among these screening modalities –HPV-Self Sampling (HPV-SS) has potential to increase the screening coverage in India due to its proven non-inferior performance to physician collected samples and lesser logistics requirements [15–19]. The test empowers women to self-screen herself for cervical cancer at her convenience. The test is poised to be a key pillar to improve access to screening. Thus, cervical cancer screening with HPV in combination with good HPV vaccination coverage will move the nation towards WHO elimination targets.
The evidence from developed countries supports HPV-SS as a potential screening test for scaling up the screening coverage of cervical cancer. There are however gaps in literature about experiences regarding self-sampling from developing countries like India. There are mixed preferences of accepting HPV-SS over other traditional modalities of screening like VIA and Cytology [20]. The success of screening programs depend on availability and acceptability of screening test by the targeted beneficiaries. India being a country with huge social and cultural diversity, it becomes important to understand the acceptability and feasibility of HPV-SS in reference to specific local context. There is limited information about experiences of HPV-SS among users and linkage of screen positive women on HPV-SS to health systems [21]. The current study appraises the acceptability, feasibility, care trajectory and user experiences of women towards HPV-SS from different geographical, social and cultural context in the State of Maharashtra in India.
Methodology
The current study looks at data of two cross-sectional community-based cohort studies on HPV-SS among marginalized population, that were implemented in - rural, tribal, urban slum settings (with temporary and unstable house, with overcrowding, inadequate sanitation, and common toilet facilities) and urban non-slum settings (stable home with overcrowding, with toilet facility at home) in neighbourhoods of Mumbai city in State of Maharashtra in India.
The objective of the current study was to understand the determinants of participation for HPV-SS, user experiences and care trajectory of women with screened positive HPV-SS test results based on their place of residence - categorized as rural, tribal, urban slum neighbourhoods and urban non-slum neighbourhoods. Initially house to house survey was conducted to identify the eligible women and they were enumerated. The study team tried to contact these women after a month or two when systematic camps were organized in their areas, in order to invite them for screening.
Under or never screened married women in age group of 30–69 years, non-pregnant, with intact cervix and with no previous history of being treated for cervical precancerous or cancerous lesion, were invited at designated camp place within the implementing areas for enrollment. Informed consent was obtained from the study participants. Baseline data on sociodemographic characteristics, reproductive history and knowledge of HPV and cervical cancer were collected through an interview-based questionnaire. This was then followed by education on cervical cancer, using art-based health education material. The education material used in the study –specially focused on HPV, different screening modalities and in-depth steps for collecting HPV-SS. Following the health education awareness sessions, women were invited for screening using HPV-SS. Women were given option for collecting their samples either at the camp place or at their home. The designated camp places had a private space that was created using mobile partitions, for women opting to collect the samples at camp place. The samples were collected on the same or subsequent day from women who opted to collect their samples at home. The HPV samples were transported to the designated laboratories on the same day in vaccine carriers maintaining the temperature using ice packs. In the implementing settings, where the samples could not be transferred on the same day to the laboratories, the samples were stored at 2 to 8 degrees in the refrigerator of the Primary Health Care centers. All the samples at the implementing sites were transported within seven days of collection to the designated laboratories. The screened positive women on HPV-SS were referred to the tertiary care Centre for further diagnosis and treatment. For participants who faced barriers in accessing tertiary care centers, a triage camp was organized in the community using Pap and VIA testing. Women positive on both the tests were referred for Colposcopy at the nodal referral hospital.
The HPV-SS were collected by women using the Qiagen sampling kit and the test was processed by Hybrid Capture 2 test (HC2) for all women enrolled under the study. The Relative Light Unit (RLU)/ cut off ratio equal to or greater than 1, corresponding to 5000 or more copies of virus in a sample was considered as positive test. The reporting of Pap smear was done as per the Bethesda classification [22].
Statistics used
The data was entered in IBM SPSS Statistics for Windows, Version 25.0 (IBM Corp., Armonk, N.Y) software. Categorical variables were summarized using frequencies and percentages. The normality of continuous variables was assessed through P-P and Q-Q plots, as well as histograms. Comparisons between demographic variables and study arms were conducted using Chi-square test or Fisher’s exact test. All tests were carried out using an α = 0.05 level of significance.
Results
Table 1 describes enrollment of respective number of women across different settings - urban slum, urban non-slum, rural, and tribal during the organization of community based cervical cancer screening camps amongst these groups. Initially house to house survey was conducted to identify the eligible women and they were enumerated. The study team tried to contact these women after a month or two when systematic camps were organized in their areas.
Table 1.
Participation of women for cervical cancer screening across different settings - urban slum, urban non-slum, rural and tribal settings
| Settings | Eligible women listed during initial survey* | Women not contacted due to lock doors or not at home during camp days | Actual women contacted during camp days | Unable to participate due to menstrual cycle during camp days | Women eligible to participate | Refused to participate N (%) | Participated N (%) |
|---|---|---|---|---|---|---|---|
| Urban slum | 857 | 87 | 770 | 132 | 638 | 138 (21.6) | 500 (78.4) |
| Urban non slum | 1002 | 114 | 888 | 167 | 721 | 221 (30.7) | 500 (69.4) |
| Rural | 2127 | 870 | 1257 | 137 | 1120 | 480 (42.9) | 640 (57.1) |
| Tribal | 307 | 126 | 181 | 50 | 131 | 51 (39%) | 80 (61) |
| Total | 4293 | 1197 | 3096 | 486 | 2610 | 890 (34%) | 1720 (66%) |
* Initial survey was done one to two months prior to implementation of the study
In the urban slum setting, of the 857 eligible women who were identified during the initial survey, 87 women could not be contacted when screening camps were organized during the implementation phase due to locked houses or women gone out during the camp timings. Out of 770 women (n = 857 − 87) contacted on the camp days, 132 women were unable to participate because they had menstrual cycle during that time, resulting in 638 women (n = 770 − 132) being actually invited for screening. Among 638 women, 500 women (78.4%) participated, while 138 women (21.6%) refused participation.
Similarly, in urban non slum setting, of the 1002 eligible women identified during the initial survey, 114 women could not be contacted due to locked houses or women not at home on the camp days. Consequently, 888 women (n = 1002 − 114) were contacted during the camp days. Among those contacted, 167 women were unable to participate due to their menstrual cycle during that time, resulting in 721 women (n = 888 − 167) being invited for screening. Among these women, 500 women (69.4%) participated, while 221 women (30.7%) refused participation.
In rural setting, among 2127 eligible women identified during the initial survey, 870 women could not be contacted due to locked houses or women not at home during the days of the camps. Thus 1257 women (n = 2127 − 870) were contacted among whom 137 women were unable to participate due to menses, resulting in 1120 women (n = 1257 − 137) being invited for screening. Subsequently, 640 women (57.1%) participated, while 480 women (42.9%) refused participation.
Similarly, in tribal settings, among 307 eligible women identified during the initial survey, 126 could not be contacted during the camp days. Among 181 women (n = 307 − 126) contacted and invited to participate, 50 women were having menstrual cycle. A total of 131 women (181 − 50) were invited, among whom, 80 women (61%) participated and 51 women (39%) refused to participate in the study.
Participation rates varied by setting from 57.1% to 78.4% with an average participation rate of 66% across settings.
Figure 1 describes the acceptance of HPV Self sampling among women after education across study settings.
Fig. 1.
Acceptance of HPV Self-Sampling after Health Education by Study Setting
Figure 1 shows the number of women enrolled from each setting was, 500 in urban slums, 500 in urban non-slums, 640 in rural setting and 80 in tribal settings [23, 24].
In urban slums, among 500 women enrolled, 485(97%) women accepted HPV-SS after education regarding cervical cancer. Similarly, in urban non slum setting, among 500 women enrolled, 496(99.2%) women accepted HPV-SS. In rural settings, among 640 women enrolled, 630 women (98.4%) accepted HPV-SS and in the tribal settings, among 80 women enrolled 78 women (97.5%) accepted HPV-SS. This was after health education in all groups. (Figure. 1)
The overall acceptance of HPV-SS among women enrolled in the study was 98.2% (n = 1689/1720).
Table 2 demonstrates that among the 1689 women accepting HPV-SS, majority were in the age group of 30–40 yrs (55.8%), followed by the age group of 41–50 yrs (35.3%). Few women were in the age group 50 years and above (8.8%). Most women (58.1%) in the study population had completed only their primary education (i.e. completed 4th Grade). This was followed by 16.1% women who were either illiterate or studied till Grade 3. Majority of women from tribal population (39.7%) were in this subgroup. Overall, 14.1% women were degree holders. Most of these women belonged to urban non-slum settings (25.4%).
Table 2.
Socio demographic characteristics and knowledge of cervical cancer among women who accepted HPV-SS from different settings
| Characteristics | Urban Non-Slum N = 496 (%) |
Urban Slum N = 485 (%) |
Rural N = 630 (%) |
Tribal N = 78 (%) |
Total N = 1689 (%) |
p-Value |
|---|---|---|---|---|---|---|
| Age Groups | <0.0001 | |||||
| 30–40 |
244 (49.2%) |
309 (63.7%) |
343(54.4%) |
47 (60.3%) |
943 (55.8%) |
|
| 41–50 |
198 (39.9%) |
150 (30.9%) |
230 (36.5%) |
19 (24.4%) |
597 (35.3%) |
|
| Above 50 |
54 (10.9%) |
26 (5.3%) |
57 (9.0%) |
12 (15.4%) |
149 (8.8%) |
|
| Education* | <0.0001 | |||||
| Illiterate or with minimal formal education |
30 (6.1%) |
92 (18.9%) |
119 (18.9%) |
31 (39.7%) |
272 (16.1%) |
|
| Completed Primary Education |
258 (52.21%) |
293 (60.4%) |
405 (64.3%) |
25 (32.1%) |
981 (58.1%) |
|
| Completed Secondary School |
82 (16.5%) |
49 (10.1%) |
59 (9.4%) |
9 (11.5%) |
199 (11.7%) |
|
| Degree Holders |
126 (25.4%) |
51 (10.5%) |
47 (7.4%) |
13 (16.7%) |
237 (14.1%) |
|
| Monthly Family Income In Rupees | <0.0001 | |||||
| Up to 5000/month |
2 (0.4%) |
10 (2%) |
35 (5.6%) |
25 (32%) |
72 (4.3%) |
|
| 5001–10,000/month |
186 (37.5%) |
180 (37.1%) |
410 (65.1%) |
30 (38.5%) |
806 (47.7%) |
|
| > 10,000/month |
308 (62.1%) |
295 (60.8%) |
185 (29.4%) |
23 (29.5%) |
811 (48.1%) |
|
| Onset of Sexual Activity | <0.0001 | |||||
| 18 and Below |
84 (16.9%) |
213 (43.9%) |
244 (38.7%) |
55 (70.5%) |
596 (35.3%) |
|
| 19 and Above |
412 (83.1%) |
272 (56.1%) |
386 (61.3%) |
23 (29.5%) |
1093 (64.7%) |
|
| Parity | <0.0001 | |||||
| 0–2 |
399 (83.8%) |
314 (66.5%) |
424 (68.6%) |
33 (42.86%) |
1170 (71.2%) |
|
| 3 and Above |
77 (16.2%) |
158 (33.8%) |
194 (31.4%) |
44 (57.1%) |
473 (28.8%) |
|
| Ever Heard about Cervical Cancer | <0.0001 | |||||
| Yes |
491 (98.9%) |
399 (82.3%) |
605 (96.01) |
22 (28.2%) |
1517 (89.8%) |
|
| No |
5 (1.1%) |
86 (17.7%) |
25 (4.1%) |
56 (71.8%) |
172 (10.2%) |
|
*Education levels captured were according to Indian Education System, Illiterate or with minimal formal education – These women were either illiterate or had some education up to 3rd Grade. Completed Primary education – These women were 4th Grade pass, Completed Secondary education – These women were 10th Grade pass and Degree holders were women who had pursued Diploma/ Degree after Grade 10th or 12th Grade
Majority of women (48.1%) reported their family income above Rs. 10,000 per month. These were mainly from urban non-slum settings (62.1%), followed by urban slum settings (60.8%). Most women from rural settings (65.1%) reported their monthly income between Rs. 5001-10,000 per month. 38.5% and 32% women from Tribal settings reported their income between Rs. 5001-10,000 and upto Rs. 5000 per month respectively.
Most women in study population reported the onset of sexual activity above the age of 18yrs (64.7%) while 35.3% reported sexual debut below age of 18 years. These were mainly women from tribal population (70.5%) followed by women from urban slum (43.9%) settings respectively.
Overall, women in study population had low parity rates (0–2 children in 71.2% across settings). Higher parity rates (3 or more children) were more prevalent among tribal women (57.1%), followed by Urban Slum women (33.8%) and then rural women (31.4%).89.8% women reported that they had heard about cervical cancer, though awareness was significantly low among tribal women (71.8%).
The distribution of socio-demographic variables among women accepting HPV-SS was significantly different among the four groups (p-value < 0.0001) indicating a completely diverse population and varied settings. These findings support HPV-SS to have good acceptability among women across different diverse settings in state of Maharashtra, India.
As seen in Table 3, majority of women (87.6%) collected self-sample at home. 5.6% women collected self-sample in public toilet due to lack of privacy at home. Most of these, were women belonging to urban slum settings (19.1%). 6.8% women opted to collect their self-samples at camp place. All women from tribal settings collected their self-samples at the camp place and 5.9% women from rural settings opted for this choice. The prevalence of HPV detected through HPV-SS ranged from 4.4% among women in urban non-slums, 5.8% in urban slums, 5.7% in rural areas and 11.5% among tribal women. The overall average HPV prevalence across all groups was5.6%.
Table 3.
Acceptability, collection place and care trajectory of screen positive women in various settings
| Settings | Urban Non-Slum | Urban Slum | Rural | Tribal | Total population |
|---|---|---|---|---|---|
| 1. Collection of samples among women accepting HPV-SS | |||||
| N = 496 (%) | N = 485 (%) | N = 630 (%) | N = 78 (%) | N = 1689 (%) | |
| Home |
496 (100%) |
392 (80.9%) |
592 (93.9%) |
0 |
1480 (87.6%) |
| Public toilet | 0 |
93 (19.1%) |
1 (0.2%) |
0 |
94 (5.6%) |
| Camp place | 0 | 0 |
37 (5.9%) |
78 (100%) |
115 (6.8%) |
| 2. Screen positive rates on HPV-SS | |||||
| N = 496 (%) | N = 485 (%) | N = 630 (%) | N = 78 (%) | N = 1689 (%) | |
| Positive Test results |
22 (4.4%) |
28 (5.8%) |
36 (5.7%) |
9 (11.5%) |
95 (5.6%) |
| Invalid samples | 0 | 0 | 0 | 0 | 0 |
| 3. Compliance to referral among screen positive women tested by HPV-SS | |||||
| N = 22 (%) | N = 28 (%) | N = 36 (%) | N = 9 (%) | N = 95 (%) | |
| Hospital |
18 (81.8%) |
25 (89.3%) |
18 (50%) |
0 |
61 (64.2%) |
| Community camp* | 0 | 0 |
6 (16.7%) |
8 (88.9%) |
14 (14.7%) |
| Lost to follow up |
4 (18.2%) |
3 (10.7%) |
12 (33.3%) |
1 (11.1%) |
20 (21.1%) |
| 4. Care trajectory of screen positive women who did not comply for referral * (Cytology and VIA was conducted as triage tests for women in camp settings) | |||||
| Non-compliers for referral | N/A | N/A | N = 6 (%) | N = 8 (%) | N = 14 (%) |
| Normal on both test | - |
3 (50) |
4 (50) |
7 (50) |
|
| Abnormal on either test | - |
2 (33.3) |
3 (37.5) |
5 (35.7) |
|
| Abnormal on both test | - |
1 (16.7) |
1 (12.5) |
2 (14.3) |
|
| 5. Results of Pap Cytology among screen positive women on HPV-SS | |||||
| N = 18 (%) | N = 25 (%) | N = 24 (%) | N = 8 (%) | N = 75 (%) | |
| Negative for malignancy |
9 (50%) |
8 (32%) |
16 (66.7%) |
5 (62.5%) |
38 (50.7%) |
| Shift of flora to BV** |
6 (33.3%) |
9 (36%) |
5 (20.9%) |
0 (0%) |
20 (26.7%) |
| ASCUS & above*** |
3 (16.7%) |
8 (32%) |
3 (12.5%) |
3 (37.5%) |
17 (22.7%) |
| 6. Care trajectory of screen positive women referred to tertiary care | |||||
| Compliance to Colposcopy | 18 | 25 | 18 | 1 | 62 |
| 7. Histopathology reports | |||||
| Significant AWA on Colposcopy**** | N = 7 | N = 14 | N = 11 | N = 11 | N = 33 |
| Benign lesion |
6 (85.7) |
11 (78.6) |
7 (63.6) |
0 |
24 (72.7) |
| Precancer on biopsy |
1 (14.3) |
3 (21.4) |
4 (36.4) |
1 (100) |
9 (27.3) |
| 8. Compliance to treatment among women detected with pre-cancers | |||||
| Compliance to treatment |
1 (100%) |
3 (100%) |
4 (100%) |
1 (100%) |
9 (100%) |
*The Triage test used in camp settings was Pap cytology and VIA. Women with both tests positive were referred to Colposcopy at tertiary care centre
**Bacterial Vaginosis
*** ASCUS & above- (Atypical squamous cells of undetermined significance, low grade squamous intraepithelial lesion, high grade squamous intraepithelial lesion, atypical squamous cells, cannot rule out high grade cervical lesion)
****Significant Acetowhite area on colposcopy- Colposcopy Swede score 4 and above
The compliance rate for referral among screen positive women were 81.8% and 89.3% for Urban Non-slum and Urban slum settings respectively. The initial compliance to referrals was low for women from rural areas (50%) and tribal settings (0%). To address this low compliance rates, triage screening camps were arranged for these women in the community. This increased the compliance to referral among rural women by additionally 16.7%. The compliance rate to referral among tribal women was 88.9% with this strategy. The loss to follow-up was18.2%for Urban non-slum, 10.7% for Urban slum, 33.3% for rural and 11.1% for tribal women. Cytology and Visual Inspection with Acetic Acid (VIA) were used as triage tests in camp settings for women who did not comply to referral for Colposcopy.
Overall, Cytology test results of 75 women who complied with referral demonstrated that 50.7% had normal cytology, 26.7% showed a shift in vaginal flora towards bacterial Vaginosis (BV) - although no genital infection was reported on cytology and 22.7% women had abnormal cytology. The highest prevalence of abnormal cytology was among tribal women (37.5%), followed by women from urban slum population (32%). Among the women, who underwent triage testing in camp settings, two women, one from rural and one from tribal settings, had VIA positive lesions and demonstrated abnormalities on Pap report. Among them the women from rural settings failed to follow up.
Totally 62 women underwent Colposcopy at tertiary care centre. Among them,33 women underwent Colposcopy directed biopsies. The overall prevalence of precancerous lesions among these screen positive women was 27.3%. All women with diagnosed precancerous lesions were accompaniedby project staff to tertiary care hospital for treatment. The compliance for treatment was 100%.
Data on perception of HPV-SS was available for 1574 women. Table 4 looks at the key variables with respect to their perception of accepting the same; i.e. .Comfort experienced while performing the test; levels of anxiety experienced; confidence of performing the test after understanding the steps of HPV-SS; perceptions regarding the procedure to conduct the HPV-SS test; self-confidence about precision of test performed; concern of injury while performing the HPV-SS test and preferred modality of screening: Self-collection verses Physician collection, if given the choice.
Table 4.
Perception of HPV-Self sampling among the women who accepted self sampling
| Urban Non-Slum N = 496 (%) |
Urban Slum N = 485 (%) |
Rural N = 593 (%) |
Total N = 1574 (%) |
p-value | ||
|---|---|---|---|---|---|---|
| Comfort Level | No discomfort |
357 (72.0%) |
279 (57.5%) |
363 (61.2%) |
999 (63.5%) |
< 0.0001 |
| Mild discomfort |
132 (26.6%) |
189 (39.0%) |
226 (38.1%) |
547 (34.8%) |
||
| Moderate discomfort |
7 (1.4%) |
17 (3.5%) |
4 (0.7%) |
28 (1.8%) |
||
| Anxiety Level | No anxiety |
343 (69.2%) |
279 (57.5%) |
381 (64.2%) |
1003 (63.7%) |
< 0.0001 |
| Slightly anxious |
144 (29.0%) |
193 (39.8%) |
208 (35.1%) |
545 (34.6%) |
||
| Very anxious |
9 (1.8%) |
13 (2.7%) |
4 (0.7%) |
26 (1.7%) |
||
| Confident about method performing the test | Confident |
450 (90.7%) |
396 (81.6%) |
494 (83.3%) |
1340 (85.1%) |
< 0.0001 |
| Not confident |
46 (9.3%) |
89 (18.4%) |
99 (16.7%) |
234 (14.9%) |
||
| Perception of ease of performing the procedure | Easy |
289 (58.3%) |
264 (54.4%) |
326 (55.0%) |
879 (55.8%) |
0.0080 |
| Neutral |
192 (38.7%) |
189 (39.0%) |
251 (42.3%) |
632 (40.2%) |
||
| Difficult |
15 (3.0%) |
32 (6.6%) |
16 (2.7%) |
63 (4.0%) |
||
| Self-confident about Precision of performing the test | Not confident |
84 (16.9%) |
146 (30.1%) |
101 (17.0%) |
331 (21.0%) |
< 0.0001 |
| Fairly confident |
255 (51.4%) |
242 (49.9%) |
383 (64.6%) |
880 (55.9%) |
||
| Very confident |
157 (31.7%) |
97 (20.0%) |
109 (18.4%) |
363 (23.1%) |
||
| Concern of Injury | Yes/ Not sure |
7 (1.4%) |
14 (2.9%) |
6 (1.0%) |
27 (1.7%) |
0.0510 |
| No |
489 (98.6%) |
471 (97.1%) |
587 (99.0%) |
1547 (98.3%) |
||
| Preference of HPV-SS over Health personnel collected sample | HPV-SS preferred |
418 (84.3%) |
261 (53.8%) |
382 (64.4%) |
1061 (67.4%) |
< 0.0001 |
| Health- personnel performed test preferred |
78 (15.7%) |
222 (45.8%) |
211 (35.6%) |
511 (32.5%) |
||
| Neither of them |
0 (0.0%) |
2 (0.4%) |
0 (0.0%) |
2 (0.1%) |
The analysis of HPV self-sampling experiences reveals distinct patterns of user experiences across the settings. Women from the urban non-slum group reported the highest levels of comfort (72%) with no anxiety (69.2%) while performing the test. Most women (58.3%) found the test easy to perform, though some (38.7%) had neutral opinion. This group of women demonstrated highest confidence levels (90.7%) of performing the test.51.4% women were fairly confident and 31.7% were very confident regarding the precision of the test performed by themselves. Nearly all women (98.6%) in this group were sure that the test caused no injury. Given a choice, 84.3% urban non-slum women reported that they shall opt for HPV-SS as a preferred modality over health personnel collected sample. This group had highest HPV-SS preference as compared to women from other settings.
Women from the urban slum group reported lowest levels of comfort (57.5%). The anxiety levels while performing the test were reported to be marginally higher among these groups (39.8%) compared to the other groups. Most women (54.4%) found the test easy to perform, though some (39.0%) were neutral about opinion on this. The confidence levels for performing the test were reported to be lower among women in this group (81.6%) as compared to urban non-slum women (90.7%). Majority of women in this group were either not confident (30.1%) or fairly confident (49.9%) regarding the precision of performing the test. Nearly all women (97.1%) were sure that the test did not cause injury. Given a choice, 53.8% women reported that they would opt for HPV-SS over health personnel collected sample (45.8%), indicating mix preferences for HPV-SS.
Rural slum participants showed a balanced perception in regards to comfort levels (61.2%- no discomfort) and anxiety levels (64.2%-no anxiety). Many rural women were fairly confident about the precision of performing the test (64.6%). Nearly all women (99.0%) were sure that the test did not cause injury, though their preference for HPV-SS (64.4%) were moderate compared to urban non-slum residents.
Across all groups, concerns about injury were minimal (98.3% reported no concern of injury), and the perceptions regarding ability to perform the test were similar. The confidence about precision of performing the self-test and preferences of HPV-SS varied across the settings.
Discussion
The burden of cervical cancer remains high for developing countries like India. Achieving the WHO elimination target of incidence rate of 4/100,000 women is particularly challenging, given the current rate of 17.7/100,000 as reported by Globocan 2022 [4, 25]. To move closer to the globally set targets, the participation rate for screening should be around 70%. The study demonstrates overall initial participation rate of 66%, which ranged from 57.1% to 78.4% among women across different settings. These findings are consistent with participation rates reported in other Southeast Asian countries [26].
Although initial participation rates in the study were low, among those who enrolled, the acceptance of HPV-SS was high (98.2%). This high uptake can be attributed to the in-depth awareness and education provided to the participants. This is an encouraging finding highlighting the importance of ongoing efforts to raise awareness about cervical cancer prevention and early detection. Culturally appropriate, art-based health education material tailored to community’s level of understanding can have a significant positive impact on participation rates [27, 28].
Education levels and socio-economic status are influencing factors for disparities related to women’s reproductive health including cervical cancer. In this study, majority of participants across all settings had completed only primary education (58.1%). Most women from rural and tribal communities reported low income below poverty line. The burden of cervical cancer is mainly shared by marginalized population within the country, largely due to the high prevalence of reproductive risk factors that contribute to persistent oncogenic HPV infections, as reflected in the study. Early sexual debut was common, with 70.5% of tribal women, 43.9% of women from urban slums, and 38.7% from rural areas reporting sexual activity before the age of 18 [29]. High parity rates were most prevalent in tribal population, followed by slum and rural groups. Knowledge about cervical cancerand an individual’s perceived risk are major predictors of cervical cancer screening uptakes. Although 89.8%. of the total study population had heard of cervical cancer, awareness was significantly lower among tribal women.In contrast, higher awareness among women in urban non-slum and rural areas may be attributed to awareness campaign undertaken by government health systems and NGOs. However, data from NFHS-5 survey reveals a major discrepancy between the awareness levels and screening uptake, reflecting the continued influence of structural and population-level barriersto cervical cancer screening in India [8].
Our study reported high acceptance of HPV-SS among a population composed largely of never- or under-screened women irrespective of setting. Majority of women performed HPV-SS at home (87.6%) and those women who lacked privacy at home preferred collection at camp place (6.8%) or public toilets (5.6%). These findings support the potential of HPV-SS as a strong enabling factor - allowing women to screen themselves at a time and place of their choice - thereby increasing accessibility and autonomy in cervical cancer screening [30, 31].
The overall prevalence of HPV was5.6% which varied across the settings (4.4% to 11.5%). This is in consensus with the literature supporting the prevalence to vary by and within regions, due to many factors like socioeconomic development, culture, molecular variability of viral genome and human migration [19, 32, 33]. The prevalence of HPV among tribal community in our study was reported to be 11.5%. Poverty, low education levels and lack of knowledge about cervical cancer supports the high prevalence of HPV and precancerous lesions among tribal population in our study [27]. Our study findings indicate that HPV-SS has a huge potential to be an acceptable modality of screening among these hard-to-reach women.
The success of screening programs will depend on accessibility of screening test and compliance to referral of screen positive women. This ultimately depends on the distance to be travelled by women to get themselves screened and the availability of diagnostic and treatment facilities under one roof [34, 35]. Low cancer screening practices may be due to non-availability of screening facilities in the communities [36]. This aligns with our study settings, as there were no screening and diagnostic facilities available at Health care centres, nor at an accessible distance in the implementing areas. The urban non-slum and urban slum areas were located approximately 13 km from the tertiary care centre, while the rural setting was 63 km away, and the tribal setting was the farthest at 139 km. Additionally, the Accredited Social Health Activists (ASHAs) and paramedical staff had inadequate knowledge and skills to deliver cervical cancer screening and treatment of pre-cancerous lesions.
Recognizing that the distance to tertiary health care centre poses a significant barrier to referral compliance, we organized triage screening camps within health care centres in rural and tribal settings. This strategy served dual purpose: sensitizing local health care personnel to cervical cancer screening practices and improving referral compliance among screened women. As a result, referral compliance rates increased from 50% to 66.7% in rural settings and reached 88.9% in tribal areas. The compliance rates among rural women were significantly lower as compared to other settings. Although the study did not capture the specific reasons for low referral compliance in this population - an accepted limitation; it is possible that additional factors such as competing household responsibilities, or limited family support played a role. Future studies are warranted to explore these factors in greater depth and inform targeted interventions. Notably, treatment compliance among those diagnosed with precancerous lesions was 100% across all settings which may be attributed to project staff’s extensive experience and effectiveness in providing counselling and support. The prevalence of abnormal cytology among study population was high; with overall 26.7% demonstrating shift of flora towards BV, indicating the high risk of acquiring HPV infection [32, 37, 38]. The overall prevalence of abnormal cytology and precancerous lesion was 22.7% and 27.3% respectively among HPV-SS screen positive women. These abnormalities were significantly higher among rural and tribal women. These findings support the need for prioritising screening among these groups and also demonstrate HPV-SS to be an appropriate strategy. The current study used Pap and VIA as triage tests in community camps. The referral criteria being stringent for a better programmatic yield in trial settings may not be feasible in real world scenario. Screen and treat with thermocoagulation would have been a mitigation step to prevent loss to follow up especially in rural settings.
Though the results of acceptance and perception of the HPV-SS are encouraging, the precision and preferences of the HPV-SS over health personnel collected samples demonstrated varied reactions among the users across settings. The women from urban non-slum group were confident about performing HPV-SS (Fairly confident 51.4% and Very confident 31.7%) with good precision levels and preferred it (84.3%) over health personnel collected modality of screening. Marginally better educational levels in this group could be the contributing factor. Our findings are in consensus with literature, which supports precision of performing HPV-SS as a key issue in HPV-SS screening modality [39–41]. Though the confidence about precision of performing the test was low in the population, there were no invalid samples reported. Sharing this finding with the community is expected to boost their confidence and encourage greater participation in subsequent screening rounds of HPV-SS.
Conclusion
Our study demonstrated that HPV-SS has the potential to improve cervical cancer screening participation. In India, low participation rates in cervical cancer screening programs remain a significant public health challenge. There is a critical need for targeted awareness campaigns that are culturally appropriate, tailored to the needs and which address the concerns of the intended beneficiaries. This is likely to increase participation and reduce the burden of this preventable disease.
The fair confidence about method and precision of performing the test seen among women from rural and urban slum settings indicates the impact that HPV SS may have when introduced at a population level. Communities have faith in local stakeholders like doctors, paramedical staff, ASHAs and local leaders. Involvement of these stakeholders remains key for success of any screening programme in local context. This also necessitates upgrading the knowledge and skills of medical and paramedical staff at grass root level regarding awareness, screening, prevention, referral, and pre-cancer management algorithms.
While our study supports the effectiveness of HPV-SS in increasing cervical cancer screening coverage within research settings, its impact in real-world context must be closely monitored through organised population-based screening programs, especially in the context of referral for triage and treatment. Key feasibility concerns remain unresolved, including the mechanisms for distributing HPV-SS kits, the logistics of sample collection and transportation from remote communities to designated laboratories. Outcome of a screening programme depends upon preparedness of health care systems to deliver both screening and treatment services. This was lacking in our trial settings. In our study, HPV testing, diagnosis, and treatment were provided free of charge and screen-positive women were accompanied by study staff to tertiary care centres, given the absence of diagnostic and treatment services at the Primary Health Care Centres in the participating villages. These operational realities must be carefully considered by policy makers before implementing a nationwide cervical cancer screening program.
Acknowledgements
The authors would like to acknowledge Mr. Aryan Kadam, Clinical Research Intern, Department of Preventive Oncology, Tata Memorial Centre, Mumbai and Dr. Sayantika Kumari, Senior Research Coordinator, WECAN, Department of Preventive Oncology, Tata Memorial Centre, Mumbai, for their contributions for documentation and formatting work which supported this Manuscript.
Authors’ contributions
Concepts: G.A. and M.V. Design & funding acquisition: G.A. and M.V. Intellectual content: K.A., G.A. and M.V. Literature search: K.A., G.A. and M.V. Clinical studies: K.A., G.A., V.K. and M.V. Data acquisition: K.A., G.A. and V.K. Statistical analysis: K.A., G.A. and V.S. Manuscript preparation: K.A., G.A., M.V., S.P., V.K and V.S. Manuscript editing: K.A., G.A., S.P., V.K., V.S and M.V. Manuscript review: K.A., G.A., S.P., V.K. and M.V. Guarantor: K.A., G.A. and M.V.
Funding
We thank funding sources Terry Fox Foundation and ‘Funds for innovation and transformation program of Inter-council network of Provincial and Regional Councils (ICN), Global Affairs Canada’ (FIT) in providing financial support to conduct our trials.
Availability of Data.
Data availability
The data supporting the findings of the study shall be made available on reasonable request to the corresponding author.
Declarations
Ethics approval and consent to participate
This study was performed in line with the principles of the Declaration of Helsinki. The study protocol received ethical approval from the Ethics and Research Committee of the Institutional Review Board of Tata Memorial Centre, Mumbai, India (Project nos-1686 & 3786 ).
Consent for publication
Not applicable.
Competing interests
The authors declare no competing interests.
Consent to participate
All participants enrolled in the study were consented as per Institutional Review Board guidelines, on IRB-approved consent forms.
Footnotes
Publisher’s Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
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Associated Data
This section collects any data citations, data availability statements, or supplementary materials included in this article.
Data Availability Statement
The data supporting the findings of the study shall be made available on reasonable request to the corresponding author.