Community cancer screening at primary care level in Northern India: determinants and policy implications for cancer prevention

Introduction

Globally, cancer is the second leading cause of mortality, accounting for one in six deaths (estimated 9.6 million deaths).1 India contributed to 6.9% and 8.6% of global cancer incidence and mortality, respectively.2 The estimated age-adjusted rate of cancer for the Indian population in 2022 was 107 per 100 000, with a female preponderance. Overall, breast, oral cavity and female genital system were among the top three leading cancer sites in India.3

Population-based clinical trials from India have demonstrated the impact of screening in the form of significant downstaging and cancer-related mortality reduction through oral visual examination (OVE), visual inspection of the cervix after staining with 5% acetic acid (VIA) and clinical breast examination (CBE). These screening methods are cost-effective and can be performed by trained front-line workers (FLWs).4 Despite the observed benefits of these methods and the operational guidelines for cancer screening by the Government of India (GOI),5 the recent National Family Health Survey (NFHS-5; 2019–2021) reported poor cancer screening coverage.6 Moreover, cancer care pathway studies from India have shown that it takes 2–9 months to diagnose cancer after the onset of symptoms.7 Thus, the majority of cancers in India are diagnosed in advanced stages with a poor prognosis.8

In Uttar Pradesh state, the reported proportion of women (aged 30–49 years) who ever had oral, breast or cervical cancer screening was 0.6%, 0.4% and 1.5%, respectively, and the proportion of men who ever had oral cancer screening was 1.1%.6 The National Programme for Cardiovascular Diseases, Diabetes, Cancer and Stroke (NPCDCS) has established a referral system for cancer suspects, where the FLWs have to screen all men and women (aged 30 years and older) for tobacco use and cancer-related symptoms through the community-based assessment checklist (CBAC) and then refer the high-risk persons to the nearest health and wellness centre for further screening and diagnosis.5 9 10 However, a recent study that cross-surveyed the state of screening in a rural Indian setting found that suspected cases of oral and breast cancer were not recorded under the NPCDCS. They also reported a lack of cervical cancer screening in the study area.11

Thus, by far, programme-based cancer screening is lacking, and there is a delay in reporting by the patients to the healthcare system even after symptom development due to a lack of cancer awareness. The community-based camps supported by various stakeholders can help bridge the gap.12 These camps also provide a learning opportunity to understand the context-specific challenges in cancer screening and can help in developing potential interventions. The WHO advocates context-specific research to identify barriers and develop pragmatic solutions.13

With this background, a community service-based project was developed and implemented in rural settings of Uttar Pradesh state of India to screen the eligible population for oral, breast and cervical cancer, in line with the NPCDCS guidelines. This study aimed to describe the determinants for oral, breast and cervical cancer prevention, focusing on screening outcomes, follow-up compliance and implementation challenges at the primary care level in a rural community in Northern India. We have discussed the policy implications based on study findings.

Materials and methods

Navigation

A trained PN, who was a local resident, enlisted the SPs during the camps and navigated the willing SPs from the block to the TCC, using the local mode of transport and incurring expenditures from the allocated funds. There was a large proportion of SPs not willing to attend the TCC despite face-to-face and telephone counselling on several occasions. To ensure that these unwilling SPs continue to be part of our surveillance, we invited them after 4–6 months of the first screening to undergo follow-up screening at the local health centre, school or panchayat, where the doctors from the screening team categorised them as high-risk,16 and were again counselled to visit the TCC for a diagnostic evaluation of the lesion. This methodology was termed ‘reverse navigation’ (figure 1). Participants were given symptomatic treatment during the screening and reverse navigation. The SPs who attended the TCC were diagnosed and treated as per the guidelines of the WHO,17 National Cancer Grid18 and the Oral Cancer Task Force.19 TCC offers multidisciplinary treatment with state-of-the-art facilities at a subsidised cost and has social support schemes for cancer treatment for poor patients. The SPs who did not attend the TCC were advised to visit their nearby health centres.

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Figure 1

Flow diagram for cancer screening and navigation for the Cholapur block, Varanasi, Uttar Pradesh, India. TCC, Tertiary Cancer Centre.

All participants with positive habit history were given a brief behavioural intervention and tobacco Quitline number for tobacco cessation during screening as well as follow-up visits. All SPs are under the surveillance of the preventive oncology division, along with the Varanasi PBCR and surveillance findings will be reported in future studies. The screening findings were shared with ASHA and ANM to supplement the CBAC forms for population surveillance.

Results

A total of 190 camps were conducted over the period of 1 year, during which 14 371 residents were registered and 14 338 residents (99.8%) were screened. Though we aimed to conduct 200 camps in the mentioned period, due to the disruptions related to the COVID-19 pandemic, screening activities were temporarily withheld. We observed lower screening participation during the third wave of the COVID-19 pandemic (January 2022 to April 2022). Full-day camps (6–8 hours) were organised, and the average attendance during camps was 63 (18–125 people).

Discussion

The proportion of the population who underwent screening for oral, breast and cervical cancer in Uttar Pradesh is below the national average (NFHS-5).6 A camp-based approach is a commonly practiced measure to augment the screening of cancers in such settings.22 We observed good participation (14 338/14 371; 99.8%) during the camps. The possible reason for this good response could be the availability of camps near the homes and workplaces of beneficiaries, as most of the screened population were farmers or housewives. Despite the availability of a non-invasive, simple test like OVE, we observed lower male participation (38.1%) compared with females (61.9%). NFHS-5 data stated that <1% of males self-reported OVE.6 There could be several socio-contextual factors attributing to lower male participation, like (1) paucity of time due to occupation, (2) resistance to quitting tobacco, (3) low perceived severity of lesions, etc and this calls for explorative research.23

Though almost all women consented to OVE, less than half consented to breast and cervical cancer screening. The high refusal rate can be partly explained by the high proportion of illiterate women in the present study; however, no association was found between education and screening participation. A previous study reported that willingness for cancer screening is positively associated with education.24 The refusal rate for breast and cervical cancer screening was significantly higher among older (≥50 years) women compared with the younger (<50 years) population. Previous Indian studies have reported epidemiological findings for sexually transmitted/reproductive tract infection (STI/ReTI) in the reproductive age group. However, older women, who are at increased cancer risk, are less likely to participate in screening.25 Older women internalise their reproductive health issues as part of a culture of silence about their health or because they are scared or ashamed to disclose a sexually transmitted disease.26 Another reason for screening refusal could be a lack of symptoms, which are more prevalent in sexually active women.27

In our study, about 22% of breast and 12% of cervical SPs were aged ≥50 years. Thus, the unmet need for cancer screening for women near and after the stopping age of screening should be addressed.28 Exploratory research to understand and overcome these barriers is required to increase screening participation among older women. Due to the nature of this service-based project, we were required to cover all the identified screening sites in the study area in a time-bound manner. Hence, those women who refused screening during the camps were counselled to undergo screening at the TCC or the nearest health centre.

About 2% of the study population was younger than 30 years. These women were sexually active and had gynaecological issues. Poor genital hygiene and associated STI/ReTI are important contributory factors for cervical carcinogenesis.29 Though the GOI guidelines have set the age of screening initiation at 30 years, young symptomatic women should also be offered screening, counselling for reproductive health and appropriate management as part of cancer prevention.

We offered screening to the younger symptomatic women for the following reasons: (1) About 8% of the 15-year-old Indian women have a sexual debut and the median age for first sexual intercourse is 17.8 years,30 (2) 1.3% of total registered cervical cancers by the 26 population-based cancer registries (2012–2014) were in the 20–29 age group,31 (3) the acceptance rate for cancer screening is reportedly higher in younger women as they are mostly symptomatic who have been categorised as high-risk for cervical cancer,32 (4) studies have reported that in the absence of screening younger women tend to delay the care-seeking for cervical cancer33 and (5) lastly, for ethical reasons and to benefit the community at large, the screening was extended to them as well.

We observed a higher proportion of tobacco use among men (56.6% SLT; 7% smoking) and women (20.4% SLT; 1.7% smoking) compared with NFHS-5 (National and Uttar Pradesh) reports.6 Hence, screening, along with robust tobacco cessation interventions, is essential for both men and women in the study settings. Passive smoking and chulha use were prevalent among the study population, contributing to IAP. In 2016, the GOI introduced the Pradhan Mantri Ujjwala Yojana to help rural women acquire clean cooking fuels and lower their health risks from IAP through biomass fuel burning.34 Further research is required to assess the health-related impact of IAP in the community and the implementation challenges of the Ujjwala scheme, which may explain the high proportion of IAP in the study population.

Out of 14 338 participants, 732 (5.1%) were SPs, of which male SPs (oral lesions; 6.5%) accounted for a significantly higher proportion compared with female SPs (oral/breast/cervical lesions; 4.2%). The SPs proportion was similar to previous studies,35–39 but some studies conducted mainly in Southern India showed higher screen positivity for cervical cancer.21 22 40 41 Screen-positivity was significantly associated with any form of tobacco use which is a well-recognised risk factor for various cancers. Our finding is supported by the Varanasi PBCR report where one-third of the registered cancers were tobacco-related.14 Oral lesions were significantly higher in men compared with women (p<0.05) owing to higher substance use among men and implicating their role in oral lesions. A significantly higher proportion of SPs had the intention to quit tobacco compared with screen negatives. Similar results were reported in previous studies,42–44 possibly because they attribute their symptoms to tobacco use and the realisation that tobacco cessation can have positive health outcomes.43 Awareness of the presence and consequences of potentially malignant disorders also motivates tobacco cessation.42 However, due to the nature of the study design, we cannot establish a temporal relationship between screen-positivity and intention to quit tobacco. Screening camps, therefore, present an appropriate opportunity to supplement and intensify tobacco control efforts.

In the present study, the presence of symptoms was significantly associated with screen-positivity. Previous study has reported that individuals with symptoms were more likely to participate, and the yield of screening is also higher among them compared with those who are asymptomatic.32 We observed that contraception use was significantly associated with screen-positivity. It is possible that the patients started using contraceptives either because of some STI/ReTI symptoms or because the use of contraceptives led to gynaecological issues as reported in previous studies.45 46 Due to the time-bound nature of the project, it was difficult to ascertain the temporal relationship between contraception use and screen-positivity and needs prospective research.

A good screening participation could not translate to follow-up, where less than one-third (30.1%) of SPs were compliant through reverse navigation. We observed that proxy variables for poor health literacy, such as alcohol use, passive smoking, burning biomass fuel for cooking and illiteracy, were associated with lower follow-up rates (on univariate analysis). This finding is in line with several studies from India and other lower-income and middle-income countries.47 The mean age of the participants who complied with follow-up advice on reverse navigation was higher than those who did not. A previous study reported longer diagnostic delays in young cancer patients compared with older patients.48 The possible reasons could be that the younger population might be engaged in their household and occupational activities, therefore having a paucity of time for follow-up. In our study, a significantly higher proportion of the unemployed population complied with follow-up advice compared with service class and daily wagers. This highlights the importance of providing screening as well as follow-up services closer to the workplace. Previous studies on mobile-health technology have also reported better compliance with follow-up in workplace settings.49

Screening is just one part of the cancer care continuum, which includes timely referral, appropriate treatment and surveillance to ensure completed care pathway. Several factors at the individual level, community, health systems and national levels affect this continuum, such as (1) poor health and cancer literacy, (2) cancer fatalism and stigma, (3) low perceived severity of precancer lesions, (4) lack of time and resources for undergoing treatment, (5) lack of faith in the health system. The contribution of these factors as barriers to screening and follow-up is heterogeneously distributed among different geographical populations.50 WHO advocates context-specific research to identify these factors and develop pragmatic solutions to overcome these barriers.

Even after reverse navigation, only 25.3% (19/75) of SPs visited TCC. This could be because the TCC was distantly located from the screening site, and barriers, especially lack of time and mode of transport, were the most cited reasons by SPs for follow-up refusal. Early symptoms can be a push factor for individuals to get screened, and that too when provided close to home, but they are not enough to drive people to seek treatment at a relatively distant hospital. This was evident in our study as symptoms were associated with screen-positivity but not with follow-up compliance. Almost similar findings were reported from different parts of India. In rural Karnataka, only 9.2% of SP women with cervical lesions visited the referral centre.22 Follow-up rate was 22% among the SPs in the rural male population for oral cancer screening in Uttar Pradesh.51 Mobile-based study from Tamil Nadu reported that 30.8% of SPs attended follow-up.52 Maharashtra-based study showed 100% compliance for treatment at campsites but only 20% for treatment at clinics, other than campsites.41 This highlights the importance of establishing model rural comprehensive cancer care centres.53 High loss to follow-up rates for VIA-positive women was reported in Mysore, which improved after providing same-day confirmatory testing, emphasising the need to bring not only screening but also follow-up care to women as much as possible.54

Apprehension towards tertiary healthcare facilities, including fear of being lost in a big hospital in the absence of any navigator, has been identified as a barrier by women for breast cancer screening in rural population of Karnataka.54 Navigation is an important pillar of the screening continuum,50 and a fractured navigation pathway could be a deterrent for cancer prevention and care. In a study, a high compliance rate was observed, partly due to the arrangement of a two-way transport vehicle for the referred women, availability of health workers at the nodal hospital and counselling sessions by doctors and medical-social workers for those attending the referral.35

The low follow-up rates among men compared with women, both during reverse navigation and after referral to TCC, were similar to the oral cancer screening trial in Kerala,37 and highlight the low perceived severity of disease among men. This could have impacted the overall follow-up rates for both men and women; as generally, men are the decision-makers in Indian families. According to a rural population study from Mysore, some VIA-positive women refused treatment when pelvic rest was advised following treatment because they were afraid of violence if they declined sexual contact. Therefore, including men in women’s health initiatives is important for screening as well as follow-up treatment.39 51 In addition, self-sampling for human papillomavirus testing which has been validated in Indian settings can help overcome some of these barriers as embarrassment, post-test discomfort, fear of visiting hospitals, distance and cost of travelling.13

Conclusion

We observed a high rate of tobacco usage in the Varanasi rural population, predominantly in men. Our study also found high screen-positivity among men, despite their lower screening participation. There are plenty of ongoing cancer screening projects for women, while very few community projects focus on the male population. The NFHS-5 data shows poor screening coverage in both sexes. Hence, male representation in community-based cancer screening is equally important.

Time-limited and target-based projects may help in identifying the high-risk population and early detection of lesions that require regular behavioural intervention, treatment and surveillance. However, they do not provide an adequate time frame to study the impact of such a camp-based approach on cancer control. Hence, continued surveillance of the screened-positive cohort is essential for cancer prevention.

We observed low male participation in oral cancer screening, high refusal for breast and cervical cancer screening among women and poor follow-up compliance despite counselling service, supporting vehicle, PN and free diagnostic service at the TCC. This reflects the need to understand the socialcultural factors through qualitative research and develop context-specific interventions to enhance screening participation and follow-up compliance. Previous studies in developed and developing countries have reported that establishing TCC may not always improve early detection and timely referral, especially in the rural population.55 Community cancer screening needs strengthening through cancer awareness, establishing referral system and integration with the National Tobacco Control and Cancer Registry Programmes. Unless the implementation challenges identified in real-life settings for cancer screening are appropriately addressed, patients with oral, breast and cervical cancer will continue to be diagnosed in advanced stages and eventually the theme ‘close the care gap’ will remain unjustified.