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HPV-DNA testing from self-sampled menstrual blood using M-strip: A proof-of-concept study on feasibility & acceptance of a novel biosampling method
For correspondence: Dr Somesh Chandra, Department of Surgical Oncology, KD Hospital, Ahmedabad 382 421, Gujarat, India e-mail: asaarhealth@gmail.com
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Received: ,
Accepted: ,
Abstract
Background & objectives
Screening for cervical cancer by self-sampling appears more acceptable to women and has the potential to boost screening uptake, which is dismal at present in India. Studies have shown that menstrual blood (MB) provides equivalent results to cervical smear for Human Papillomavirus (HPV)-Deoxyribonucleic acid (DNA) testing, but sample collection needs standardization. This study explored the feasibility and acceptance of self-sampling using ‘M-strip’ for high-risk HPV DNA (hr-HPV DNA) testing from MB.
Methods
One hundred and eleven women aged 30-50 yr without a previous diagnosis of pre-cancer or cancer used the M-strip to collect the MB sample. The strip was peeled off the sanitary pad after use, sent in a zip-lock pouch, and tested for high-risk human papillomavirus (hr-HPV) DNA by real-time polymerase chain reaction (rt-PCR). Instructions were provided verbally, in video illustration, and print. Feedback from participants regarding acceptance and comfort in sampling was documented, and from women who refused to participate.
Results
Seventy-seven women provided MB samples, all of which were evaluable. Six tested positive for hr-HPV DNA, and all six had direct cervical smears obtained subsequently. Randomly selected HPV DNA-negative MB samples were also tested by direct cervical smear. Positive and negative MB samples were 100 per cent in concordance with the findings from direct cervical smears. Participants expressed a high level of acceptance and preference for this method.
Interpretation & conclusions
Women could successfully collect adequate samples with the M-strip for hr-HPV DNA testing. Using M-strip with their sanitary pads was preferred by and highly acceptable to women in this study.
Keywords
Cervical cancer
HPV DNA
menstrual blood
screening
Cervical cancer continues to be one of the leading causes of cancer mortality in India and many low socio-economic countries1. A primary reason contributing to the high mortality is the poor uptake of the screening strategy using Papanicolaou (PAP) smear, which requires obtaining a direct cervical smear by a medical professional or trained healthcare worker. The low uptake of this conventional screening method in socio-economically challenged regions has been attributed to various factors. On the individual level, they include concerns about privacy, discomfort, and the need to visit a medical facility. For large-scale population-based screening, the issues of accessibility, resource constraints, and concerns about expertise and related costs have been faced. Based on the World Health Organisation (WHO) guidelines, the conventional cytological testing of the cervical smear sample has been replaced by testing for high-risk human papillomavirus (hr-HPV) DNA2. Secondly, to make screening more inclusive, efforts are made to evaluate self-sampling methods for obtaining the sample for hr-HPV DNA testing. Most of the studies were done in the Western world, but an Indian study showed that self-sampling is preferred over a physician-collected sample. The currently used self-sampling methods, however, remain interventional as they need a vaginal sample to be collected by women themselves. Moreover, vaginal self-sampling method has been found to evoke concerns in users regarding self-inflicted trauma during the process and also doubts about the adequacy of sampling. The sample also needs to be stored and transported in a liquid medium. Furthermore, to bring down cancer mortality in low-resource countries, any self-sampling method should be scalable for large-scale adoption and cost-effective for widespread use. A dried sample of MB has been shown in multiple studies to be a reliable source for diagnosing hr-HPV DNA infection compared to direct cervical smear3. This approach carries the dual benefits of being a self-sampling and a non-interventional passive technique. Two conceivable issues, as yet, remain unaddressed: first, its acceptability to women in our country, and second, the availability of a uniform, easy, practicable, and reproducible technique to collect the sample. This emerged from one of the large studies of HPV DNA testing on MB, conducted in India, which showed high acceptance, but a precise and uniform method to obtain the sample was not available. An acceptable and easily reproducible technique carry the potential of higher uptake as a screening modality with scalability at the population level. It can be particularly useful in low-resource countries if it is also cost-effective, and usable in areas remote from advanced health facilities.
This proof-of-concept study was undertaken to examine the feasibility and acceptance of a novel method of hr-HPV DNA testing using a sample of self-collected menstrual blood on menstrual pads using a specially designed sampling strip (M-strip). The cost-effectiveness and scalability are also discussed.
Materials & Methods
This is across-sectional study (study name: ASAAR PS-1) designed and undertaken by the department of Surgical Oncology, Sterling Hospital, Ahmedabad, Gujarat, India and the protocol was submitted to and approved by the Institutional Ethics Committee. The participants were enrolled from September 2023 to March 2024.
Inclusion/Exclusion criteria
The inclusion criteria were: (i) women aged 30-50 yr, (ii) not previously diagnosed with cancer or pre-cancer, which were in accordance with the WHO recommendations. The exclusion criteria were: previous history of genital/oral cancer, since a screening test is typically not performed in those who have already been diagnosed. Women who met the criteria were recruited after obtaining informed consent. None of the participants reported having been tested earlier for HPV.
Sample size
This was a pilot feasibility study. In this cross-sectional investigation, the sample size was calculated with a 95% level of confidence (α/P=0.05, Z=1.96), population incidence rate of 6 per cent, and a random sampling error of 5 per cent; the total number to be recruited was 87. Allowing for a 20 per cent dropout, the minimum number required for enrolment was 1084.
Sample collection
The participants were explained about the sample collection method and also provided a short video clip showing the steps for collection. They were then provided a ‘collection kit’ containing (i) specially designed strips (licensed by Central Drugs Standard Control Organization, Government of India; Supplementary Figure) for sticking on to the menstrual pad to be used, (ii) a pouch to transfer the used strip after peeling it off from the used menstrual pad, (iii) a printed pictorial version of the instructions for using the strip on their menstrual pads, and (iv) a pair of disposable gloves. No specially designed menstrual pad was used, and women could use any of their choice after sticking the strip over the absorbent area of the pad. The first day of the menstrual bleed was the preferred day for sample collection, but samples collected on day 2 were also accepted. The strip was peeled off the used pad after 4 h or when the pad was to be discarded. The pad was discarded as usual, and the strip was placed in the zip-lock pouch provided with the kit and sent to the nearest designated laboratory. All samples were analysed at the National Reference Centre of Laboratory (NABL-accredited), participating in the study.
The collection strip
The M-strip was developed in collaboration with IOTA diagnostics at Gandhinagar, Gujarat, India. The M-strip (Supplementary Figure) comprises three collection discs made of hydrophilic porous materials (Collection Matrix) arranged between two thin polypropylene membranes. The porous material precisely absorbs the blood and other biofluids with a defined volume (50 μl x 3). Afterwards, the device can be stored at ambient temperature and shipped to the laboratory for analysis. An adequate sample collection was deemed done when at least one of the three dots was blood-stained when the strip was peeled off. Each participant submitted one strip.
The feasibility measures were: (i) the proportion of women who attempted and could collect and submit the sample using the kit provided, and (ii) the proportion of submitted samples that were adequate for testing.
Sample testing for hr-HPV DNA
The testing was done at the National Reference Centre of Sterling Accuris Laboratory, Ahmadabad, Gujarat, India. For the extraction of DNA from the strip with the MB sample, Qiagen (Hilden, Germany) QIAamp DNA MiniKit (Qiagen, Germany) was used with a modified protocol. Sample collection discs were separated with sterile forceps from the strip. One of the discs was added to 20 μl of Proteinase K and 200 μl of lysis buffer provided by the kit in a micro-centrifuge tube. The tube was vortexed for 10-15 sec and briefly centrifuged. The tube was incubated at 56˚C for 10 min. After incubation, DNA was precipitated using absolute ethanol. Tube contents were transferred to a QIAamp mini spin column, and the disc was discarded. DNA was further purified as per the kit manufacturer’s instruction manual protocol. The unused sample collection discs were stored at 2-8°C for future use (if any).
For the detection of HPV DNA, a Taqman probe-based real-time PCR test was performed with HPV-HR RealAmp Kit (OSANG Healthcare, South Korea). Positive and negative controls were used in every run. The recorded fluorescence values emitted by the specific probes and the specific internal control probe in the amplification reactions were analysed by the software of the CFX96 thermal cycler from Biorad (California, United States). The samples were considered evaluable if the internal control was amplified. HPV DNA positive samples were further tested for HPV Genotyping with Anyplex HPV HR Detection Kit (Seegene, South Korea) covering 14 High-risk genotypes (Genotype 16, 18, 31, 33, 35, 39, 45, 51, 52, 56, 58, 59, 66 and 68).
All women who tested positive for hr-HPV in the menstrual blood had a PAP smear obtained by a doctor, which was also tested for HPV DNA and cytology using the liquid-based cytology (LBC) technique. Direct cervical smears were also obtained from randomly selected women who had tested negative for HPV on a menstrual blood sample. Women testing positive were counselled to pursue appropriate work-up for further management and/or observation. All women participating in the study were encouraged and instructed to pursue the standard cervical screening program irrespective of the test results.
Participating women were asked to voluntarily provide feedback on an electronic online form. Women who were screened but refused to participate were also requested to indicate the reasons for not participating in a pre-designed form. A response from a minimum of 60 per cent of the participants was considered adequate to come to a valid inference from the survey5. Statistical significance of the observed differences was measured by the Chi-square test. Even though cost analysis was not one of the objectives, at the conclusion of the study, an estimate of the cost of testing per sample was mentioned.
Results
A total of 140 women were screened for eligibility, and upon satisfying the inclusion criteria, were invited to participate in the study, of whom 111 (79%) consented to participate. Of the 111 consenting women, 77 (69.4%) submitted samples within the pre-defined study period. Of the 34 women not providing sample, 23 of them forgot to collect the samples on day 1 or day 2 of the menstrual cycle, two had conceived, seven were diagnosed with polycystic ovarian syndrome, and two were in the perimenopausal state, leading to irregular menstrual cycles. Six out of 77 (7.8%) samples were found to be positive for hr-HPV DNA in menstrual blood. All 77 samples were deemed adequate for evaluation by the internal control in testing. Five out of six positive samples had a single hr-HPV genotype, and one had mixed genotypes. The MB samples collected by M-strip and the direct cervical smear samples showed 100 per cent concordance in matching genotypes. The interval between MB sample and direct cervical smear was 5-27 days (mean 10 days).
Of the 71 women testing negative for HPV DNA in their menstrual blood, 10 (14%) were randomly selected for HPV testing on cervical smears, and all tested negative again (100% concordance; Figure). In women who tested negative on MB, randomly selected women underwent a direct cervical smear examination between 10 and 79 days after (mean 37 days) the MB test result.
- Flow chart of testing process and results. RTPCR, real-time polymerase chain reaction; LBC, liquid-based cytology; LSIL, low-grade intra-epithelial squamous lesion; HSIL, high-grade intra-epithelial squamous lesion; IC, invasive cancer; HPV, human Papilloma Virus.
The six women who tested HPV positive and the randomly selected 10 who tested negative for hr-HPV DNA underwent liquid-based cytology (LBC) examination; none (0/16) showed any atypia, Cervical Intraepithelial Neoplasia (CIN) or malignancy. Only two of them showed inflammatory changes. Regarding the suitability of the menstrual blood sample for HPV DNA testing, all the submitted samples were found adequate for DNA extraction. All samples were analysed within 10 days from the time of collection of the sample and seven days from the time of receiving at the laboratory. Five of the samples testing positive were collected on day 1 of the menstrual cycle, and one was collected on day 2. Overall, 53 samples were collected on day 1 and 24 on day 2.
The first set of response forms was submitted by 24 out of 29 women who did not consent to participate. The refusal to adopt MB as a sampling source was evinced by a small minority, and the majority refused to participate due to general resistance to screening (Table I). Of the 77 women who participated, 48 (62%) submitted their responses about the study. Nine questions were asked. The majority (47/48) of the responders indicated preference for the method of sample collection, one indicated preference for sample by doctor/healthcare worker (P<0.01). Only a quarter of women (7/28) preferred submitting a whole pad, while 75 per cent indicated preference for using the specially designed stick-on M-strip for collection of samples from menstrual blood (P<0.01; Table II).The overall cost per test, including the cost of the kit and laboratory testing, was approximately 12$ USD.
| Reason | No. of participants |
|---|---|
| It feels unhygienic to deal with menstrual blood | 1 |
| I fear it can be used to cause me harm | 1 |
| I do not want to be tested/screened for cervical cancer | 9 |
| My family will not allow | 4 |
| I have been checking regularly; I don’t trust new things | 2 |
| Other | 7 |
| Feedback question | Option | Responses (in %) | Interpretation | P value |
|---|---|---|---|---|
| If you have to choose between this method & going to a clinic for testing by doctor or nurse, which would you prefer? |
This method. At clinic by doctor or nurse. |
A. 47 (97.9%) B. 1 (2.1%) |
Self-sample collection is preferred over collection by doctor or nurse. | <0.01 |
| If you have to choose one of these, what is your choice? |
Provide whole pad. Use strip. |
A. 38 (79.2%) B. 10 (20.8%) |
Sample collection from strip is preferred over whole pad | <0.01 |
| Which of these would you prefer? |
Applying strip yourself to pad of your choice. Use pad and strip provided in one pack. Use pad ready with strip stuck on to it. |
A. 30 (62.5%) B. 3 (6.3%) C. 15 (31.2%) |
Prefer to use own pad with strip provided separately. | <0.01 |
| Was the Sample collection strip comfortable? |
Very comfortable. Not much comfortable. Uncomfortable. |
A. 45 (93.7%) B. 3 (6.3%) C. 0 |
Use of strip is most comfortable. | <0.01 |
| How was the overall guidance for the Sample collection? |
Very useful. A little confusing. Not useful at all. |
A. 48 (100%) B. 0 C. 0 |
Guidance of sample collection is very important and useful | <0.01 |
| Did you find any challenges at a time of sample collection? |
Strip didn’t stick with pad properly. At a time of removing a strip, collection dots came out. Strip felt very irritating and inconvenient. No challenges. It was little tricky to transfer sample collected strip to the sample storage box. The strip end was irritating. The container mouth should be broad as strip used to stick over inner surface and difficult to push inside to close the lid. |
A. 3 (6.2%) B. 8 (16.7%) C. 0 D. 34 (70.8%) E. 1 (2.1%) F. 1 (2.1%) G. 1 (2.1%) |
Transfer of sample from pad to pouch is very crucial and easy for majority. The strip is very convenient for over 95% of users |
<0.01 |
| How do you define sample collection process? |
Unhygienic Kit. Components made it very convenient & hygienic for me. None of the above. |
A. 0 B. 45 (93.7%) C. 3 (6.3%) |
Components made it very convenient & hygienic. | <0.01 |
| Did you understand the clinical significance about this testing? |
Fully understood. Partially understood. Not understood at all. |
A. 47 (97.9%) B. 1 (2.1%) |
Fully understood | <0.01 |
| Would you recommend the test to your relatives or friends? |
Yes No Maybe |
A. 47 (97.9%) B. 1 (2.1%) C. 0 |
Yes, they will recommend the test. | <0.01 |
Discussion
Cervical cancer ranks second in cancer mortality in women in India and in many other countries with limited resources. It has been shown that the mortality from cervical cancer can be reduced by nearly 80 per cent by a simple screening test like PAP smear when performed regularly2,6-8, and followed by appropriate intervention. However, the uptake of this mode of screening has been dismal9. The principal reasons for this poor participation are the need to visit a medical facility, the discomfort in going through the test, and concerns about privacy10.
Since over 85 per cent of cervical cancers are caused by certain high-risk HPV strains, co-testing for HPV DNA with LBC had been mooted. Still, the International Agency for Research on Cancer (IARC) statement pointed out that, potentially, the benefits did not outweigh the harms11,12. Besides, the issues about access, privacy, discomfort, the resource requirement and cost remained the same since the sample collection required similar technological approach. The US FDA, in 2014, approved HPV DNA testing as a single test for primary cervical cancer screening modality in specific context8. In 2021, the WHO recommended testing for HPV DNA alone as the preferred screening modality.
Furthermore, in an attempt to increase the uptake of screening, other methods of obtaining a sample for HPV testing, in the form of self-collected vaginal samples were evaluated and very recently approved by the US FDA13,14. In this method, using a brush or spatula, a woman can collect samples from the vagina. There were favourable reports about its efficacy as a screening method for cervical cancer15,16.
However, doubts persist over the accuracy when it is performed at different times during the menstrual cycle17,18. Women themselves have expressed concerns about proper sample collection. As a recourse to easing concerns about any intervention, HPV testing on menstrual blood was explored19. Initial studies performed on women known to harbour high-risk lesions or cancer showed that the accuracy of HPV DNA testing on menstrual blood was as high as that done on a direct cervical smear20. However, such studies did not directly address the issue of screening an untested population, even though a good concordance was shown for high-risk HPV between samples from menstrual blood and cervical sample21. The potential use of menstrual blood as a screening tool for cervical cancer gains leverage from very few studies7. The only study from India tested over 500 women. This landmark Indian study provided the proof of concept for using menstrual blood for HPV testing as a screening tool; however, it raises one more concern, namely, a standardised sample collection method, which was not ascertained in the Indian study22. The randomised study by Naseri et al19 using the ‘Q-pad’ was a step in this direction of standardising the methodology, which re-confirmed the performance of MB as a reliable sample for hr-HPV testing19. To implement it on a mass scale, however, as a population-based method, the user acceptance needed further elucidation. The current study, even though small in sample size, addresses precisely those issues. Our results of HPV positive population without atypia, dysplasia, or cancer are similar to those reported historically, being 7.8 per cent in our series, which compares well with earlier reports of positivity in women without pre-cancer or cancer23. In this study, the uptake of this novel method was high, approximately 80 per cent, reaching desired levels as proposed by the WHO, which promises to address the main concern with screening programmes. The patients’ responses also reflected the ease of sample collection and transport to the laboratory, being a ‘dry’ specimen, and preference for the method by using a small strip instead of the whole pad. Additionally, with the use of the strip, a special pad is not needed for sampling and testing. Instead, they use one of their own preferences; this again seems to be a preferred path to pursue, as evinced from the feedback of participants. The idea of using self-sampling for hr-HPV DNA testing in an unscreened, healthy population eliminates the need for using an intervention for obtaining a cervical smear. It thus potentially eliminates the need to obtain a smear on more than 90 per cent of the target population initially. Those who test positive can be expected to be more motivated to undergo further testing. The HPV positive women need to be reassessed for persistence of infection (the body’s immune response clears the majority of infections) and, in those with persistent infection, for any pathological changes. A negative test also helps by eliminating the need to test that large population for at least another five years. The objective nature of DNA tests and the ability to centralise the testing could also help to overcome the challenges inherent in PAP smear testing, namely targeting the proper area for proper smear collection, and the subjectivity in processing and reading the smears. Furthermore, the use of MB as against self-sampled vaginal samples appears to be a further welcome step towards higher acceptance of testing. The issue then remains about developing a reproducible, easy, and reliable method of obtaining MB samples for such testing. All three objectives, namely, self-sampling, non-interventional, and reproducible collection technique, were addressed in this study. Even though conducted with a small sample size, it opens the prospects of higher scalability with ease of participation and simplification of the sample collection process.
This study also tried to look at the quality parameters outlined by the WHO for implementing a screening programme. It remains to be seen whether the indicators of performance remain at the desirable or essential levels, but in this study, they were achieved as indicated by the proportion screened (80% consented), and 70 per cent were screened. There was 100 per cent concordance with conventional methods in both positive and negative results. Most importantly, the overall cost per test, including the cost of the kit and laboratory testing, was well within the WHO recommendation of 15$ USD2. The principal drawback of the study was its small sample size. However, this is presumably the first study from a low-resource country to document a reproducible, non-interventional, scalable, and highly acceptable method within the desired cost as outlined by the WHO by adopting a proven method for hr-HPV testing.
Overall, this cross-sectional study demonstrates that screening for cervical cancer using menstrual-blood-based hr-HPV DNA can be standardised, with high accuracy and acceptance at a low cost. It raises the prospects of implementing it as a state-funded larger program to ascertain and achieve the desired level of uptake for cervical cancer screening and reduce the related mortality thereof.
Declaration
This was an investigator initiated study. M-strip was provided by IOTA diagnostics. Laboratory support was provided by Sterling Accuris Wellness Pvt. Ltd. There was no financial compensation for investigators. There was no financial cost borne by participants.
Acknowledgment
Authors acknowledge Mr. Harsh Patel for co-ordinating programme with participants and help in preparing instruction manual.
Financial support & sponsorship
None.
Conflicts of Interest
None.
Use of Artificial Intelligence (AI)-Assisted Technology for manuscript preparation
The authors confirm that there was no use of AI-assisted technology for assisting in the writing of the manuscript and no images were manipulated using AI.
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