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Barriers and facilitators for adherence to follow-up by HR-HPV-positive women with premalignant cervical lesions: a mixed-design study in Mexico

BMC Women's Health volume 24, Article number: 550 (2024) Cite this article

Abstract

Background

Mexico reports low follow-up completion rates among women with abnormal cervical cancer screenings. This study aimed to identify barriers and facilitators to follow-up adherence among women with human papillomavirus (HPV) infection and premalignant cervical lesions in Mexico.

Methods

A mixed-methods study was conducted from February to April 2019. Participants included women undergoing follow-up care for high-risk human papillomavirus (HR-HPV) and premalignant lesions, along with health personnel from the Women’s Healthcare Center (CAPASAM) in Mexico. Quantitative data were obtained from the Women’s Cancer Information System and through a questionnaire about factors affecting follow-up adherence. Additionally, the health personnel involved completed a compliance checklist regarding care regulations. Descriptive statistics were used for analysis. Qualitative data were collected via semi-structured interviews with both groups, followed by a content analysis based on identified categories. The Hazard Analysis and Critical Control Point System confirmed care process risks. Proposals to enhance the Early Detection Program for Prevention and Control of Cervical Cancer were collected from a CAPASAM health personnel nominal group.

Results

Identified barriers to follow-up included low income among CAPASAM users, family provider roles limiting time for appointments, long waits for testing and results delivery, distant facilities, insufficient service hour communication, inadequate health personnel training, and a lack of systematic counseling. Hesitation toward follow-up was also linked to shame, apprehension, uncertainty, test aversion, fear of positive results, and limited cervical cancer and screening knowledge. Patriarchal attitudes of partners and limited access to the now-discontinued PROSPERA government program further discouraged follow-up. Facilitators comprised respectful treatment by CAPASAM staff, no-cost services, health campaigns, and positive user attitudes.

Conclusions

The study found more barriers than facilitators to follow-up adherence, highlighting the need for strategies to bolster the Early Detection Program. Future strategies must address the comprehensive array of factors and incorporate stakeholder perspectives.

Peer Review reports

Background

Cervical cancer is the second most common cancer among Mexican women despite being highly preventable. In 2022, Mexico reported 10,348 new cases and 4,909 deaths, with a 5-year prevalence of 33,441 cases [1]. Most cases occurred in women from low-resource areas [2, 3], making it a significant public health issue with substantial social costs and a problem entrenched in pre-existing inequities [2,3,4].

The Mexican program for early detection, prevention, and control of cervical cancer in Mexico uses traditional cervical cytology and biomolecular tests to detect high-risk human papillomavirus (HR-HPV) using PCR with liquid-based cytology [5]. However, this approach has been largely ineffective due to systemic issues [6,7,8,9], inadequate screening and diagnostic quality, and poor follow-up for women with positive results [7, 9]. Remarkably, up to 50% of Mexican women with positive results for cervical cytology or PCR for HR-HPV do not receive necessary diagnostic confirmation or follow-up [7, 8, 10].

This issue arises within a fragmented health system characterized by limited and inefficiently allocated financial resources [11], a lack of preventive health focus [12], insufficient intercultural awareness, a dearth of trained health personnel [13], poor coordination across different levels of care, and unreliable health information systems [11]. Identifying and inviting eligible women to participate in early detection and ensuring proper follow-up for those with positive results is critical [7,8,9].

It is crucial to identify barriers and facilitators for follow-up adherence among women with positive HR-HPV tests and premalignant cervical lesions. The World Health Organization defines adherence as the extent to which an individual’s behavior aligns with health professional recommendations, highlighting the importance of active collaboration between health personnel and patients [14]. Adherence is influenced by socioeconomic conditions, health services and personnel, users, and disease and treatment dynamics [14].

The current international health policy framework provides an opportunity to address cervical cancer effectively and holistically, assuming prevention and control measures are sustainable and universally implemented. In 2020, the World Health Organization launched a global strategy to eliminate cervical cancer as a public health issue, aiming to meet several 2030 Sustainable Development Goals [15]. The strategy includes vaccinating 90% of girls by age 15, screening 70% of women by age 35 and again by age 45, and treating 90% of women with precancerous or cancerous lesions [15,16,17].

Given this context, our study aims to understand the barriers and facilitators affecting follow-up adherence among women diagnosed with HR-HPV and premalignant cervical lesions. We analyzed the perspectives of women undergoing follow-up and health personnel involved in the Women’s Healthcare Center (CAPASAM) care process of the Cervical Cancer Early Detection Program in Morelos (Mexico).

Methods

Study design and location

Our study was a cross-sectional mixed methods investigation approved by the Subdirectorate of Teaching, Research, and Training of the Morelos State Health Services, as well as by the Research Ethics Committee of the National Institute of Public Health in Mexico. Prior to participation, all participants provided informed consent through a form administered by a researcher. This study employed both qualitative and quantitative methods, with a major emphasis on qualitative aspects. The integration of these components occurred at the results stage. Data collection was conducted at the CAPASAM, which is affiliated with the Morelos State Health Services in Mexico. CAPASAM caters to women with challenging socioeconomic backgrounds, referred from health facilities due to abnormal liquid-based cytology results, from February to April 2019.

Participants and procedures

Our methodological approach targeted two participant groups (Table 1). Women aged 35 to 64, identified as follow-up cases, were invited to participate as they arrived for their consultations at the Early Detection Program for the Prevention and Control of Cervical Cancer. Eligibility for inclusion required registration of their appointments through the Women’s Cancer Information System (SICAM) within the study period and their consent to participate. First-time attendees were excluded. All participants signed the informed consent form. Selection concluded upon achieving theoretical saturation. The second group consisted of health personnel involved in managing women’s consultations at CAPASAM. Due to the small size of this group, it was deemed unnecessary to select samples; therefore, all individuals meeting the inclusion criteria were enrolled in the study.

Table 1 Methodological framework employed in this study
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Data collection

Quantitative data—CAPASAM users

To collect quantitative data for women utilizing CAPASAM services under the Early Detection Program, we extracted sociodemographic information and waiting times from SICAM and then administered a questionnaire designed to assess treatment adherence in patients with cardiovascular risk. We employed a validated instrument tailored for this study (Supplementary Material 1) to examine a range of factors: users' socioeconomic conditions, perceptions, attitudes, and emotions, experiences with CAPASAM health services and personnel, and knowledge about early detection tests [18]. The aspect of user knowledge was further investigated using the Battle Test [19]. Adherence was measured overall and by category using a Likert scale, with classifications from very adherent to non-adherent based on percentage scores.

Qualitative data—CAPASAM users

The qualitative aspect was examined through semi-structured interviews with 18 users. The interview guide aimed to uncover barriers and facilitators to adherence for follow-up among HR-HPV-positive women with premalignant cervical lesions using CAPASAM services under the Early Detection Program. It covered (a) Participant profile; (b) Knowledge about cervical cancer and screening tests; (c) Socioeconomic conditions, attitudes, perceptions, emotions of users, and the influence of their partners, experiences with CAPASAM health services and personnel; and (d) Suggestions for enhancing the Early Detection Program. Interviews were conducted in Spanish by a trained study researcher in person at CAPASAM facilities, and the average was 30 min. They were audio-recorded for textual transcription. The number of interviews was deemed sufficient for female participants to reach theoretical saturation.

Quantitative data—health personnel

To gather quantitative data on the health personnel, we accessed CAPASAM administrative records and then had clinic health personnel complete a 24-item checklist on adherence to care process guidelines. The checklist was created according to Official Mexican Standard 014-SSA2-1994 for cervical cancer prevention, diagnosis, treatment, control, and epidemiological surveillance, revised in 2007 [20].

Qualitative data—health personnel

The qualitative component was explored by conducting semi-structured interviews with seven health personnel. The interview guide aimed to identify the barriers and facilitators to adhere to the follow-up of HR-HPV-positive women with premalignant cervical lesions using the CAPASAM services under the Early Detection Program. The guide included sections on (a) Participant profile, (b) Knowledge about cervical cancer and screening tests, (c) Users’ socioeconomic condition, attitudes, perceptions, and emotions, as well as the role of male partners, experiences with CAPASAM health services and personnel, and (d) Proposals for improving the Early Detection Program. The interviews, conducted in Spanish by one of the study researchers in person at CAPASAM facilities, lasted about 30 min each and were audio-recorded for textual translation.

The results of the checklist identified phases of the follow-up process that could be improved. We adapted two of the seven principles from the Hazard Analysis and Critical Control Point System to this end [21]. Hazards were defined as factors in the healthcare process that could affect women’s adherence to follow-up using CAPASAM services under the Early Detection Program. The first principle of this system involved conducting a hazard analysis to identify and examine low compliance rate factors in the healthcare process, from the checklist. The second principle established critical control points, areas where control measures could be implemented to prevent, reduce, or eliminate specific risk factors [21]; a decision tree helped determine if the identified hazards were such points.

One of the study researchers also formed a nominal group with five healthcare personnel involved in the follow-up process. Members from the CAPASAM morning shift were chosen by convenience to identify actions that could strengthen the Early Detection Program for Cervical Cancer Prevention and Control. The meeting, held at CAPASAM facilities, lasted about one hour. Based on quantitative and qualitative results and proposals from CAPASAM users and personnel, the dialogue evolved through brainstorming, followed by analysis and discussion, resulting in a consensus on actions to enhance the Early Detection Program.

Data analysis

For quantitative data analysis, descriptive statistics summarized the sociodemographic traits of CAPASAM users and characterized the center’s health personnel by age, sex, professional profile, work shift, and collaboration time with CAPASAM. We defined the waiting time as the period from HR-HPV detection test sample collection to the first follow-up appointment, calculating the average days. Percentages evaluated compliance with the official care standard and adherence to follow-up results across five dimensions using the STATA/MP software (version 16.0).

For qualitative analysis, interviews were audio-recorded, transcribed verbatim and analyzed using grounded theory to define codes and to identify analytical categories with the support of Nvivo 11 software. This analysis identified barriers and facilitators to follow-up adherence among women in the study.

We triangulated information from the two study populations, integrating and contrasting results for users’ socioeconomic condition, perceptions, attitudes, emotions, services and personnel experiences, general understanding of cervical cancer, and knowledge about early-detection tests. The English translation of the semi-structured interviews and nominal group discussions was performed by language professionals to ensure fidelity to the participants' testimonies.

Results

Participants included 18 CAPASAM users with an average age of 46 ± 6.47. Most (83%) had a stable partner, 61% had completed secondary school, and only 11% had attended high school. The majority (83%) were employed, predominantly in domestic work outside the home. The study included seven CAPASAM professionals averaging 39.28 ± 9.19 years of age regarding the health personnel. Six held bachelor’s or graduate degrees, and one had a technical degree.

Most findings, from the perspectives of both populations, aligned in the following dimensions of adherence: socioeconomic condition of users; their perceptions, attitudes, and emotions; general understanding of cervical cancer; knowledge about early-detection tests; and experiences with CAPASAM health services and personnel. These findings are summarized in Table 2. It is important to note that both participant groups identified more barriers than facilitators to adherence to follow-up care for HR-HPV-positive women with premalignant cervical lesions.

Table 2 The barriers and facilitators for adherence to follow-up for HR-HPV-positive women with premalignant cervical lesions: the perspectives of CAPASAM users and health personnel
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Socioeconomic issues were the most significant barriers to follow-up among CAPASAM users. Many lacked the financial resources for public transportation to the health facility. Additionally, numerous individuals were family providers and also engaged in unpaid domestic work, limiting their time for testing and follow-up appointments. Those who were employed outside the home faced the loss of daily wages if they missed work. Only a small number reported financial support from relatives to cover follow-up costs.

Regarding CAPASAM’s health services and personnel, our study found that both groups identified lengthy waiting times for tests and result delivery as major barriers (Table 2). Base on the checklist, this is acknowledged as a phase of the care process that is often non-compliant with regulations and eligible for enhancements.

Data from SICAM allowed us to calculate waiting times across the care cascade for women. The average duration from HR-HPV PCR testing to colposcopy was 45.72 ± 13.89 days; from collecting the histological sample to providing histopathological results, it was 20.33 ± 9.02 days. The mean time from the start of therapy to the follow-up appointment was 23.92 ± 11.75 days, though this varied based on the specialist’s evaluation and required treatment type. Barriers also included the long distance from homes to CAPASAM and inadequate promotion of service schedules (Table 2).

By utilizing the checklist, our analysis showed that areas needing improvement included refresher courses for health personnel and coordination at the first level of care. Only 29% of the CAPASAM personnel in this study had recent training in the Early Detection Program, yet 43% reported their facility had feedback on the program’s operational performance. Additionally, 57% noted frequent and close staff communication at the primary care level. However, counseling was systematically provided only to women diagnosed with cervical cancer, excluding those who tested positive for HR-HPV with premalignant lesions.

Conversely, dignified treatment, free services—particularly screenings, which can be expensive—and the execution of health campaigns and fairs to reach remote populations were identified as positive aspects of CAPASAM health personnel (Table 2).

Regarding users, barriers included perceptions and emotions that might impede utilizing the screening test, such as sadness, anxiety, uncertainty, and apathy. Confusion, fear, and overestimation of disease severity were common upon receiving test results, leading many to prematurely assume a cancer diagnosis. Despite these challenges, including socioeconomic conditions and obstacles within the health services, most users maintained a positive attitude and attended their appointments.

Our study found that participating women had limited awareness of tests for the early detection of cervical cancer. All were familiar with cervical cytology, known as the Pap smear, but not with the test for HR-HPV or colposcopy. This lack of awareness made it less likely for them to opt for testing or adhere to follow-up care if a premalignant lesion was detected. Several women expressed doubts about the efficacy of cervical cytology after receiving negative results, and subsequently be informed of a premalignant lesion or cervical cancer.

Most participants had limited knowledge about cervical cancer, coupled with misinformation and doubts. While many understood that the disease was sexually transmitted, some believed it could be contracted through other means. Only half recognized HPV as a causal factor for cervical cancer.

Interestingly, two factors influenced women’s experiences: cultural and gender dynamics and access to a conditional transfer program such as PROSPERA. Partners' patriarchal attitudes negatively impacted women’s adherence to follow-up care, often due to moral judgments about women’s sexuality. Moreover, partners tended to blame women for developing an HPV infection, associating it with promiscuity and infidelity. The users highlighted the importance of educating men about the Early Detection Program, disease transmission and prevention.

Limited access to conditional transfer programs (e.g., PROSPERA) also posed a barrier. The discontinuation of PROSPERA in 2019, due to federal administrative changes, led to women no longer receiving direct cash transfers, thus halting their visits to healthcare facilities for sampling or monitoring.

Based on our nominal group analysis, proposals are clearly needed to strengthen the Early Detection Program for the Prevention and Control of Cervical Cancer. Over 90% of the stakeholders involved had never participated in identifying improvement areas within the care process nor in developing proposals to enhance adherence to follow-up procedures in women’s health care. Among the staff proposals were systematic sensitization and training of operational personnel, alongside an organizational approach that includes teamwork and periodic feedback on processes, within the framework of effective coordination at the first level of care.

Discussion

Our study revealed low adherence rates among HR-HPV-positive women with premalignant cervical lesions, identifying more barriers than facilitators. Figure 1 summarizes the interrelated barriers and facilitators to adherence identified in women who received positive early screening results. These findings on barriers and facilitators are consistent with previous studies [22,23,24,25,26,27,28,29].

Fig. 1
figure 1

Barriers and facilitators for adherence to follow-up by HR-HPV-positive women with premalignant cervical lesions. Source: prepared by the authors

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The main obstacle to follow-up is the lack of economic resources, consistent with findings from previous studies [26, 30]. Research conducted along the Texas-Mexico border showed that many women rely on family and friends for transportation due to a limited bus system. Thus, securing transportation to a clinic site can pose a challenge [31]. Studies in Cameroon identified poverty and transportation costs as significant barriers preventing women from attending follow-up sessions [22]. Another study highlighted that low-income women prioritize their families’ needs over prevention, making it a secondary concern [32]. Transportation, food costs, and loss of income were significant barriers to screening in other studies [23, 33,34,35], even when tests were free [23, 33, 34].

Lack of time to attend appointments emerged as another key barrier, a finding echoed by research in both high- and low-income countries [27, 36]. For instance, 56% of women in a German study reported lacking time to attend colposcopy sessions following abnormal cytology results [27]. Other studies found that family and work responsibilities further limited women’s ability to be tested and receive follow-up care [25, 35, 37]. It was also noted that work leave is usually only granted for ‘real’ illness, leading to income loss when missing work [37].

Long waiting times in the cascade of care significantly hinder access for women [29]. Globally, long wait times for testing and service refusals due to high patient volumes [23, 26] and insufficient staffing [26] are barriers, persisting even for those arriving early at health facilities [33].

Our study found CAPASAM facilities to be inconveniently located from the homes of many women, with transportation costs exacerbating their challenges. Literature suggests that distance from healthcare facilities is a primary barrier to access [24, 35, 38]. In Germany, 48% of respondents cited travel distance and costs as major reasons for missing colposcopy appointments [27]. In Kenya and Cameroon, the substantial distance from care providers was a significant obstacle [22, 38]. Rural dwellers face the compounded barrier of cost and difficulty accessing health care [34].

Additionally, our study pointed to inadequate dissemination of information about health services as a significant barrier to follow-up. The critical need to inform the target population about available tests and hours of operation necessitates inclusion in strategies to reduce follow-up barriers. Previous findings indicate that many women are unaware of where to go or which facility to use for preventive or treatment services [38].

Another area requiring improvement is the provision of refresher courses for health personnel. This issue is particularly important as it significantly impacts the quality of care. A qualitative study conducted with women and health care providers in communities with a high percentage of Indigenous populations in Morelos, Mexico, revealed that providers are poorly informed about current regulations and specific clinical indications for cervical cancer detection [13]. A study on Peruvian women highlighted the need for monitoring and/or quality control training for staff collecting samples [32]. Additionally, a lack of adequately trained personnel in facilities providing oncology services, including at the primary level of care, was reported in another study [30].

Our study identified counseling as another area of opportunity, given that these services were not systematically provided to the analyzed women. This gap had not been thoroughly defined in previous studies. Counseling can encompass advice, guidance, and health education, all sharing the common goals of providing accurate, clear, and easily understood information to guide health decision-making according to the user’s needs [39]. One study underscored that women did not receive adequate advice, leading to a knowledge gap about when to return for follow-up [22]. Another investigation found that while Peruvian women were aware of the tests, they did not receive friendly and comprehensible information about what they were involved in, hindering their implementation [32].

Issues concerning sexuality are integral to belief systems that influence attitudes toward morality, relationships, love, and fidelity. Opinions on these subjects can generate feelings about intimacy involving deeply rooted values. Thus, fear, shame, and uncertainty about performing screening tests and apprehension about a cervical cancer diagnosis were identified as barriers for participants in our study, with similar instances widely documented [26, 27, 29, 35, 40,41,42,43,44]. Along with these emotions, a reluctance to undergo screening was noted, with individuals avoiding these tests to evade the associated feelings and anxiety. One study discovered that reluctance to undergo a gynecological examination prevented several HPV-positive women from returning for follow-up, fearing a cancer diagnosis [23]. Other studies indicated that the embarrassment of exposing one’s private areas during tests was a significant barrier [33, 35, 37], especially if the examiner was male [35, 37]. For instance, researchers have reported anxiety and fear of results deterring Nepalese and Cameroonian women from undergoing tests [34, 36], affecting their adherence to follow-up routines [45]. However, fear did not always serve as a barrier: in some cases, the fear of having cervical cancer and understanding the importance of care motivated women to seek follow-up [25, 46].

Due to unfamiliarity with the tests and their processes, the limited knowledge of PCR tests for HR-HPV and colposcopy among study participants was a crucial factor in their decision-making. This is a common situation for women globally. Evidence suggests that a limited understanding of these tests negatively impacts their acceptance [47], undermining adherence to follow-up. A study on Mexican women found that those most likely to receive a Pap smear were the most knowledgeable about the test and cervical cancer risk factors [28]. Another study revealed that women were generally unaware of cervical cancer screening but familiar with the Pap test, implying that some underwent the test without understanding its purpose [32]. Additional research identified limited knowledge of the screening process and purpose, along with little recognition of its importance [37]. A study in a predominantly low-income African-American community in the United States found that the main barrier to follow-up for women with abnormal cytology was a limited understanding of the meaning of an abnormal test result and what a colposcopy entails [7, 45].

Consistent with previous studies, our findings indicate that a limited understanding of cervical cancer, its association with HPV, and the route of transmission, alongside misinformation and doubts, are significant barriers to follow-up. These barriers influence the decision to undergo testing [33,34,35,36,37, 40, 41, 43], leading many women to believe they should seek medical check-ups only when showing specific symptoms [36]. A study in Yucatan (Mexico) found that over 50% of participants were aware of HPV, while 38.9% knew about the Pap test and 25% were informed about cervical cancer [48]. In a mixed study in Peru among sex workers with abnormal Pap tests, non-adherence was linked to lesser knowledge about the connection between HPV infection and premalignant lesions in the cervix [46].

Similar to other studies [22, 24, 29, 33, 35, 36, 38, 43], a key finding of our research is that male partners often obstruct follow-up, either by objecting to their partners attending screenings, requiring their permission, or by not providing financial support for the services. This is often tied to patriarchal views on control over their partners' bodies and sexuality. In severe cases, this control has led to violence against women by their partners, triggered by jealousy related to gynecological examinations for screening [49]. A critical discovery was that male partners frequently accused women of infidelity upon learning of their sexually transmitted HPV infection, associating it with promiscuity [35, 38]. Additionally, our study underscores the need for education and counseling for couples about HPV transmission and prevention, as well as the cervical cancer screening program, echoing a study that emphasized increasing couple involvement in cervical cancer’s secondary prevention [24].

Evaluations of conditional-transfer programs, like the defunct PROSPERA Program, show improved access to health services and enhanced human capabilities. However, their impact on health status is varied and often diminishes once the programs end, as seen when PROSPERA concluded and participants significantly reduced their use of health services [50,51,52]. Our study confirms that free testing and treatment are major facilitators and strengths of the Cervical-Cancer Detection Program in Mexico. The cost of testing and treatment remains a deterrent for women globally from accessing health services, as extensively documented in prior research [36, 41, 53]. In fact, one study in El Paso (Texas) found that many Hispanic women opted for Pap tests in Ciudad Juarez due to lower cost or free services, highlighting cost as a critical factor [54].

Respectful treatment by CAPASAM personnel was another facilitator for women accessing services, aligning with reports of women valuing the personnel’s kindness, patience, and professionalism [22]. Conversely, poor health communication and disrespectful treatment by health professionals were identified as significant barriers to the Early Detection Program and counseling activities [34, 39]. Our research identified health campaigns and fairs in remote areas without health facilities as facilitators for screening, consistent with findings that mobile services in communities increase testing uptake despite follow-ups occurring in established health facilities elsewhere [26, 33, 36]. In Mexico, diagnostic confirmation and treatment occur in colposcopy clinics, and follow-up continues to be challenged due to other factors. A positive attitude from users emerged as a primary facilitator for follow-up adherence in our study, potentially influencing decision-making positively, even amidst prevailing barriers. A prior study reported that a majority of women viewed cervical cytology as very important (70%) and had discussed their test results and experiences with others (58%) [42].

This study had both strengths and limitations. Notably, its strengths included a mixed-methodology approach, enabling a comprehensive exploration of factors influencing whether women in this group seek follow-up care. This analysis encompassed elements common across various national and international contexts, while some facets of multidimensional adherence were unique to the CAPASAM study population. The use of diverse qualitative instruments facilitated the identification of a broad spectrum of perspectives. Another significant strength was the involvement of two key stakeholders—patients and staff—in operationalizing the Early Detection Program for the Prevention and Control of Cervical Cancer, yielding several convergent findings. Our results underscore the need to dismantle the barriers identified and reinforce facilitating factors, turning them into strengths of the Early Detection Program.

Regarding limitations, the study focused on women who attended health services for follow-up, omitting those who did not seek care due to being HR-HPV-positive with premalignant cervical lesions. Therefore, further investigation into this subgroup’s issues is warranted, necessitating a deeper examination of the barriers and facilitators uncovered in our analysis.

Conclusions

This mixed-methods study provides insights into the factors influencing adherence to follow-up among women in Mexico participating in an early detection program for cervical cancer who tested positive for HR-HPV infection and had premalignant cervical lesions. Our approach, emphasizing adherence, enabled the integration of various elements at different levels and involving multiple stakeholders. Socioeconomic conditions, CAPASAM health services and personnel, emotional responses and perceptions of CAPASAM users, lack of awareness about cervical cancer and early detection tests, as well as patriarchal attitudes from partners and restricted access to conditional-transfer programs, emerged as barriers to follow-up adherence. Conversely, facilitators included respectful treatment by health personnel, complimentary services, health campaigns, and a positive user attitude. These findings could be considered for the development of interventions to enhance the effectiveness of Early Detection Programs for preventing and controlling cervical cancer.

Availability of data and materials

Data generated and analyzed during the present research are not publicly available because of the need to protect personal information, but are available from the corresponding author upon reasonable written request.

Abbreviations

CAPASAM:

Centro de Atención para la Salud de la Mujer [Women’s Healthcare Center]

PCR for HR-HPV:

Biomolecular test for high-risk human papillomavirus

PROSPERA:

Social inclusion/conditional transfer program

SICAM:

Sistema de información de cáncer de la mujer [Women’s Cancer Information System]

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Acknowledgements

The authors kindly thank the valuable collaboration of Morelos State Health Services, particularly the users and staff of the Women’s Healthcare Center (CAPASAM) who participated in this study.

Funding

This study was supported by the National Council of Humanities, Sciences, and Technologies (CONAHCYT) of Mexico (FONSEC SSA/IMSS/ISSSTE-2018 grant no. A3-S-49099).

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Authors and Affiliations

  1. Hospital General de Zona 3, Instituto Mexicano del Seguro Social, San Juan del Río, Querétaro, Mexico

    Gengly Aguilar-Linares

  2. Centro de Investigación en Sistemas de Salud, Instituto Nacional de Salud Pública, Cuernavaca, Morelos, Mexico

    Margarita Márquez-Serrano, Sergio Meneses-Navarro & Blanca Estela Pelcastre-Villafuerte

  3. Consejo Nacional de Humanidades Ciencias y Tecnologías (CONAHCYT), Instituto Nacional de Salud Pública, Cuernavaca, Morelos, Mexico

    Sergio Meneses-Navarro & Kirvis Torres-Poveda

  4. Instituto de La Mujer de Cuernavaca, Morelos, Mexico

    Lorena E. Castillo-Castillo

  5. Centro de Investigación en Salud Poblacional, Instituto Nacional de Salud Pública, Cuernavaca, Morelos, Mexico

    Jesús A. Estévez-García

  6. Universidad Nacional Autónoma de México, Servicios de Salud Pública de La Ciudad de México, Mexico City, Mexico

    Tania O. Valadez-George

  7. Dirección de Infecciones Crónicas y Cáncer, Instituto Nacional de Salud Pública, Cuernavaca, Morelos, Mexico

    Margarita Bahena-Román, Vicente Madrid-Marina & Kirvis Torres-Poveda

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  1. Gengly Aguilar-Linares
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Contributions

KTP, GAL, MMS: Conceptualization; GAL: data curation; KTP: resources and project administration; GAL, KTP, MMS, SMN, BPV, LECC, JAEG, TOVG, MBR: writing—original draft; and VMM: writing—revision and editing. All authors revised the manuscript. All authors contributed to the article and approved the submitted version.

Corresponding author

Correspondence to Kirvis Torres-Poveda.

Ethics declarations

Ethics approval and consent to participate

This research received approval from the Research Ethics Committee of the National Institute of Public Health in Mexico (Protocol Resolution CI: 505) and the Subdirectorate of Teaching, Research and Training of Health Services of the State of Morelos, through an official letter of authorization (DAM/SFIC/DIC/1905/2019). All participants provided written informed consent before joining the study. The research was conducted according to the guidelines laid out in the Regulations of the General Health Law on Health Research, the General Health Law of the State of Morelos, and international research agreements, aligning with the Declaration of Helsinki.

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Not applicable.

Competing interests

The authors declare no competing interests.

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Aguilar-Linares, G., Márquez-Serrano, M., Meneses-Navarro, S. et al. Barriers and facilitators for adherence to follow-up by HR-HPV-positive women with premalignant cervical lesions: a mixed-design study in Mexico. BMC Women's Health 24, 550 (2024). https://doi.org/10.1186/s12905-024-03379-3

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BMC Women's Health

ISSN: 1472-6874

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