Implementation of Breast Cancer Screening and Its Effect Among Chinese Rural Women: A Mixed-Methods Evaluation Based on RE-AIM Framework

doi:10.21203/rs.3.rs-5284188/v1

Background:

Many rural areas lack screening for breast cancer. This study employs the RE-AIM framework to assess the implementation, effectiveness, and sustainability of a breast cancer screening program in China to provide insights into developing an effective implementation strategy suitable for rural areas with limited health resources.

Methods:

This mixed-methods study evaluated a breast cancer screening program in Ordos, Inner Mongolia, using quantitative and qualitative approaches. Quantitative data from 2016 to 2020 were gathered through surveys and screening results involving 116,013 women aged 35–64. Qualitative data were obtained via semi-structured interviews with MCHH health workers in 2024 to identify program facilitators and barriers. Quantitative and thematic qualitative analyses were conducted, with findings compared using a convergent mixed methods approach.

Results:

The screening program reached 35.05% of the target population by 2018, rising to 52.24% among women aged 35–64 in 2020. Cancer detection rates were 0.56/1000, ranging from 0.08/1000 in women aged 35–39 to 1.89/1000 in those aged 60–64. The PPV for biopsy was over 67%, but few patients with abnormalities completed the procedure. Key facilitators included strong patient-provider communication, staff involvement, adequate funding and training, and strict supervision, while barriers involved geographical distance, lack of multi-sector support, limited service capacity, and low health awareness. The “rural outreach” model and routine hospital screening were seen as the most effective solutions for the dispersed population and low self-efficacy. Increased awareness from prior screenings improved participation and compliance in subsequent programs. A key challenge in program maintenance was reduced quality control, supervision, and training efforts.

Conclusion:

It is recommended to delay the initiation of breast cancer screening to age 40 or 45 in rural areas with low incidence rates. Improving the screening capacity at primary healthcare facilities and strengthening the patient navigation system for timely referrals to higher-level centers are essential to enhance cancer detection in these regions. The “rural outreach” model is effective in reducing health disparities among marginalized women while simultaneously raising their awareness. Further research is needed to evaluate long-term outcomes and to develop customized implementation strategies for addressing the identified barriers.

breast cancer screening

implementation

mix-methods

RE-AIM framework

Breast cancer is one of the most commonly diagnosed cancers worldwide, with 2.3 million new cases and 685 thousand deaths occurring in 2022. More than 70 percent of the women who die from breast cancer live in low- and middle-income countries (LMICs)[1], which largely attributed to more advanced stages of diagnoses, limited access to early diagnosis and optimal treatment in these countries[2, 3]. In 2020, China had the highest number of new breast cancer cases worldwide, constituting 40.7 percent of the global total. Additionally, 117 thousand women died from breast cancer[4], marking a rapid increase in both incidence and mortality rates, a trend particularly noted in rural areas[5]. This indicates the necessity of implementing a breast cancer control program that aligns with the local socioeconomic status and healthcare system to tackle the dilemma.

China initiated a national program offering free cervical cancer and breast cancer screening for women aged between 35 and 64 years old living in selected rural areas. From 2009 to 2011, the program used clinical breast examination (CBE) as the primary screening method. In 2012, breast hand-held ultrasound (HHUS) replaced CBE as the primary screening method, and mammography (MG) was used for diagnostic examinations in cases classified as BI-RADS 0 or 3 by HHUS[6]. Due to unbalanced and limited resources in China, this program covered a small proportion of women. Approximately 30 million breast examinations were conducted between 2009 and 2018 across 2,644 selected counties[7]. A nationwide survey reported that 18.8% of women in rural China had been screened over the last three years, a rate lower than most Western countries[8]. Residents of rural areas were less likely to undergo breast cancer screening[9]. Therefore, it is important to implement more effective screening strategies to improve breast cancer screening in these areas.

To develop a more effective and sustainable strategy, it is essential to further investigate factors influencing the implementation of breast cancer screening programs in areas with limited medical resources, with the goal of improving both coverage and quality of screening. In 2016, the Ordos government launched a program that provided breast cancer screening every three years to all female residents aged 35 to 64. To assess the implementation and long-term impact of this program, the Reach, Effectiveness, Adoption, Implementation, and Maintenance (RE-AIM) framework, a widely accepted approach for evaluating the implementation of public health intervention, will be applied This study aims to evaluate the implementation of this program, assess its effects and sustainability using the RE-AIM framework, and provide insights into conducting breast cancer screening in areas with limited medical resources.

To improve the coverage and quality of breast cancer screening in areas with limited medical resources, it is crucial to examine factors affecting program implementation. In 2016, the Ordos government launched a screening program for women aged 35 to 64, providing services every three years. This study applies the RE-AIM framework to evaluate the screening program through five dimensions, including Reach, Effectiveness, Adoption, Implementation, and Maintenance, offering insights for similar efforts in resource-limited settings[10].

Settings and participants

This study was conducted in a medical resource-constrained minority region with low population density who were poorly educated. The area of the Ordos is 87,000 km² with a sparse population of 2,045,100 (including migrants) in 2015[11]. At the beginning of the program, there were 27 public hospitals, 39 community health centers, 53 community health units, 93 township health units, 682 village health units, and nine centers for disease control and prevention in Ordos City. Public hospitals had 6330 beds. Every thousand people had approximately 3.1 beds[11], which was similar to China’s average level (3.8 beds per 1000 people) in the year of 2015[12].

Reliable data on breast cancer epidemiology in Ordos is unavailable. In Inner Mongolia, the incidence and mortality of breast cancer were 53.19/10⁵ and 8.80/10⁵, respectively, ranking as the second most commonly diagnosed malignancies and the fifth leading cause of cancer death in 2015. The trend of incidence showed a slight increase from 2010 to 2015[13].

There are approximately 339,000 female residents aged 35–64 years old in Ordos. They were all considered as the targeted population for breast cancer screening if they met the inclusion criteria: a) aged between 35 and 64 years old; b) were residents in Ordos or had lived in Ordos for more than six months; c) were able to understand the screening procedure and voluntarily participated in the program. The exclusion criteria include: a) had been diagnosed with breast cancer before; b) were pregnant.

The screening program was organized by the Ordos Health Committee and implemented by all MCHHs. Working together with township and village health units, MCHHs served as the primary point of contact, responsible for educating and mobilizing residents to participate in the program. We invited health workers from each MCHH for interviews, with participants ranging from hospital directors to department members (Table 1). The inclusion criteria included participation in on-site breast cancer screening or organization and management of the local breast cancer screening program from 2016 to 2020.

Table 1

Characteristics of Interviewees
Code of Interviewee	Gender	Job Title in the Hospital	Duty of Participation
1	Female	Department Head	On-site Screening
2	Female	Department Head	On-site Screening
3	Male	Director	Management
4	Male	Deputy Director	On-site Screening& Management
5	Female	Department Head	On-site Screening
6	Female	Department Head	On-site Screening
7	Male	Director	Management
8	Female	Department Head	On-site Screening
9	Female	Department Member	On-site Screening

Screening methods

Breast ultrasound was used as the primary screening modality in this program. The first round of screening took place from 2016 to 2018. Images were interpreted according to the Breast Imaging Reporting and Data System (BI-RADS). All eligible women underwent HHUS and CBE examinations first, and those who were categorized as BI-RADS 0, 4, or 5 were referred to undertake MG. An assessment of BI-RADS categories 4–5 by MG was considered for biopsy. An assessment of BI-RADS categories 1–3 by HHUS or MG was considered negative and women were advised to return for re-examination after three years. Those with benign lesions or normal biopsy results were followed up actively. They were called back annually for a free re-examination by project personnel.

Data collection

Screening data

Personal information and breast cancer risk factors (age, race, marital status, education level, method of payment, knowledge of breast cancer screening) were collected through a face-to-face questionnaire before the examination began. All demographic and examination results were recorded based on the pre-designed case report form (CRF) and were stored in an integrated electronic data system that enables information sharing among MCHHs in Ordos.

Semi-structured interviews with health workers of MCHHs

A semi-structured interview guide was developed based on the RE-AIM framework[10], previous research[14], and expert recommendations. Nine health workers from seven MCHHs were invited to the semi-structured interview (three through video call, six through face-to-face interview), covering seven of the nine local counties. Each interview lasted 45–90 minutes and was recorded with the interviewees’ consent. WQ and YH transcribed all recordings verbatim to ensure that the research findings accurately reflected the interview’s statements.

Data analysis

For quantitative data, the unit of analysis was the individual participant. The continuous variables were presented as mean and standard deviation, while the categorical variables were presented as proportion and percentage. The screening effect was evaluated by screening coverage, HHUS screening positive rate, breast cancer detection rate (CDR) and the positive predictive value (PPV) for biopsy performed. BI-RADS 0 and 4 + on HHUS was considered as screening positive. The rate of MG completion and biopsy completion were used to assess screening adherence, calculated as the number of MG or biopsy finished divided by the number of HHUS positive. The Chi-square test was used to compare each subgroup’s positive rate and cancer detection rate. P < 0.05 was considered statistically significant for two-sided tests. All statistical analysis was conducted using SAS software, version 9.4 (SAS Institute Inc.).

For qualitative data, a thematic analysis approach was applied. After becoming familiar with the transcripts, YH and WQ developed a coding structure based on five dimensions of the RE-AIM framework, and coded the transcripts independently, discussing the coding structure and reaching a consensus on any discrepant issues. Facilitators and barriers of each dimension were identified from each transcript. All the quotes involved in the article were translated from Chinese to English. Nvivo was used as the qualitative data management system.

Convergent mixed methods were applied to the analysis because quantitative and qualitative data were collected independently and in parallel, integrating findings under each RE-AIM framework domain. We used a narrative approach that describes the quantitative and qualitative results thematically. By using the methods of joint display and meta-inference, this study demonstrated the possible confirmation, expansion and discordance between quantitative and qualitative data, which further verified our findings[15].

Utilizing the RE-AIM framework, we summarized the context, implementation outcomes, and impact pathways of the screening program. Characteristics of interviewees involved in the in-depth interviews are summarized in Table 1. The facilitators and barriers that influence each domain of the implementation outcomes are summarized in Table 6 and described briefly below.

Reach

A total of 118,812 eligible women participated in this program by 2018, covering 35.05% of all women aged 35-64 years. By 2020, participation increased to 177,107 women, representing 52.24% of this age group (Figure 1). Nearly 46% of them aged younger than 45 years old, 42% had either never received any education or only had primary education. Farmers and herdsmen accounted for 52.37% of all the participants. 26.32% of the participants had never heard of breast cancer screening before the program, and 26.03% of the participants reported that they had never undergone a breast cancer examination (Table 2).

Table 2. demographic characteristics of participants
	2016-2018		2016-2020
	n	%	n	%
age	46.60±7.50		46.61±7.76
35-44	54519	45.89	81680	46.12
45-54	45538	38.33	65312	36.88
55-64	18755	15.79	30115	17
race
Han	108296	91.15	163602	92.37
Mongolian	10112	8.51	12792	7.22
Other minorities	270	0.23	411	0.23
Unknown	134	0.11	302	0.17
Marital status
Unmarried	1675	1.41	1703	0.96
Married	115044	96.83	172422	97.35
Others	1926	1.62	2640	1.49
Unknown	167	0.14	342	0.19
Education status
Below primary school	50165	42.22	72995	41.22
High school	53937	45.40	82639	46.66
College and above	14547	12.24	21136	11.93
Unknown	163	0.14	337	0.19
Occupation		0.00		0.00
Farmers and herdsmen	62030	52.21	92752	52.37
Employees	42675	35.92	62080	35.05
Others	13952	11.74	21945	12.39
Unknown	155	0.13	330	0.19
Method of medical payment		0.00		0.00
Medical insurance	114421	96.30	168601	95.20
Self-pay	3649	3.07	7391	4.17
Unknown	742	0.62	1115	0.63
Had heard of breast cancer screening
Yes	68825	57.93	98917	55.85
No	31273	26.32	55894	31.56
Unknown	18714	15.75	22296	12.59
Had received breast cancer screening
Yes, within three years	37806	31.82	46053	26.00
Yes, three years ago	18138	15.27	30107	17.00
No, never	30921	26.03	43735	24.69
Unknown	31947	26.89	57212	32.30

All respondents identified geographical distance as a significant barrier that objectively hindered eligible women from participating in screenings. In some counties, the nearest town with an MCHH was often 30 to 60 kilometers away, posing a challenge for women who needed to travel for screening. Five out of nine interviewees mentioned that limited health education and awareness among local women impeded efforts to reach the target population. Women with limited health awareness, especially older women, were hesitant to participate due to misconceptions about the time involved and the impact of the screening process.

“Less educated and older women were more reluctant to participate in screenings, and they are the hard-to-reach population. In recent years, my observation is that people diagnosed with breast cancer are mostly those who have never undergone our screenings.” –Interviewee 2, Department Head

In response to these difficulties, local MCHHs explored a model of “rural outreach plus routine screening in hospital”. To reach marginalized populations, MCHH staff regularly travel to each town with ultrasound to mobilize and screen women who face difficulties visiting the MCHH. At the same time, they accept all women who voluntarily seek screenings at the MCHH. Leveraging the influence of professional specialists also proved effective in attracting more women to participate.

“We (MCHHs) committed to covering all remote areas within five years, ensuring that each township was visited at least once during this time.” –Interviewee 4, Deputy Director

Moreover, eight out of nine interviewees emphasized that high-quality provider-patient communication was crucial in breast cancer screening adherence. They identified explanations of breast cancer risks and benefits, and responsiveness to patients’ concerns about screening, as key items of communication. Additionally, communications provided by doctors, as opposed to nurses, produced better screening adherence.

Adoption

Before implementation, we surveyed the breast cancer screening capacity of each MCHS, including equipment and personnel allocation. Although all MCHHs had at least one HHUS facility, only one county possessed an MG facility. Four MCHHs were capable of performing breast surgeries, however, only clinical breast examination (breast palpation) was provided in these facilities. Therefore, patients screened with abnormalities in the primary-care level facility were referred to the higher-level facility to receive diagnostic evaluation. A total of 33 medical staff specialized in breast imaging: 12 majored in radiology, 17 majored in clinical medicine, two majored in nursing, one majored in pharmacy, and one had no medical school background (Table 3).

Table 3. number of facilities and personnel related to breast cancer screening
	Facilities (N)		Personnel (N)
	HHUS	MG	Breast surgery			Imaging department
			Education level		Average working years	Education level		Average working years
			Bachelor and above	Under Bachelor	Average working years	Bachelor and above	Under Bachelor	Average working years
Dongsheng	2	0	0	0	0	2	0	17.00
Dalad	3	0	1	0	28	3	1	22.50
Junger	1	0	0	0	0	2	3	18.00
Etuoke Front	1	0	0	1	5	2	2	3.75
Etuoke	1	0	0	0	0	1	1	8.00
Haggin	1	0	0	0	0	2	2	24.00
Wushen	1	0	0	0	0	2	1	5.67
Ejin	1	1	1	0	6	4	0	6.00
Kangbashi	2	0	2	0	18	5	0	16.80
Total	13	1	4	1	57	23	10	14.12
Abbreviations: HHUS: hand-held ultrasound; MG: mammography

In accordance with the abovementioned data, poor diagnostic capacity including limited human resources and equipment, especially the lack of mammography and biopsy capabilities were also identified as the major barriers to adoption by all respondents. Another significant barrier mentioned was the lack of cooperation and coordination among different organizations and MCHH departments.

“It seems that only MCHH shouldered the responsibility of screening, with few involvements from other organizations. Within our hospital, there were also issues with unclear divisions of responsibilities, sometimes leading to conflicts over the assignment of duties (targeted population mobilization, clinical examinations, follow-up management, etc.) Currently, these duties are all shouldered by our department.”—Interviewee 6, Department Head

Despite these barriers, several facilitators contributed to the successful adoption of the program. A key facilitator was the economic incentives for staff participating in rural outreach screening (ranging from 7-14$ per day). All respondents mentioned that they considered the screening program as a valuable public welfare, and the majority of MCHH staff were willing to work on it. Regarding leadership (mentioned by four interviewees), the formation of a dedicated screening group composing radiologists, doctors and nurses from relevant departments significantly facilitated the program’s adoption.

Effectiveness

At the end of the first screening round, 118,812 women underwent breast cancer screening, among whom 105,506 received CBE and 116,013 received HHUS. The HHUS positive rate was 1.02% (1,182/116,013). A total of 67 women were diagnosed with breast cancer in the first round of screening—65 by HHUS and two by CBE—yielding a cancer detection rate (CDR) of 0.56/1000. The CDR was lower in women aged 35-39 years, while it increased to a high level in women aged over 40 years. The CDR was higher in postmenopausal compared with premenopausal women (0.92 vs 0.41 per 1000 screens, P<0.001) (Table 4)

Table 4. Rate of HHUS positive and breast cancer detection by characteristics of participants
	No. HHUS	No. Positive (%)	P*	Breast cancer detection rate 1/1000(95%CI)	P*
Total	116,013	1,182(1.02)		0.56(0.42.-0.70)
Age
35-39	25957	216(0.83)	0.0198	0.08(0-0.18)	<0.001
40-44	27236	316(1.16)		0.40(0.17-0.64)
45-49	25756	290(1.13)		0.62(0.32-0.93)
50-54	18767	202(1.08)		0.85(0.43-1.27)
55-59	11859	98(0.83)		0.67(0.21-1.14)
60-64	6438	60(0.93)		1.86(0.81-2.92)
Race
Han	105,630	1,088(1.03)	0.1387	0.55(0.41-0.69)	0.5524
Mongolian	10,057	88(0.88)		0.70(0.18-1.21)
Educational level
Primary school	49,141	447(0.91)	0.0034	0.65(0.43-0.88)	0.5358
High school	52,413	564(1.08)		0.50(0.31-0.69)
College	14,372	170(1.18)		0.49(0.13-0.85)
Menopause
Yes	29,297	256(0.87)	0.0046	0.92(0.57-1.27)	0.001
No	85,989	917(1.07)		0.41(0.27-0.54)
Breast disease history
Yes	22,593	400(1.77)	<0.001	0.53(0.23-0.836)	0.9717
No	93,069	767(0.82)		0.54(0.39-0.69)
Chi-squareTest

All participants expressed a positive attitude towards the program’s impact on women’s health and believed that they reached a rational breast cancer detection rate.

“With the screening program rolling out, people were increasingly with more health awareness…They started to be familiar with the screening procedure and some of them actively persuaded their friends and relatives into screening."—Interviewee 6, Department Head

Implementation

A standardized protocol was disseminated to each MCHH at the beginning of the program with strict instructions for adherence. However, the screening adherence was poor. A total of 1,341 (1.16% of those who underwent HHUS) were categorized as BI-RADS 0,4,5 and were referred to MG examination. Of those referred, few completed definitive diagnosis work-ups: 470 (35.05%) completed MG examination, 96 (7.16%) completed the biopsy examination, and 65 were diagnosed as having breast cancer. The likelihood of being diagnosed with breast cancer for those having a biopsy was higher than 67%. (Table 5).

Table 5. Results of the breast cancer screening in Ordos, 2016-2018
	N (%)	cancers diagnosed (PPV)
HHUS	116013
BI-RADS 0,4,5	1341(1.16)
completed MG according to protocol	470(35.05)
BI-RADS 4+	123
actual completed MG	813
BI-RADS 4+	159
completed biopsy according to protocol	35	24 (68.57)
actual completed biopsy	110	75 (68.18)
completed biopsy for HHUS positive	96 (7.16%)	65 (67.01)

Other than protocol compliance, the qualitative data revealed other several barriers, including data collection and fund management. Data collection was initially paper-based, requiring time-consuming transfers to an electronic system. Despite interviewees claiming they followed the implementation protocol with strong fidelity, quantitative results showed poor compliance. Interviewees identified two main reasons for these discrepancies: poor patient compliance and lack of inter-institutional communication.

“There are limited inter-hospital data sharing mechanisms…What we can do is to contact the patient through phone call or message to claim the results of further examinations outside our hospital…However, in many cases, patients who received positive results after reexamination were reluctant to report to us. It required continuous follow-up calls, which involved a significant amount of work. ” –Interviewee 1, Department Head

Facilitators to ensure the quality of implementation reported by interviewees included: a well-designed executive manual, regular quality control, sufficient funding, and the green referral channel along with effective follow-up and management system for women with abnormalities.

Maintenance

The first round of screening concluded in 2020. Subsequently, the advisory committee ceased overseeing the local screening operations, and the management of ongoing regular screenings was taken over by the provincial government. A significant barrier to maintenance was the reduced quality control, supervision, and training efforts, which were less rigorous than in the first round (as mentioned by four interviewees).

“The quality control and supervision are not as stringent as the first round of screening.” –Interviewee 5, Department Head

“We feel that technical training is becoming less and less available.” –Interviewee 2, Department Head

Previous experiences and established screening capacity not only played a positive role in maintaining the screening program but also facilitated the independent execution of the following screening.

“Although the screening procedure was slightly changed, we generally followed our previous model of screening, including the experience of motivation, organization and follow-up.” –Interviewee 6, Department Head

In addition, sufficient financial support from provincial, prefectural and county-level governments ensured the program’s financial stability. Abandonment of the paper-based data collection significantly reduced the workload. Furthermore, increased health awareness among the target population through the previous screening program improved participation and compliance.

“People are more motivated these days in terms of motivation and recall…This round of screening saw a significant increase in their health awareness.”—Interviewee 2, Department Head

Early diagnostic capacity and management of ultrasound-detected abnormalities are key factors influencing the quality of screening services. We identified barriers and facilitators to implementing breast cancer screening programs based on the RE-AIM framework. Effective provider-patient communication, robust staff involvement, sufficient funding and training, and stringent supervision were identified as key facilitators. Conversely, sparse population distribution, low self-efficacy, inadequate multi-sector involvement, and limited service capacity were recognized as the main barriers.

The CDR of this program is as low as 0.56 per 1000 screens, which is lower than in other rural areas (0.70, 95%CI: 0.57–0.83)[16]. When stratified by age groups, the CDR increased in those aged over 40 years, particularly among those aged over 45 years. Therefore, to provide breast cancer screening, we recommend focusing on those aged over 40 or 45 years or high-risk populations in areas with low breast cancer incidence. Another main reason underlying this is the low biopsy rate due to the insufficient diagnostic capacity of Ordos City. A centralized diagnostic center is established in each county, which is conducive to keeping quality and resource allocation; however, it is less convenient for patients who need to travel to access them, and this can be a source of diagnostic delay or uncompleted diagnosis. Given the current situation, in order to achieve prompt diagnoses, it is essential to enhance the provider-patient communication and patient navigation system from the primary screening facility where the patient first presents to the higher-level facility where diagnostic evaluation takes place.

Provider communication contributed to cancer screening intention and adherence[17]. Almost all interviewees stated the importance of provider-patient communication for breast cancer screening adherence. Furthermore, shared decision-making that includes risk communication and values clarification was associated with improvements in knowledge regarding breast cancer and reduced decisional conflict[18]. Some studies reported that effective provider communication increased screening intentions by enhancing perceived effectiveness and perceived ease of use, particularly when providers explain the reasons behind and methods of screening[19]. Apart from the content, communication quality is also crucial for screening adherence and more studies are needed to evaluate the effect of provider-patient communication with a focus on screening rate and women’s satisfaction[18, 19].

The capacity of primary screening units is recognized as another main aspect contributed to the quality of breast cancer screening. We found that enhanced training and supervision, investment in infrastructure are the requisite for improving the screening capacity. Training on knowledge and skills is expected to improve providers’ objective knowledge and confidence in breast cancer screening[20]. Evidence of meta-analysis indicates that training health workforce from LMICs in CBE benefited the early detection of breast cancer[21]. Healthcare access and quality, particularly access to MG, are the most frequently mentioned social determinants of health interventions to increase breast cancer screening[22, 23]. For MG unavailable areas, alternative methods such as CBE and ultrasound can be used for screening breast cancer. Investment in screening infrastructure plays a key role in breast cancer screening, as it ensures accessibility to primary care services, which is vital for screening utilization[24].

A strong partnership between multiple stakeholders including government, hospitals, practitioners, and experts is important for maintaining effective implementation[25, 26]. Studies found that interventions involving community health workers have been shown to elevate screening rates across diverse demographic groups, regardless of different races, incomes, and insurance statuses[27]. The Rwandan Ministry of Health built a strong partnership with NGOs, experts from the USA, and a local hospital to improve the capacity of conducting cancer care in this hospital in 2012[24]. Peru initiated a community-based program for breast health, which set an example of stakeholder and collaborator involvement to increase breast healthcare capacity[28]. Likewise, the Ordos government led the coordination and allocation of resources to ensure that this program was systematically organized and fully supported. However, a lack of cooperation and coordination among different institutions and within departments of MCHHs was mentioned as one of the top barriers to adopting the breast cancer screening program. Therefore, a policy initiative is not enough to motivate multiple-sector involvement; task assessment and incentive systems should be established simultaneously.

Ordos had a sparsely distributed population with low self-efficacy, which was reported as a barrier to breast cancer screening implementation. Level of education has an impact on cancer screening adherence[29], and education through group classes, videos, or educational booklets is an effective way to improve people’s awareness and breast cancer screening rates[30, 31]. However, health education is time-consuming and influenced by the scale and the literacy level of the people who are being educated. It is hard to persuade people to take action through one-day education, as stated by one of our interviewees. The “rural outreach” model, which delivers breast cancer examination to township-level health stations, aims to make cancer screening more accessible and closer to those who are far from or reluctant to come to hospitals for screening. This strategy was stated by most interviewees as the most effective way to address both the sparsely distributed population and low self-efficacy. Moreover, awareness is increased with the dissemination of breast cancer screening.

This study has several strengths. We used the RE-AIM framework to comprehensively evaluate the implementation of the previous screening program, integrating the screening results from 2016 to 2020 with subsequent screening from 2020 to 2024 into one framework. Particularly in the “maintenance” domain, because qualitative data were collected in 2024, we can thoroughly assess the continuous implementation of local screening after the cessation of program support. In addition, we combined the findings from quantitative and qualitative data to demonstrate how the program was implemented and to identify the facilitators and barriers that may influence the program’s implementation and effectiveness.

There are also some limitations. First, the number of participants we interviewed is small and all only came from MCHHs, limiting our results on the perspectives of health workers. Further studies could include multiple sectors involved in breast cancer screening. Second, the measurement of the program maintenance is limited to qualitative data obtained from interviews. Longer-term surveillance of the screening outcomes is warranted to evaluate the maintenance.

Postpone screening starting age to 40 or 45 years is recommended to rural areas with low breast cancer incidence. The capacity of screening in primary healthcare facility and the patient navigation system from it to the higher-level facility for prompt diagnosis need to be enhanced to increase cancer detection in rural areas. “Rural outreach” is an effective way to reduce health inequity in marginalized women and increase their awareness at the same time. Further research is needed to assess long-term outcomes and develop customized implementation strategies for overcoming the identified barriers.

Acknowledgements

The authors would like to thank Maternal and Child Healthcare Hospital of Ordos, Jungar Banner Maternal and Child Healthcare Hospital of Ordos, Otog Banner Maternal and Child Healthcare Hospital of Ordos, Dongsheng District Maternal and Child Healthcare Hospital of Ordos, Otog Front Banner Maternal and Child Healthcare Hospital of Ordos, Dalad Banner Maternal and Child Healthcare Hospital of Ordos, Wushen Banner Maternal and Child Healthcare Hospital of Ordos for their contribution in study implementation and data acquisition. This work has been supported by the Tencent Sustainable Social Value Inclusive Health Lab” and Chongqing Tencent Sustainable Development Foundation.

Ethics approval and consent to participate

Ethical approval was obtained from the Ethics and Protocol Review Committee of the School of Population Medicine and Public Health, Chinese Academy of Medical Science & Peking Union Medical College with approval number [CAMS-PUMC-IEC-2022-077]. All methods were carried out in accordance with relevant ethical guidelines and regulations.

Consent for publication

Not applicable.

Availability of data and materials

The datasets used and/or analyzed during the current study are available from the corresponding author on reasonable request.

Competing interests

The authors declare that they have no competing interests

Funding

This work has been supported by the Tencent Sustainable Social Value Inclusive Health Lab and through the ChongQing Tencent Sustainable Development Foundation “Comprehensive Prevention and Control Demonstration Project for Eliminating Cervical Cancer and Breast Cancer in Low Health Resource Areas of China” (Project Number：SD20240904145730)

Authors' contributions

The contribution of each co-author has been substantial and integral to the completion of this study. YLQ encompassed overseeing the project and, alongside FHZ, initiating and conceptualizing the idea of this study. HJY and QKW are responsible for drafting the manuscript, while HJY contributed significantly to the collection of materials. All authors have read and approved the manuscript, and we collectively concur with the submission to your esteemed journal.

Bray F, Laversanne M, Sung H, Ferlay J, Siegel RL, Soerjomataram I, Jemal A: Global cancer statistics 2022: GLOBOCAN estimates of incidence and mortality worldwide for 36 cancers in 185 countries. CA Cancer J Clin 2024.
Allemani C, Matsuda T, Di Carlo V, Harewood R, Matz M, Nikšić M, Bonaventure A, Valkov M, Johnson CJ, Estève J et al: Global surveillance of trends in cancer survival 2000-14 (CONCORD-3): analysis of individual records for 37 513 025 patients diagnosed with one of 18 cancers from 322 population-based registries in 71 countries. Lancet (London, England) 2018, 391(10125):1023-1075.
Allemani C, Weir HK, Carreira H, Harewood R, Spika D, Wang XS, Bannon F, Ahn JV, Johnson CJ, Bonaventure A et al: Global surveillance of cancer survival 1995-2009: analysis of individual data for 25,676,887 patients from 279 population-based registries in 67 countries (CONCORD-2). Lancet (London, England) 2015, 385(9972):977-1010.
Sung H, Ferlay J, Siegel RL, Laversanne M, Soerjomataram I, Jemal A, Bray F: Global Cancer Statistics 2020: GLOBOCAN Estimates of Incidence and Mortality Worldwide for 36 Cancers in 185 Countries. CA Cancer J Clin 2021, 71(3):209-249.
minlu Z, peng P, chunxiao W, yangming G, siwei Z, wanqing C, pingping B: Report of breast cancer incidence and mortality in China registry regions, 2008-2012. Chin J Oncol 2019, 41(4):315-320.
Yan-xia Z, lan M, Zhenqiang L, linhong W, qi W, jiuling W: Ultrasoud-based breast cancer screening in Chinese rural women in 2014: a multi-center data analysis. Chin J Cancer Prev Treat 2020, 27(3):1673-5269.
Letter on the Reply to Proposal No. 0873 (Medical and Sports No. 094) of the Second Session of the 13th National Committee of the Chinese People's Political Consultative Conference [http://www.nhc.gov.cn/wjw/tia/202009/511b9b02b53e4aa2a2b67cdbf6878435.shtml]
Zhang M, Bao H, Zhang X, Huang Z, Zhao Z, Li C, Zhou M, Wu J, Wang L, Wang L: Breast Cancer Screening Coverage - China, 2018-2019. China CDC Wkly 2023, 5(15):321-326.
Kurani SS, McCoy RG, Lampman MA, Doubeni CA, Finney Rutten LJ, Inselman JW, Giblon RE, Bunkers KS, Stroebel RJ, Rushlow D et al: Association of Neighborhood Measures of Social Determinants of Health With Breast, Cervical, and Colorectal Cancer Screening Rates in the US Midwest. JAMA network open 2020, 3(3):e200618-e200618.
Glasgow RE, Harden SM, Gaglio B, Rabin B, Smith ML, Porter GC, Ory MG, Estabrooks PA: RE-AIM Planning and Evaluation Framework: Adapting to New Science and Practice With a 20-Year Review. 2019, 7.
Statistical Bulletin of National Economic and Social Development of Ordos City in 2015 [http://www.ordos.gov.cn/gk_128120/tjxx/tjgb/201603/t20160319_2458363.html]
World Bank: Hospital beds (per 1000 people)-world (updated 2024-09-19) [https://data.worldbank.org/indicator/SH.MED.BEDS.ZS?locations=1W&most_recent_year_desc=false]
wenjie C, weiqi D, liying Q, huimin L, peng W, yunfeng X: Incidence and mortality of female breast cancer in Inner Mongolia in 2015 and its trend from 2010 to 2015. China Cancer 2020, 29(10):736-743.
Zhu J, Ge Z, Xia J, Liu Q, Ran Q, Yang Y: Status quo and problem analysis of cervical cancer screening program in China: Based on RE-AIM framework. Frontiers in public health 2022, 10:987787.
Liu Y, Chu H, Peng K, Yin X, Huang L, Wu Y, Pearson SA, Li N, Elliott P, Yan LL et al: Factors Associated With the Use of a Salt Substitute in Rural China. JAMA Netw Open 2021, 4(12):e2137745.
Li M, Wang H, Qu N, Piao H, Zhu B: Breast cancer screening and early diagnosis in China: a systematic review and meta-analysis on 10.72 million women. BMC women's health 2024, 24(1):97.
Peterson EB, Ostroff JS, DuHamel KN, D'Agostino TA, Hernandez M, Canzona MR, Bylund CL: Impact of provider-patient communication on cancer screening adherence: A systematic review. Prev Med 2016, 93:96-105.
Riganti P, Ruiz Yanzi MV, Escobar Liquitay CM, Sgarbossa NJ, Alarcon-Ruiz CA, Kopitowski KS, Franco JV: Shared decision-making for supporting women's decisions about breast cancer screening. The Cochrane database of systematic reviews 2024, 5(5):Cd013822.
Zhu X, Squiers L, Helmueller L, Madson G, Southwell BG, Alam S, Finney Rutten LJ: Provider communication contributes to colorectal cancer screening intention through improving screening outcome expectancies and perceived behavioral control. Social science & medicine (1982) 2024, 340:116397.
Bittencourt L, Scarinci IC: Training Community Health Workers to promote breast cancer screening in Brazil. Health promotion international 2019, 34(1):95-101.
Sayed S, Ngugi AK, Nwosu N, Mutebi MC, Ochieng P, Mwenda AS, Salam RA: Training health workers in clinical breast examination for early detection of breast cancer in low- and middle-income countries. The Cochrane database of systematic reviews 2023, 4(4):Cd012515.
Korn AR, Walsh-Bailey C, Correa-Mendez M, DelNero P, Pilar M, Sandler B, Brownson RC, Emmons KM, Oh AY: Social determinants of health and US cancer screening interventions: A systematic review. CA Cancer J Clin 2023, 73(5):461-479.
Jhumkhawala V, Lobaina D, Okwaraji G, Zerrouki Y, Burgoa S, Marciniak A, Densley S, Rao M, Diaz D, Knecht M et al: Social determinants of health and health inequities in breast cancer screening: a scoping review. Frontiers in public health 2024, 12:1354717.
Shulman LN, Mpunga T, Tapela N, Wagner CM, Fadelu T, Binagwaho A: Bringing cancer care to the poor: experiences from Rwanda. Nat Rev Cancer 2014, 14(12):815-821.
Neta G: Ensuring the Value of Cancer Research: Opportunities in Implementation Science. Trends Cancer 2021, 7(2):87-89.
Ramanadhan S, Minsky S, Martinez-Dominguez V, Viswanath K: Building practitioner networks to support dissemination and implementation of evidence-based programs in community settings. Translational Behavioral Medicine 2017, 7(3):532-541.
Okasako-Schmucker DL, Peng Y, Cobb J, Buchanan LR, Xiong KZ, Mercer SL, Sabatino SA, Melillo S, Remington PL, Kumanyika SK et al: Community Health Workers to Increase Cancer Screening: 3 Community Guide Systematic Reviews. American journal of preventive medicine 2023, 64(4):579-594.
Duggan C, Dvaladze AL, Tsu V, Jeronimo J, Constant TKH, Romanoff A, Scheel JR, Patel S, Gralow JR, Anderson BO: Resource-stratified implementation of a community-based breast cancer management programme in Peru. Lancet Oncol 2017, 18(10):e607-e617.
Damiani G, Basso D, Acampora A, Bianchi CB, Silvestrini G, Frisicale EM, Sassi F, Ricciardi W: The impact of level of education on adherence to breast and cervical cancer screening: Evidence from a systematic review and meta-analysis. Prev Med 2015, 81:281-289.
Secginli S, Nahcivan NO, Gunes G, Fernandez R: Interventions Promoting Breast Cancer Screening Among Turkish Women With Global Implications: A Systematic Review. Worldviews on evidence-based nursing 2017, 14(4):316-323.
Sangwan RK, Huda RK, Panigrahi A, Toteja GS, Sharma AK, Thakor M, Kumar P: Strengthening breast cancer screening program through health education of women and capacity building of primary healthcare providers. Frontiers in public health 2023, 11:1276853.

Table 6 is available in the Supplementary Files section.

No competing interests reported.

Table6.docx

Implementation of Breast Cancer Screening and Its Effect Among Chinese Rural Women: A Mixed-Methods Evaluation Based on RE-AIM Framework

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Abstract

Background:

Methods:

Results:

Conclusion:

Figures

Introduction

Methods

Settings and participants

Screening methods

Data collection

Screening data

Semi-structured interviews with health workers of MCHHs

Data analysis

Results

Discussion

Conclusion

Declarations

References

Table

Additional Declarations

Supplementary Files

Status:

Version 1