Analysis of breast cancer cases according to county-level poverty status in 3.5 million rural women who participated in a breast cancer screening program of Hunan province, China from 2016 to 2018.

The Hunan provincial government has implemented a free breast cancer screening program for rural women aged 35 to 64 years from 2016, under a 2015 policy aimed at of poverty eradication and improving women's health in China. However, there has been no population study of the breast cancer screening program in China to date, especially considering exploring differences related to the area's poverty status. We explored differences in risk factors, clinical examination results, and clinicopathological features among breast cancer patients in poor compared with non-poor counties in rural areas of Hunan province from 2016 to 2018 using χ and Fisher's exact test, and multivariate logistic regression analysis. A total of 3,151,679 women from rural areas participated in the screening program, and the breast cancer prevalence was 37.09/10. Breast cancer prevalence was lower in poor (29.68/10) than in non-poor counties (43.13/10). There were differences between breast cancers in poor and non-poor counties in terms of cysts, margins, internal echo, blood flow in solid masses in the right breast on ultrasound examination, lump structure in mammograms, and clinicopathological staging and grading in pathological examinations. Breast cancer in poor counties was more likely to be diagnosed at later stages as determined by ultrasound, mammography, and pathological examinations. Furthermore, indexes of the breast screening program including early detection, prevalence, pathological examination, and mammography examination were lower in poor compared with non-poor counties. Multivariate logistic regression analysis showed that education, ethnicity, reproductive history and the year 2017 were associated with an increased risk of breast cancer in poor counties (odds ratio >1, P < .05). In conclusion, women in poor areas were more likely to be diagnosed with breast cancer at a later stage compared with women in non-poor areas. Women in poor areas of Hunan province should therefore have better access to diagnostic and clinical services to help rectify this situation.

Introduction

Breast cancer is the most frequently diagnosed cancer and the second leading cause of cancer-related deaths in women worldwide.[ It is estimated that over 508,000 women die from breast cancer globally each year and ∼58% of those live in low- and middle-income countries. Breast cancer is now the most common cancer in Chinese women, and its incidence in China has increased by 3% to 5% annually for the last 20 years, which is much faster than the average annual global increase of 0.5%.[ Notably, breast cancer incidence and mortality rates among Chinese women in rural areas have been increasing rapidly during the last 10 years.[ The incidence and mortality rates of breast cancer in the eastern and middle areas of China are similar to or higher than those in western areas,[ and the estimated age-standardized death rate due to breast cancer among women in Hunan province in 2013 was 7.3/10,[ which was higher than the Chinese average of 6.7/10.[

China has undergone significant development and remarkable change in its social economy, resulting in a shift from a predominately rural lifestyle to a more Western/urban lifestyle over recent decades.[ The risk factors for breast cancer are prevalent, and include early menarche, late menopause, nulliparity, and no history of breastfeeding.[ The incidence and mortality of breast cancer in China are thus expected to continue to increase especially in rural rather than urban areas.[ Individuals living in poorer areas are less likely to seek cancer screening compared with individuals living in wealthier areas because of the lack of diagnostic and screening opportunities throughout rural areas.[ Furthermore, women in poor areas are more likely to be diagnosed with breast cancer at later stages than those in more affluent areas.[ Breast cancer screening programs are mostly applied in upper-middle and high income countries, and are less likely to occur in low-income and lower-middle income countries.[ It is therefore necessary to carry out population-based breast cancer screening in poor areas.[ No nationwide breast cancer population screening has been implemented in China to date because of difficulties associated with large-scale screening programs, and no large-scale, geographically representative study of breast cancer screening has been conducted among the general population. However, Hunan province organized a population-based breast cancer screening program in rural areas from 2016 to 2018 with government support.

This study explored the influence of economics on population-based breast cancer screening programs and the clinical epidemiological characteristics of breast cancer in poor and non-poor counties in rural areas of Hunan province, China, from 2016 to 2018. The results suggest policy changes aimed at improving breast cancer screening programs, improving health, and alleviating poverty in rural areas of China in the future.

Materials and methods

Subjects and study design

This study was based on breast screening programs in Hunan province, China, which were required to carry out breast screening for at least one million women from rural areas each year from 2016 to 2018. The inclusion criteria were:

age 35 to 64 years;

never diagnosed with breast cancer;

rural registered women;

voluntarily amenable to undergoing breast screening; and

not pregnant at the time of enrollment.

The exclusion criteria were:

pregnant women;

refusal to participate;

a history of breast cancer;

difficulty in obtaining information from the woman; and

not locally registered rural women.

All the subjects were familiar with the purpose and procedures of the breast screening program and provided written informed consent for participation in the study. All study protocols were approved by the Ethics Committee of the Hunan Provincial Maternal and Children Health Care Hospital.

Screening protocols and procedures

Trained investigators registered the subjects and obtained basic information such as age, education, ethnicity, menstrual history, family history, and fertility history. Subjects then underwent clinical breast examination and breast ultrasonography (BUS). During the ultrasound examination, the physician scanned each quadrant of the breast using the radiating and crossing method at the center of the nipple and completed the ultrasound examination and diagnosis report for each subject. Subjects with positive or suspected positive results of BUS received mammography (MAM) and patients who were MAM-positive or suspected positive were subjected to further pathological examination. Patients who were positive upon pathological examination were recalled for treatment and followed in the clinic. A schematic of the screening process is shown in Figure 1.

Figure 1

Schematic of the breast cancer screening process followed in Hunan province, China.

Data collection

We collected breast cancer screening information from China's major public health service projects’ direct reporting system. We obtained quarterly report data on the breast cancer screening program in the rural areas of Hunan province in China from 2016 to 2018. Data in the quarterly report included yearly checkup information, the results of BUS, MAM, and pathological examination, as well as the tumor, node, and metastasis (TNM) stage. We obtained information on breast cancer cases in the system, including basic and clinical information, results of BUS, MAM, and pathological examination, and TNM stage and grade.

Hunan province has a population of 71.47 million people and covers 21.18 km2 in central China, including 90 counties in rural and 33 in urban areas.[ Fifty-one of the rural counties are considered to be poor and 39 as non-poor. The list of poor and non-poor counties was stipulated by the provincial government and the geographical positions are shown in Figure 2. The reporting system was established in 2009 and has expanded to cover all 90 counties in rural areas throughout the entire province from 2016.

Figure 2

Geographical position of breast cancer screening counties in Hunan province, China.

Data quality control

The information system was subjected to four audit levels to ensure data accuracy: county, prefectural, provincial, and national. The county-level unit submitting the original data was responsible for the examination, verification, and modification of the data after receipt of all suggestions made during the initial review. The health administration departments at the prefectural, provincial, and national levels were subsequently responsible for reviewing the reported data.

Statistical analyses

Statistical analyses were performed using SPSS 20.0 software. Differences in the basic information, results of BUS, MAM, and pathological examination, and differences in treatment between breast cancer patients in poor and non-poor counties were analyzed using χ2 and Fisher's exact tests. Multivariate logistic regression analyses were performed to assess the risk factors of breast cancer patients in poor counties. All statistical tests were considered significant when P < .05.

Results

Comparison of breast cancer screening program in relation to county poverty level

Comparison of the breast cancer screening programs in non-poor and poor counties was summarized in Table 1. A total of 3,151,679 women from rural areas were screened for breast cancer, of whom 82,333 women were found to be 0-grade and 3-grade by BUS examination. A total of 62,577 women underwent MAM, accounting for 76% of all women who were 0-grade or 3-grade by BUS examination. The proportions of women in non-poor and poor counties who underwent histopathological examination in were 79.60% and 63.60%, respectively. The total number of breast cancer cases was 1,169 and 601 women received an early diagnosis of breast cancer. The prevalence of breast cancer in non-poor and poor counties were 43.13/105 and 29.68/105, respectively.

Table 1

Comparison of evaluation indicators in the breast cancer screening population between poor and non-poor counties.

Comparison of basic and clinical information in relation to county poverty level

Basic and clinical information are shown in Table 2. The number of breast cancer cases in poor counties increased in 2017 compared with 2016 (N = 181, 43.10% vs N = 255, 34.05%, P = .003). The median age of women diagnosed with breast cancers was 50 years in both poor and non-poor counties. Breast cancer patients in non-poor and poor counties mainly received middle high school (N = 336, 44.86%) and primary school educations (N = 205, 48.84%), respectively. The proportion of breast cancer patients of Han ethnicity was significantly lower in poor compared with non-poor counties (N = 310, 73.81% vs N = 682, 91.05%, P < .001, respectively). Most breast cancer patients in both groups experienced menarche at 13 to 14 years of age (N = 406, 54.21% vs N = 231, 55.00%, P = .046). The proportion of breast cancer patients with a reproductive history was significantly lower in poor compared with non-poor counties (N = 414, 55.27% vs N = 741, 98.93%, P = .04). However, there were no significant differences between breast cancer patients in the two groups with respect to age, age at menarche, breastfeeding history, surgical history, hormone replacement history, and family history.

Table 2

Comparison of basic and clinical information among female breast cancer cases between poor and non-poor counties.

Comparison of BUS results in relation to county poverty level

There were significant differences in the aspect ratio and edge of the solid mass in the left breast and cyst, the edge of the solid mass and the internal echo and blood flow of the solid mass in the right breast between the two groups (Table 3). Breast cancers in women in poor counties were significantly more likely to have a solid tumor aspect ratio >1 (N = 94, 40.17% vs N = 162, 37.85%, P = .039) and an unclear edge of the solid mass in the left breast (N = 141, 60.26% vs N = 232, 54.21%, P = .028). Conversely, cancers in women from non-poor counties were significantly less likely to have a complicated cyst (N = 18, 2.00% vs N = 15, 4.29%, P = .016) in the right breast. Moreover, the proportion of cancers without blood flow in the solid mass (N = 156, 36.19% vs N = 51, 21.61%, P < .001) and with a clear edge of the solid mass (N = 140, 32.48% vs N = 53, 22.46%, P = .02) in the right breast were both higher in women in non-poor counties. Women with breast cancer in non-poor counties were significantly more likely to be encouraged to undergo a pathological examination compared with those in poor counties (N = 444, 59.28% vs N = 203, 48.33%, P < .001, respectively). Overall, BUS examination results revealed differences in cysts, margins, internal echo, and blood flow in the solid mass in the right breast between the two groups. Examination of women with breast cancer showed that patients from poor counties were more likely to have complex cysts, unclear edges, high internal echoes, an aspect ratio of the solid mass >1, and rich blood flow to the solid mass.

Table 3

Comparison of BUS results among female breast cancer cases between and non-poor counties.

Comparison of MAM results in relation to county poverty level

Women with breast cancers in poor counties were significantly more likely to have a structural disorder in the solid mass in both the left (N = 54, 25.35% vs N = 85, 23.61%, P = .006) and right breasts (N = 48, 22.54% vs N = 68, 18.89%, P = .045), and to be followed-up with a pathological examination (N = 201, 47.86% vs N = 323, 43.12%, P = .022) (Table 4). Women in poor counties thus had larger breast tumors based on MAM results for both breasts.

Table 4

Comparison of MAM results among female breast cancer cases between poor and non-poor counties.

The patients’ pathological characteristics are displayed in Table 5. Regarding clinical and pathological staging, breast cancers were staged to a lesser extent in poor compared with non-poor counties (N = 203, 49.27% vs N = 484, 65.58%, P < .001 and N = 187, 45.39% vs N = 439, 59.49%, P < .001, respectively). Breast cancers in women in non-poor counties were significantly more likely to be considered as c-TNM clinical staging grade 2 (N = 282, 59.75%, N = 82, 43.62%, P = .008) and p-TNM clinical staging grade 2 (N = 245, 57.92%, N = 72, 41.62%, P = .009). However, breast cancer patients in poor counties were significantly less likely to be treated following a pathological diagnosis (N = 394, 93.81%, N = 713, 95.19%, P = .026). Breast cancer cases in poor counties were less likely to undergo clinical and pathological staging in both breasts compared with women in non-poor counties.

Table 5

Comparison of pathological examination results among female breast cancer cases between poor and non-poor counties.

Multivariate logistic regression analysis of risk factors among breast cancer patients in poor counties

Data for 1015 women from poor counties with breast cancer were analyzed by multivariate logistic regression analysis, after deleting cases with missing values of analysis variables. The following risk factors were identified as related to breast cancer in poor counties: year (2017 compared with 2016), education, ethnicity, and reproductive history (odds ratio >1, P < .05). All results of the analysis are listed in Table 6.

Table 6

Binary logistic regression analysis of female breast cancer related factors in poor counties.

Discussion

To the best of our knowledge, this is the first study analyzing data from the population breast cancer screening program in China. In this study, we explored differences in the effects of implementing the breast cancer screening program and in clinical examination results between breast cancer patients in poor and non-poor counties in rural areas of Hunan province from 2016 to 2018. The results showed that indexes of the breast screening program including the proportion of breast cancers detected early, breast cancer prevalence, the proportion of breast cancer patients who underwent pathological examination, and the MAM examination rate were all lower in poor compared with non-poor counties. The prevalence of breast cancer was lower in poor areas, in accordance with the results of other studies.[ However, the prevalence of breast cancer in rural areas of Hunan province in our study was 37.09/105, which was higher than the 25.28/105 reported in rural areas of China in 2010 based on 145 population-based cancer registries[ and the 21.0/105 in rural areas of Jiangsu province based on statistics from eligible cancer registries in Jiangsu in China from 2006 to 2010.[ Furthermore, the prevalence was lower than the 73.4/105 reported in developed countries but higher than the 31.3/105 in developing countries, according to global cancer statistics from 2012.[ Breast cancer patients in poor rural areas were relatively undereducated and underwent menarche at an older age compared with patients in non-poor areas. Worldwide, the prevalence of breast cancer increases in parallel with socioeconomic development, and breast cancer risk has changed in parallel with socioeconomic development and urbanization in China over the past three decades.[ The allocation of and accessibility to health resources is reduced in poor counties compared with non-poor counties, resulting in lower pathological examination and MAM rates. Regional differences in breast cancer prevalence and allocation of and accessibility to health resources should thus be taken into account when planning breast screening programs.[

The present study identified differences in various factors including year, level of education, ethnicity, age at menarche, and reproductive history between breast cancer patients in poor and non-poor counties. Furthermore, multivariate logistic regression analysis showed that the year (2017 vs 2016), non-Han ethnicity, education, and reproductive history were associated with an increased risk of breast cancer in poor counties. Since the program was launched in 2016, women with symptoms volunteered to participate in the program in 2017, resulting in an increase in the number of patients diagnosed with breast cancer.

Racial disparity persists in breast screening, such as between Hispanic and non-Hispanic white women.[ In this present study, women of non-Han ethnicity had a lower education level and socioeconomic status, and reduced access to health care. Age at menarche was identified as a breast cancer risk factor[ and early menarche has been associated with an increased risk of breast cancer.[ Western style fast food and high-sugar drinks have become increasingly popular among children in China. Ma et al reported that the age of menarche among healthy urban Chinese girls decreased from 13.5 years in 1979 to 12.27 years between 2003 and 2005.[ Age at menarche (>13 years compared with ≤13 years) was not found to be a risk factor after adjusting for all the variables with differences in the single logistic regression analysis in our study. Studies over the past several decades have indicated that individuals living in less-developed areas often had poorer general health than individuals living in relatively developed areas.[ This could also help to explain the current differences in breast cancer screening results between women in poor and non-poor counties.

Doctors more readily advised women with breast cancer in poor counties to receive pathological examination following BUS and MAM examinations. However, the proportion of women receiving treatment for breast cancer in poor counties was lower than that for women in non-poor counties, indicating that women with breast cancer in poor counties had a higher rate of malignancy and reduced access to medical services, despite the lower prevalence of breast cancer in poor compared with non-poor counties. Other similar studies have come to the same conclusion. For example, Williams et al found that the odds of a late diagnosis among women living in non-metropolitan or rural counties was >11% higher compared with their metropolitan or urban counterparts, and that black women had a 1.5-fold increased odds of being diagnosed with late-stage breast cancer compared with their white counterparts, despite the fact that black women have a lower prevalence of breast cancer than white women.[ Nguyen-Pham et al found that breast cancer patients from rural areas had 1.19-fold higher odds of being diagnosed with late-stage breast cancer compared with patients from urban areas.[ Anderson et al concluded that a lack of breast cancer screening and living in poorer rural areas were associated with a 3.31-fold increase in the rate of diagnosis of later-stage breast cancer in Appalachia, compared with women living in less deprived regions.[ Socioeconomic status has been identified as a key determinant of cancer stage at diagnosis in western countries,[ and a systematic study of the relationship between socioeconomic status and breast cancer stage at diagnosis in China also concluded that women in low socioeconomic status areas were more likely to be diagnosed at a later breast cancer stage than those in higher socioeconomic status areas.[ The current results suggested that women with breast cancer in poor counties are in need of more diagnostic and clinical, rather than screening services. This finding emphasizes the fact that just providing free screening services cannot make up for a lack of preventive care for low-income and uninsured women.[

Environmental factors play an important role in the development of cancer and suggest that region-tailored cancer prevention strategies are warranted.[ To improve breast cancer outcomes in rural areas of China, we suggest that free screening services should be supported by more diagnostic and clinical services as a long-term policy to benefit women in rural areas, and that these services should be made available in poor areas in Hunan province.

Our study had some limitations. First, we did not investigate some important risk factors such as economic income and body mass index because we obtained the data from the unified national register. Importantly, we could not analyze and compare the age distributions between poor and non-poor counties to determine if the apparently lower prevalence of breast cancer in poor counties was due to the age distribution because of data unavailability. Second, there was recall bias regarding the basic information obtained for the breast cancer cases. Third, although the whole province carried out a unified training for all doctors involved in administering BUS, MAM, and pathological examinations, there were differences in the qualities of the examinations and information filling, which also led to information missing.

Conclusions

Analysis of population-based breast cancer screening programs in rural areas revealed differences in the evaluation indicators and clinicopathological characteristics of the breast cancer cases in relation to county-level poverty status. Although the prevalence of breast cancer was lower in poor than in non-poor counties, women in poor areas were more likely to be diagnosed at later stage than those in non-poor areas, and additional diagnostic and clinical services should be provided in poor areas to address these concerns.

Acknowledgments

We wish to think all the staff of the breast screening program in Hunan province, China. We thank Liwen Bianji, Edanz Editing China (www.liwenbianji.cn/ac), for editing the English text of a draft of this manuscript

Author contributions

Conceptualization: xiong lili, Wu Yinglan, Fang Junqun.

Data curation: xiong lili, Wang Aihua, Li Hongyun, Liang Ting, Wang Yingxia, Xie Donghua, Kong Fanjuan, Fang Junqun, Chen Xianghua.

Formal analysis: xiong lili, Yang Guanghui.

Methodology: xiong lili, Chen Xianghua.

Project administration: Liu Zhiyu.

Software: xiong lili.

Supervision: xiong lili, Liu Zhiyu, Fang Junqun.

Writing – original draft: xiong lili.

Writing – review & editing: xiong lili, Fang Junqun, Chen Xianghua.