Global Health and Cancer
Exploring Knowledge, Attitudes, and Practices Related to Breast and Cervical Cancers in Mongolia: A National Population-Based Survey POOJA YERRAMILLI,a OTGONDUYA DUGEE,b PALAM ENKHTUYA,b FELICIA M. KNAUL,c ALESSANDRO R. DEMAIOc,d a
Perelman School of Medicine, University of Pennsylvania, Philadelphia, Pennsylvania, USA; bPublic Health Institute, Ministry of Health of Mongolia, Ulaanbaatar, Mongolia; cHarvard Global Equity Initiative, Harvard Medical School, Boston, Massachusetts, USA; dSchool of Global Health, Department of Public Health, University of Copenhagen, Copenhagen, Denmark Disclosures of potential conflicts of interest may be found at the end of this article.
Key Words. Asia x Noncommunicable disease x Cancer x Public health x Global health
ABSTRACT Background. Mongolia bears the second-highest cancer burden in the world (5,214 disability-adjusted life years per 100,000 people, age standardized). To determine drivers of the growing burden of noncommunicable diseases, including breast and cervical cancers, a national knowledge, attitudes, and practices (KAP) survey was implemented in 2010. Methods. This paper analyzed the results of the 2010 KAP survey, which sampled 3,450 households nationally. Reflecting Mongolian screening policies, women aged 30 and older were included in analyses of questions regarding breast and cervical cancer (n 5 1,193). Univariate and multivariate odds ratios (MORs) were derived through logistic regression to determine associations between demographic covariables (residence, age, education, employment) and survey responses. Results. This study found that 25.7% (95% confidence interval [CI]: 23.3–28.3) and 22.1% (95% CI: 19.8–24.5) of female participants aged 30 years or older self-rated their
knowledge of breast and cervical cancers, respectively, as “none.” Employment and education were associated with greater awareness of both cancers and participation in screening examinations (p , .05). Clinical breast examinations were more common among rural than urban participants (MOR: 1.492; 95% CI: 1.125–1.979). Of all female participants, 17% (95% CI: 15.3–18.5) knew that cervical cancer is vaccine preventable. Conclusion. Our results suggest that cancer control in Mongolia should emphasize health education, particularly among lower-educated, rural, and unemployed women. The health infrastructure should be strengthened to reflect rural to urban migration. Finally, although there is awareness that early detection improves outcomes, a significant proportion of women do not engage in screening. These trends warrant further research on barriers and solutions. The Oncologist 2015;20:1266–1273
Implications for Practice: The rising burden of breast and cervical cancers, particularly in low- and middle-income countries, necessitates the development of effective strategies for cancer control. This paper examines barriers to health service use in Mongolia, a country with a high cancer burden. The 2010 national knowledge, attitude and practices survey data indicate that cancer control efforts should focus on improving health education among lower-educated, rural, and unemployed populations, who display the least knowledge of breast and cervical cancers. Moreover, the findings support the need to emphasize individual risk for disease in cancer education and ensure that the health-care infrastructure reflects Mongolia’s urbanization.
INTRODUCTION Cancer constitutes the second-leading cause of death in Mongolia , a lower-middle income country with a population of roughly 2.8 million people [2–4] (Table 1). A nation with the second-highest overall cancer burden in the world (5,214 disability-adjusted life years per 100,000 population, age standardized, both sexes) , Mongolia also faces the highest global mortality rate for all cancers (161.0 deaths per 100,000, age standardized, both sexes), excluding nonmelanoma skin cancer, and has age-standardized mortality rates of 4.2 and
9.3 per 100,000 women for breast and cervical cancers, respectively . These high rates, in large part, are attributable to the late detection of generally preventable or treatable cancers. Breast and cervical cancers explain a large proportion of the cancer burden in Mongolia; in 2005, approximately 80% of breast cancer cases and 88% of cervical cancer cases were diagnosed in late stages . Although literature on breast and cervical cancers in Mongolia is scarce, recent data and few studies
Correspondence: Pooja Yerramilli, M.Sc., 105 Brinley Court, Philadelphia, Pennsylvania, 19146, USA. Telephone: 609-933-8286; E-Mail: Pooja. [email protected]
Received March 22, 2015; accepted for publication August 21, 2015; published Online First on September 28, 2015. ©AlphaMed Press 1083-7159/2015/$20.00/0 http://dx.doi.org/10.1634/theoncologist.2015-0119
The Oncologist 2015;20:1266–1273 www.TheOncologist.com
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Yerramilli, Dugee, Enkhtuya et al.
Population in 2009 Crude birth rate/Crude death rate, 2005–2010, per 1,000 Human Development Index, 2010
Gross national income per capita, PPP (int. 2009 U.S. $) Population living on ,U.S. $1 PPP int. U.S. $ per day 2005, % Education national net enrollment rate in 2008, %
0.622 (rank: 100 of 169 countries) $3,330 22.4 91.5
Abbreviations: PPP, purchasing power parity; int., international.
indicate that the burden of women’s cancers in the country is rising. Relative to other countries in the region, breast cancer incidence in Mongolia is low, at one-third of that in China . However, the relatively low breast cancer incidence in Mongolia may be due partly to underdiagnosis. In China, where breast cancer screening has improved, at least in urban settings, the proportion of late-stage diagnoses is significantly lower than that in Mongolia: roughly 8% of all cases in Shanghai as opposed to roughly 80% across urban and rural settings in Mongolia . The burden of breast cancer appears to be increasing in Mongolia, as breast cancer-associated mortality shows an upward trend . Moreover, according to a multicenter human papillomavirus (HPV) prevalence survey of all Asian countries, Mongolia has the highest prevalence of cervical HPV DNA in sexually active women , and from 2005 to 2010, the mortality rate due to cervical cancer has increased . As both cancers are preventable and/or treatable if detected early, these patterns highlight the need to analyze health literacy with regard to primary and secondary prevention of women’s cancers. The Mongolian Ministry of Health has recognized both the need and the opportunity to reduce the burden of noncommunicable diseases, including cancers, through several initiatives. One key response has been the development and implementation of a National Cancer Control Plan, 2007-2017 (NCCP) . The NCCP emphasizeshealthpromotion,primaryprevention,andsecondary prevention, particularly for breast and cervical cancers, as means to lower the cancer burden.The objectives are to educate women on the early signs of both cancers for self-referral to physicians and to encourage women to perform breast self-examinations (BSEs) . The Mongolian government hopes for a significant outcome from its awareness campaigns and has set a goal of improving the percentage of patients cured of breast and cervical cancers from 15% in 2007 to 60% in 2017 . The NCCP delineates some specific strategies for care and control of women’s cancers, such as the vaccination of young girls against the HPV as a tool to prevent 70% of cervical cancer cases . Further, the government has taken significant steps to improve access to breast and cervical cancer screening programs. By law, Mongolia ensures universal coverage for primary health services. Through compulsory social health insurance (SHI) and subsidies to uninsured and vulnerable groups, the country was able to achieve legal coverage of 98.6% of the population in 2011. While SHI covers individual
services, including outpatient and inpatient care for beneficiaries, the government budget covers preventive, public health, maternal and child care, and chronic and infectious disease services for the entire population, without any associated user charges. Moreover, through several programs, including the National Program for Healthy Mongolians (2006–2008) and the National Program on Integrated Noncommunicable Disease (NCD) Prevention and Control (2006–2013), the government expanded access to free cancer screenings for all Mongolians . Support from the US Millennium Challenge Corporation (MCC) from 2007 to 2013 and the World Health Organization (WHO) has enabled the country to make cervical cancer screening freely available in family clinics.Women in the target age range were invited to participate in screening via text messaging and posts. While 70,000 women were screened in 2013, a drop to roughly 56,000 women was noted in 2014 . Because breast and cervical cancer screening are fully covered through government programs , understanding trends in knowledge and awareness regarding women’s cancers may ultimately help improve use of preventive and screening services, particularly in the current, crucial period following the recent completion of MCC financial and infrastructural support in 2013. Indeed, the NCCP defines as its targets for breast and cervical cancers an increase in the proportion of women reporting knowledge of risk factors, understanding of early symptoms, and seeking such diagnostic tests as Papanicolaou (Pap) smears or mammograms. The NCCP proposes awareness campaigns that are designed to increase knowledge, attitude, and practices related to cancers . Results are to be measured based on knowledge, attitude, and practice (KAP) surveys. KAP surveys collect information regarding the target population’s perceptions of risk factors, health priorities, and knowledge of health conditions, and are a useful public-health monitoring and evaluation modality . Currently, many NCD programs in Mongolia are predicated on NCD risk-factor data collected and analyzed based on World Health Organization’s STEPwise approach to surveillance (STEPs). While these data are crucial in the design of health policies, they do not provide information regarding knowledge and attitudes toward NCDs and associated risk factors . Thus, in 2010, a national KAP survey on NCDs, including women’s cancers, as suggested in the NCCP, was conducted to complement the STEPs survey and provide a baseline for monitoring.This paper is one in a series of publications exploring data from the 2010 national NCD KAP survey with the purpose of informing and contextualizing public health policies in Mongolia. The objective of this research is to determine the levels of and some of the drivers behind health literacy and access to services with regard to breast and cervical cancer prevention among Mongolian women and, ultimately, to help inform the design of targeted interventions.
METHODS Setting and Population A door-to-door, household-based questionnaire was conducted on a nationally representative sample. The full study protocol has been published . Trained, Mongolian field workers from the National Institute for Public Health administered the questionnaire. ©AlphaMed Press 2015
Table 1. Demographics in Mongolia
Breast and Cervical Cancers KAP Survey in Mongolia
Table 2. Disaggregated descriptive information on sample population (women only)
Table 3. Disaggregated descriptive information on sample population (women aged $30 years)
Total Age, years 15–19 20–24 25–29 30–34 35–39 40–44 45–49 50–54 55–59 $60 Location Urban Rural Education Primary or less Secondary school Tertiary school Employment Student Retired/home Unemployed Employed
Women $30 years old, N Age 30–39 40–49 50–59 $60 Location Urban Rural Education Primary or less Secondary school Tertiary school Employment Student Retired/homemaker Unemployed Employed
318 (15.6) 264 (13.0) 254 (12.5) 187 (9.2) 202 (9.9) 201 (9.9) 156 (7.7) 150 (7.4) 173 (8.5) 132 (6.5) 1,035 (50.8) 1,002 (49.2) 112 (5.5) 1,407 (69.1) 517 (25.4) 387 (19.0) 530 (36.0) 304 (14.9) 807 (39.6)
Sample Size A nationally representative sample was designed considering a 95% confidence interval.The sample size was calculated such that disaggregated data analysis according to sex, urban residence, and other key demographic variables could be conducted. A design effect based on the WHO STEPs methodologies was adopted. The final sample size for the KAP study was calculated to be 3,854, accounting for an assumed nonresponse rate of 10%. Of this, a total of 2,037 women participated in the KAP survey. These participants were roughly evenly distributed between rural and urban residences, and 58.9% were above the age of 30 years (n 5 1,201) (Tables 2 and 3). Reflecting national screening guidelines, only women 30 years old or older were included in analysis for questions 78–88. Among those who fit the demographic criteria, 2 students, and 5 respondents for whom employment data were not collected, were excluded because of inadequate sample size, resulting in the total number of 1,193 women. All women (N 5 2,037) were included in analysis of questions 89 and 90, which focus on knowledge of the HPV vaccine.
389 (32.4) 357 (29.7) 323 (26.9) 132 (11.0) 606 (50.5) 595 (49.5) 75 (6.2) 843 (70.2) 283 (23.6) 2 (0.2) 418 (34.8) 167 (13.9) 608 (50.6)
cluster sampling. Sampling for primary and secondary units used a proportional population to size method. Simple random sampling from household lists was applied for tertiary sampling units. Finally, a Kish method was used to select participants within households . The eligibility criteria for participants included permanent residency in the household sampled and age between 15 and 64 years. A total of 3,450 participants completed the survey. While the KAP survey does not sample the same participants as the 2009 WHO STEPs survey, both methodologies are aligned and draw nationally representative samples from the same general population.
Questionnaire The KAP survey was interviewer administered and quantitative. The 102 questions covered demographic and socioeconomic characteristics of the participants. All women were asked if they have ever been told that they have or had breast or cervical cancers. Knowledge, attitudes, and practices related to breast and cervical cancers were gauged through 9 questions administered to women aged 30 years or older, and 2 questions administered to all female survey participants. The first section (six questions) focused on breast cancer while the second section (five questions) related to cervical cancer, as shown in the supplemental online Appendix.
To optimize the scientific rigor of this research, several processes were included in the questionnaire methodologies, including the following:
Sampling Methods Participants were selected from households in 21 urban and 21 rural sites across Mongolia through multistage, random
1. Translation and back translation: Questionnaire questions were developed first in English with a panel of international
©AlphaMed Press 2015
and local research and medical experts. These questions were then translated into Mongolian by specialist medical translators and then back into English again by a separate, nonmedical translator before they were finally checked for consistency by the research team. 2. Peer and expert review: A panel of medical and research experts, primarily Mongolian, was formed to review the research design and questionnaire development. 3. Pretesting using cognitive interviewing: A process of cognitive interviewing was used to study the interpretation of the questionnaire questions on lay volunteers. This involves verbalizing the thought processes occurring while reading the questions. 4. Piloting: The questionnaire was piloted repeatedly by the field workers during their training for implementation. This allowed for the questionnaire delivery to become practiced and fluid, and also for final errors, confusion, or inconsistencies to be amended by the research team.
Ethics Approval This data collection was conducted accordingto the principles of the Helsinki declaration and was approved by the Mongolian National Ministry of Health’s Medical Ethical Committee on October 06, 2010. Participation in the research was voluntary. No financial remuneration was offered. Participants consented to complete the questionnaire once informed of the methodology, use of data, and anonymity and confidentiality of their responses.
Data Analysis Data entry and analysis were completed using Statistical Package for Social Sciences version 20.00 (IBM Corp., Armonk, New York, USA, http://www-01.ibm.com). Bivariate and multivariate (adjusted) odds ratios (MORs) for each of the dependent variables (responses to survey questions) were derived through logistic regression models. Covariables included in multivariate analyses were urban residence, age, education, and employment. Age was transformed into a categorical variable with intervals of 10 years. Questions 78–81 and 84, 88, and 90 were transformed into binomial variables, as shown in Tables 4 and 5. Additional analyses included different combinations of covariables and stratification by such variables as residence; however, none improved or yielded statistically significant results and are not reported in this paper. Statistical significance was defined as p , .05 for all tests.
RESULTS Knowledge, Attitudes, and Practices Toward Breast Cancer Screening Of the women sampled, 25.7% (95% CI: 23.3%–28.3%) rated their knowledge of breast cancer as “nothing at all.” Basic knowledge of breast cancer was higher among more educated and urban participants. These associations remain statistically significant in the multivariate logistic models (all p , .05). Further, lack of breast cancer awareness was significantly higher among unemployed (MOR: 1.718; p 5 .017) and lower among employed participants (MOR: 0.608; p 5 .011), than among homemakers or retired respondents (Table 4).
Approximately 49.3% (95% CI: 46.4%–52.2%) of the women sampled stated that they never worry that breast cancer can affect them or their families. The differences in responses among demographic subgroups were not statistically significant. The majority of participants affirmed that finding breast cancer early confers higher chances of survival (91.1%; 95% CI: 89.3%–92.6%) and that it is possible for women to look for early signs ofcancer in their own breasts through BSE (80.6%; 95% CI: 78.3%–82.8%). Yet after the interviewer explained a BSE, only 65.1% (95% CI: 62.3%–67.7%) of respondents answered that they knew how to conduct the examination. Those participants who completed secondary (MOR: 3.071; p 5 .000) or tertiary education (MOR: 3.920; p 5 .000) reported greater BSE ability than those whose education levels were primary or less. Further, participants aged 50– 59 years (p 5 .004) and 60 years old or older (p 5 .041) communicated less ability to perform a BSE than those in the age 30–39 years subgroup (Table 4). Of the 1,193 respondents, 56.1% (95% CI: 53.2%–58.9%) reported having conducted a BSE in the last 3 years. Employment and higher levels of education corresponded to greater odds of having conducted a BSE (Table 4). The majority of respondents (76.5%; 95% CI: 74.0%–78.8%) had a health worker perform a breast examination (clinical breast exam [CBE]) within the last 3 years.The adjusted odds of using this health service are higher among secondary- and tertiary-educated participants than primary or less educated respondents (p 5 .031 and p 5 .006, respectively). In addition, rural participants seemed more likely to avail themselves of this service than were their urban counterparts (Table 4).
Knowledge, Attitudes, and Practices Toward Cervical Cancer Screening More than one-fifth of female participants (21.9%; 95% CI: 19.6%–24.4%) self-rated their knowledge of cervical cancer as “nothing at all.” There was greater lack of cancer awareness among rural than urban participants (MOR: 1.792; p 5 .000) (Table 5). Unemployment and lower levels of education were also linked to lower cervical cancer awareness (all p , .05) (Table 4). Further, participants in the 50–59 year age group had significantly greater awareness than those in the 30–39 year cohort (p 5 .000) (Table 5). After the trained interviewer defined the terms “cervical cancer” and “Pap smear,” approximately 45.7% (95% CI: 43.2%–48.9%) of participants stated that they do not worry that cervical cancer can affect them or their families. Among female participants aged 30 or older, 63.2% (95% CI: 60.4%–65.9%) reported having a Papanicolaou test within the last 3 years.The adjusted odds of participating in such screening were higher for employed participants than those who were retiredor homemakers (MOR5 1.527, p 5 .014), andassociated with increasing levels of education (all p , .002) (Table 3).Those who did not have a Papanicolaou test were asked to select the reason that characterizes why they did not utilize the service. The highest proportion of respondents stated that they did not know that they needed the cervical cancer test (40.1%; 95% CI: 37.3%–42.9%). The second and third most common responses were that the participants did not have time (9.6%; 95% CI: ©AlphaMed Press 2015
Yerramilli, Dugee, Enkhtuya et al.
Breast and Cervical Cancers KAP Survey in Mongolia
1.006 (0.609–1.661) 1.170 (0.802–1.707) 33 (2.8; 1.9–3.9) 151 (12.7; 10.8–14.7)
8.0%–11.4%) or did not know where to access services (9.05%; 95% CI: 7.5%–10.8%) (Table 6). All female participants (all ages) were asked whether cervical cancer is preventable by vaccination. While 16.8% (95% CI: 15.3%–18.5%) responded accurately, 26.5% (95% CI: 24.6%–28.5%) and 56.3% (95% CI: 54.2%–58.5%) answered no or that they did not know, respectively. The odds of answering incorrectly or not knowing versus answering correctly were higher among rural participants than their urban counterparts.
MOR was adjusted for urbanicity, age, education, and employment. a
100 (8.4; 6.9–10.1) 406 (34.0; 31.4–36.8) 1.718 (1.102–2.677) 0.608 (0.415–0.892)
1.150 (0.753–1.757) 1.350 (0.963–1.891)
87 (7.3; 5.9–8.9) 368 (30.9; 28.3–33.5)
1.180 (0.783–1.777) 1.435 (1.041–1.977)
1 88 (7.4; 6.0–9.0) 214 (17.9; 15.8–20.2) 1 267 (22.4; 20.1–24.8) 1
Employment (n) Homemaker/ 119 (10.0; 8.4–11.8) retired (418) Unemployed (167) 72 (6.0; 4.8–7.5) Employed (608) 114 (9.6; 8.0–11.4)
23 (1.9; 1.2–2.) 463 (38.8; 36.0–41.6) 183 (15.3; 13.4–17.5) 1 3.071 (1.831–5.152) 3.920 (2.197–6.994) 31 (2.6; 1.8–3.7) 545 (45.7; 42.8–48.5) 197 (16.5; 14.5–18.7) 1 0.301 (0.178–0.511) 0.150 (0.080–0.282)
1 2.257 (1.079–4.721) 3.011 (1.376–6.593) 9 (0.8; 0.4–1.0) 187 (15.7; 13.7–17.8) 76 (6.4; 5.1–7.9)
97 (8.1; 6.7–9.8) 89 (7.5; 6.1–9.1) 77 (6.5; 5.2–8.0) 42 (3.5; 2.6–4.7) Age group, years (n) 30–39 (384) 40–49 (354) 50–59 (323) $60 (132)
Education (n) Primary or less (73) 43 (3.6; 2.7–4.8) Secondary (838) 226 (18.9; 16.8–21.3) Tertiary (282) 36 (3.0; 2.2–4.2)
121 (10.1; 8.5–12.0) 184 (15.4; 13.5–17.6)
1 2.571 (1.506–4.389) 3.717 (2.064–6.693)
1 1.052 (0.741–1.494) 1.242 (0.843–1.829) 1.088 (0.612–1.933) 84 (7.0; 5.7–8.6) 83 (7.0; 5.6–8.5) 79 (6.6; 5.3–8.2) 26 (2.2; 1.5–3.2)
307 (25.7; 23.3–28.3) Total (N 5 1,193)
Urbanicity (n) Urban (604) Rural (589)
1 0.855 (0.602–1.215) 0.642 (0.430–0.959) 0.837 (0.487–1.439)
238 (20.0; 17.7–22.3) 222 (18.6; 16.5–20.9) 227 (19.0; 16.9–21.4) 86 (7.2; 5.8–8.8)
1 0.971 (0.715–1.319) 1.704 (1.191–2.437) 1.684 (1.021–2.777)
213 (17.9; 15.7–20.1) 207 (17.4; 14.3–19.6) 182 (15.3; 13.3–17.4) 67(5.6; 4.4–7.1)
1 1.112 (0.824–1.499) 1.262 (0.902–1.765) 1.227 (0.763–1.972)
1 1.492 (1.125–1.979) 120 (10.1; 8.4–11.9) 152 (12.7; 10.9–14.8) 1 1.644 (1.238–2.184)
776 (65.1; 62.3–67.7)
381 (31.9; 29.3–34.6) 392 (32.9; 30.2–35.6)
1 1.274 (0.990–1.640)
673 (56.4; 53.6–59.2)
343 (28.8; 26.2–31.4) 326 (27.3; 24.8–29.9)
1 1.012 (0.795–1.287)
273 (22.9; 20.5–25.3)
Multivariate odds ratioa (95% CI) n (%; 95% CI) Multivariate odds ratioa (95% CI) n (%; 95% CI) Multivariate odds ratioa (95% CI) Multivariate odds ratioa (95% CI) n (%; 95% CI)
Reported “never heard ‘breast cancer’ before”
Table 4. Knowledge and attitudes toward breast cancer
n (%; 95% CI)
Reported having breast self-examination skills
Reported a breast self-examination in the last 3 years
Reported breast exam by a health worker in the last 3 years
According to the KAP survey results, 25.7% (95% CI: 23.3%–28.3%) and 22.1% (95% CI: 19.6%–24.4%) of participants indicated that they knew “nothing at all” regarding breast and cervical cancers, respectively. A lack of awareness of both cancers was associated with participants who were less-educated, unemployed or retired, and who lived in a rural area. These trends are consistent with those found in the nearby Sichuan Province of China, where women who lived in a rural area and were less educated and unemployed also were less knowledgeable of breast cancer and screening . The results may be attributed, in part, to the unequal geographic distribution of poverty in Mongolia, with 43% of rural populations being impoverished as opposed to 30% in urban settings . Disadvantaged communities in suburban and rural areas often lack access to social services and adequate information. Additionally, consistent provision of health education and services in rural regions is generally more difficult than in urban settings due to the migration of nomadic populations and sparse population density . Factors that may explain the discrepancy between the number of participants who self-rated their knowledge of breast cancer as “nothing” and the number who correctly answered that early detection of breast cancer improves survival are subjectivity and responder bias. The participants may have significantly overstated their ignorance, potentially because of a lackof confidence in their knowledge. Moreover, the participants may have used logic and reasoning rather than explicit education on breast cancer to deduce the significance of early detection. For example, participants’ awareness of breast cancer specifically may be low, but they may generally understand that early detection for any illness may improve survival. This is a topic for further qualitative research. While the majority of participants correctly answered that early detection of breast cancer improves survival and identified BSE as an early detection method, only 64.8% reported having the ability to perform a BSE.The higher odds of having BSE skills among participants older than 50 years are consistent with the higher risk for breast cancer in this age group.Yet almost half of the participants stated that they were not concerned that breast (49.3%; 95% CI: 46.4%–52.2%) and cervical (45.7%; 95% CI: 43.2%–48.9%) cancers could affect them or their families. This apparent inconsistency between knowledge of the disease and participation in screening may again be attributed, in part,to the use of reasoning versus explicit breast cancer education, as well as bias toward optimism regarding own personal risk. Despite breast cancer education, women may perceive their own risk to be lower than that of others .This bias may contribute to the
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Yerramilli, Dugee, Enkhtuya et al.
Table 5. Knowledge and attitudes toward cervical cancer Reported “never heard of ’cervical cancer’ before” Demographic Total (N 5 1,193) Urbanicity (n) Urban (604) Rural (589) Age group, years (n) 30–39 (384) 40–49 (354) 50–59 (323) $60 (132) Education level (n) Primary or less (73) Secondary (838) Tertiary (282) Education (n) Homemaker/retired (418) Unemployed (167) Employed (608)
Reported having a Papanicolaou test in the last 3 years
n (%; 95% CI)
MORa (95% CI)
n (%; 95% CI)
MORa (95% CI)
263 (22.1; 19.8–24.5) 100 (8.4; 6.9–10.1) 161 (13.5; 11.6–15.6)
1 1.792 (1.327–2.420)
415 (34.8; 32.1–37.5) 214 (17.9; 15.9–20.2) 200 (16.8; 14.7–19.0)
1 0.990 (0.770–1.272)
1 0.818 (0.565–1.183) 0.462 (0.300–0.712) 0.679 (0.391–1.180)
128 (10.7; 9.1–12.6) 144 (12.1; 10.4–14.1) 108 (9.1; 7.5–10.8) 34 (2.9; 2.0–4.0)
1 1.347 (0.991–1.832) 1.247 (0.878–1.769) 1.060 (0.629–1.787)
36 (3.0; 2.2–4.2) 198 (16.6; 14.6–18.8) 27 (2.3; 1.5–3.3)
1 0.390 (0.230–0.660) 0.163 (0.084–0.315)
9 (0.8; 0.4–1.0) 287 (24.1; 21.7–26.6) 118 (9.9; 8.3–11.7)
1 3.167 (1.522–6.590) 4.163 (1.927–8.991)
117 (9.8; 8.2–11.6) 50 (4.2; 3.2–5.5) 94 (7.9; 6.4–9.6)
1 0.815 (0.511–1.302) 0.413 (0.276–0.617)
118 (9.9; 8.3–11.7) 54 (4.5; 3.5–5.9) 242 (20.3; 18.1–22.7)
1 1.237 (0.796–1.922) 1.527 (1.088–2.144)
85 (7.1; 5.8–8.7) 74 (6.2; 4.9–7.7) 62 (5.2; 4.0–6.6) 40 (3.4; 2.4–4.5)
Abbreviations: CI, confidence interval; MOR, multivariate odds ratio. a MOR adjusted for urbanicity, age, education, and employment.
Table 6. Reasons women gave for not having a Papanicolaou test Reason
% (95% CI) (N 5 1,193)
I don’t have time I didn’t know I needed to It’s expensive I don’t know where to go It’s embarrassing Other
114 478 18 108 12 88
9.6 (8.0–11.4) 40.0 (37.3–42.9) 1.5 (0.9–2.4) 9.1 (7.5–10.8) 1.0 (0.6–1.8) 7.4 (6.0–9.0)
Abbreviation: CI, confidence interval.
participants of the 2010 KAP survey did not seek Pap smears was that they were unaware that they required the test at all. This confusion may be associated with the simultaneous design and implementation of screening programs using Pap smears and visual inspection with acetic acid (VIA), with guidelines for the latter method developed for the primary care level . The delivery of Pap smears also requires capacity building, including standardized training of cytologists. In Mongolia, the shortage of cytologists delays Papanicolaou test results, often deterring patients from seeking the test . These infrastructural difficulties may be linked with the respondents’ response that they either did not have time for the test (9.6%; 95% CI: 8.0%–11.4%) or did not know where to access the service (9.05%; 95% CI: 7.5%–10.8%). Such health systems challenges raise the question of whether screening through Papanicolaou test delivery is most appropriate in resourcelimited settings such as Mongolia, or whether less resourceintensive alternatives such as HPV DNA or VIA should entirely ©AlphaMed Press 2015
trends found in the 2009 STEP survey. Namely, roughly one-third of women surveyed had conducted a BSE and 3.2% of respondents received a CBE (confidence intervals not published) . Furthermore, only 11.4% underwent Papanicolaou test testing . The KAP results indicating that higher educated women were more likely to have undergone a BSE, CBE, or Pap smears suggest that general education and literacy may help some women fully understand and translate public health messages into individual action or behavioral change. Indeed, KAP surveys in such resource-constrained settings as Wuhan, China, suggest that personalized and targeted breast cancer education significantly improves awareness and accurate practice of BSE . Although the higher odds of CBE among rural participants may appear counterintuitive, this trend may be associated with demographic shifts and the maldistribution of health-care facilities. Namely, the decrease in the percentage of the population in rural regions from 43% to 30% over 10 years has not resulted in a corresponding drop in the number of rural health-care facilities. Hence, the number of primary care physicians per 1,000 people is higher in rural regions than Ulaanbaatar . These trends may have reduced the accessibility of primary health care, including CBE, in urban regions and particularly in poorer urban regions . The relatively high unawareness ofcervical cancer prevention may be partly due to the fact that programs for primary and secondary prevention of these cancers are in initial stages of development and implementation. Through the Millennium Challenge Corporation’s Health Project in Mongolia (2007–2013), national screening programs for noncommunicable diseases, including hypertension, diabetes, and breast and cervical cancers, were implemented . The most common reason for why
replace or be combined with cytology-based screening for higher cost-effectiveness. Research in China suggests that combined Papanicolaou test testing alongside HPV DNA testing at 5-year intervals may be the most cost-effective . Consistent delivery of the most cost-effective option may improve behaviors with regard to cervical cancer screening. Moreover, at the time of the KAP survey, the HPV vaccine had not yet been incorporated into the routine immunization schedule. As of January 2013,the vaccine had only been piloted in two Mongolian provinces . This incomplete rollout may be a source of the participants’ unfamiliarity with cervical cancer as a vaccine-preventable disease.
Limitations of Research This KAP survey was devised to accompany the findings of the STEPs surveys and enhance and facilitate data interpretation and policy design. Hence, the KAP survey is not intended to function alone, as knowledge has a limited impact on health behaviors . In this paper, data, analyses and conclusions from the distinct surveys were compared. However, regression analyses were not conducted on data combined from both surveys, as the sample populations differed. Quality assurance processes were included in the training of interviewers, sampling methods, and determination of sampling size, to minimize selection bias . Recall bias and response bias may have impacted results, particularly with regard to health-care use. Questions were developed and interviewers were trained to minimize social desirability bias related to health, health knowledge, and health behaviors. However, this bias still likely affected the data and may minimize the true gaps in health knowledge and awareness. Additional qualitative research may elucidate the discrepancies in knowledge and attitudes in more detail, as well as the relative impacts ofoptimism bias, inference, and explicit health education on health literacy. One weakness of the KAP survey as administered is the use of the term breast self-examination, which was accepted nomenclature and the metric at the time of the study. However, such terms as breast health awareness are now favored over BSE, due to uncertainties in the clinical effectiveness of the procedure . These uncertainties arise from large-scale randomizedcontrolled trials in China and India, which suggested that BSEs do not reduce breast cancer mortality [22, 23]. A study in the U.S. further indicated that women who performed BSE were more likely to undergo diagnostic mammograms with no improvement of tumor size and stage . Breast health awareness emphasizes education regarding breast cancer symptoms, appropriate medical planning for symptomatic and asymptomatic women, and familiarity with one’s own breasts and body to identify changes [25, 26]. Nonetheless, the insights gained from the analysis of KAP regarding BSE may be useful in informing design of breast health education and awareness interventions to maximize uptake and impact.
CONCLUSION The results of this KAP survey suggest a low level of health literacy in the Mongolian female population regarding breast and cervical cancer, and this is particularly evident among
Breast and Cervical Cancers KAP Survey in Mongolia lower educated, rural, and unemployed populations. Thus, cancer control efforts, especially in marginalized populations of Mongolia, should focus on improving health education among lower educated, rural, and unemployed populations, as well as improving the supply of higher-quality services. A greater emphasis on individual risk for disease in publichealth-education materials regarding breast and cervical cancers may improve outcomes. Health education about vaccinations and cervical cancer, accompanying the national rollout of the HPV vaccine and cervical cancer screening, may also improve uptake. Opportunities exist to apply a diagonal approach, which aims to synergize and integrate disease-specific interventions with strategic health-system strengthening to achieve better results. Awareness and health education for women’s cancers can be integrated into reproductive and maternal health programs that have broad population coverage [27, 28], particularly given the attention and resources devoted to reproductive health programs in Mongolia . Furthermore, health infrastructure should be strengthened to reflect recent and rapid rural-to-urban migration. While the results indicate that respondents were generally aware that early detection improves clinical outcomes, a significant proportion of Mongolian women do not engage in breast cancer screening or in cervical cancer prevention and screening. This should be a focus for future research that should investigate specific methods to address the lack of uptake of services and barriers to accessing care, including the knowledge, attitudes, and practices of primary care personnel . The recommendations derived from this study can be particularly relevant now, following the completion in 2013 of the MCC’s Mongolia Health Project, which provided financial, infrastructural, and administrative support for NCD screening . The insights gained from this KAP survey highlight the importance of identifying obstacles to care seeking as part of the evaluation and strengthening of public health programs, such as the cervical cancer screening initiative currently underway in Mongolia . The results of this study also highlight the importance of the design of public health messaging with regard to individualized risk, including the significant differences between rural and urban populations. Successful cancer control programming requires knowledge and planning around both supply-related factors (service provision) and demand-related factors (patient engagement and uptake). Ignoring beliefs, attitudes, and practices that are often specific to particular population groups and regions can significantly impair programs for early detection of women’s cancers and should be factored into the development and deployment health interventions. Incorporating evidence on beliefs and practices into Mongolia’s process of expanding access to NCD screening will help guarantee better uptake of and more effective programs.
ACKNOWLEDGMENTS This research was completed at the Public Health Institute, Ministry of Health of Mongolia, and funded by the Millennium Challenge Account—Mongolia. During the writing of this article, Felicia M. Knaul was affiliated with the Harvard Medical School and the Harvard Global Equity Initiative, but is now affiliated with the Miller School of Medicine, University of Miami, Miami, USA.
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Yerramilli, Dugee, Enkhtuya et al.
1273 Final approval of manuscript: Pooja Yerramilli, Otgonduya Dugee, Palam Enkhtuya, Felicia M. Knaul, Alessandro R. Demaio
AUTHOR CONTRIBUTIONS Conception/Design: Otgonduya Dugee, Palam Enkhtuya, Alessandro R. Demaio Collection and/or assembly of data: Otgonduya Dugee, Palam Enkhtuya, Alessandro R. Demaio Data analysis and interpretation: Pooja Yerramilli, Otgonduya Dugee, Alessandro R. Demaio Manuscript writing: Pooja Yerramilli, Palam Enkhtuya, Felicia M. Knaul, Alessandro R. Demaio
DISCLOSURES Felicia M. Knaul: GlaxoSmith Kline, Avon Mexico, Pfizer Inc., Chinoin Pharmaceutical Products, Nadro, Sanofi, Roche (RF). The other authors indicated no financial relationships. (C/A) Consulting/advisory relationship; (RF) Research funding; (E) Employment; (ET) Expert testimony; (H) Honoraria received; (OI) Ownership interests; (IP) Intellectual property rights/ inventor/patent holder; (SAB) Scientific advisory board
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