Prevalence and Risk Factors for Patient Delay Among Women With Breast Cancer in Rural India

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1 620630APHXXX / Asia-Pacific Journal of Public HealthGangane et al research-article2015 Original Article Prevalence and Risk Factors for Patient Delay Among Women With Breast Cancer in Rural India Asia-Pacific Journal of Public Health 2016, Vol. 28(1) APJPH Reprints and permissions: sagepub.com/journalspermissions.nav DOI: / aph.sagepub.com Nitin Gangane, MD, DNB 1, Anshu, MD, DNB 1, Shiva Manvatkar 1, Nawi Ng, MD, MPH 2, Anna-Karin Hurtig, MD, PhD 2, and Miguel San Sebastián, MD, PhD 2 Abstract Delay in seeking health care by women with breast cancer increases mortality risk. This study was conducted in rural India to identify risk factors associated with patient delay. A total of 212 women with primary breast cancer diagnosed between 2010 and 2012 were interviewed. Sociodemographic characteristics, time interval between seeking medical attention and appearance of symptoms, and reasons for delay were inquired. Patient delay was defined as more than 3 months between date of first symptoms and medical consultation. Logistic regression was applied to assess associations between potential risk factors and patient delay. Almost half the women with breast cancer experienced patient delay. Age more than 60 years (odds ratio = 4.9, 95% confidence interval = ) was significantly associated with patient delay. Only 6.6% of patients had heard about breast self-examination. Significantly higher number of patients with delay presented with advanced clinical stage (P =.000). Health education programs should be introduced with specific strategies to shorten patient delay. Keywords breast cancer, patient delay, screening, rural India Introduction Breast cancer is one of the most common causes of death among women worldwide, accounting for 522,000 deaths every year. 1 In India, breast cancer has overtaken cervical cancer as the most common cancer among women. Of the 26 population-based cancer registries in India, 15 have reported breast as the leading site of cancer in The National Cancer Registry Programme also runs hospital-based cancer registries in major Indian cities that have diagnostic and treatment facilities for cancer. The latest consolidated report of the 7 hospitals in this network reported 1 Mahatma Gandhi Institute of Medical Sciences, Sevagram, Wardha, India 2 Umeå University, Umeå, Sweden Corresponding Author: Nitin Gangane, Department of Pathology, Mahatma Gandhi Institute of Medical Sciences, Sevagram, Wardha, , India. nitingangane@rediffmail.com

2 Gangane et al 73 breast as the leading site of cancer, in Mumbai, Thiruvananthapuram, and Dibrugarh from 2007 to The hospital registries from Bengaluru, Chennai, Guwahati, and Chandigarh still report cervical cancer at the top of their lists. There are several gaps in the evidence base around noncommunicable diseases, especially cancer, in the Asia-Pacific region that need further investigation. 4 Delayed presentation of patients with breast cancer is a problem in both, high- and low- and middle-income countries (LMICs). Early diagnosis and treatment are the main strategies for improved survival outcomes for breast cancer patients. The Surveillance, Epidemiology and End Results (SEER) program of the National Cancer Institute in the United States reported that in 2010, the 5-year relative survival for breast cancer in American women of all races was 99% for localized disease, 85% for regional disease, and 25% for distant-stage disease. 5 Any delay by patients in reporting to health facilities for either diagnosis or treatment of breast cancer is likely to result in disease progression to a later stage, which will ultimately affect prognosis of the disease. Delay can also occur at health facilities in establishing diagnosis and providing treatment. However, this type of delay is not the focus of the present study. Several high-income countries have organized breast cancer screening programs. 6-8 However, middle-income countries like India lack similar functioning organized screening programs. Only a small percentage of Indian women are screen-detected and most patients report to health facilities only after they notice the appearance of late-stage symptoms. Furthermore, accessibility to health facilities varies across different states in India. Evidence shows that women who wait more than 3 months after their first symptoms appear before attending a medical consultation have significantly lower survival rates compared with women who seek medical attention promptly. 9 Therefore, 3 months was used as the cutoff point to define patient delay in this study. The proportion of patient delay among women with breast cancer is between 8% to 18% in high-income countries This proportion is higher in the LMICs ranging from 11% in Thailand, 13 20% in Colombia, 14 25% in Egypt, 15 to 82% in Nigeria. 16 Causes of patient delay reported in these studies included lack of education, 16 old age, 10,14 benign breast disease, 10 poor knowledge of breast cancer symptoms, 12 low family income, 13 lack of social security, 14 and being unmarried. 16 More advanced stage of the disease resulting from patient delay has been significantly identified in most studies. 10,13,14,17 In a study in Delhi, India, Pakseresht et al 17 reported a patient delay of 11 months among women with breast cancer, and old age was identified as the main factor associated with the delay. Data of patients delay in rural India is however limited and scarce. It is pertinent to explore the underlying causes that lead to patient delay in seeking medical attention in Indian women, particularly those who live in underserved rural areas. The availability of data from the National Cancer Registry Programme can provide evidence to design and implement measures to improve early detection of breast cancer. This study was conducted in a tertiary care hospital in rural central India to examine the extent of diagnosis delay among breast cancer patients and to identify the underlying risk factors associated with the delay. Material and Methods Study Setting This study was conducted at Kasturba Hospital, which is attached to the Mahatma Gandhi Institute of Medical Sciences (MGIMS) in Wardha district, Maharashtra state. The hospital caters to patients from Wardha district and adjacent districts, as well as from neighboring states. The hospital has tertiary care services for cancer diagnosis and treatment, including surgery, radiotherapy, and chemotherapy.

3 74 Asia-Pacific Journal of Public Health 28(1) A population-based cancer registry (PBCR) was started in the Department of Pathology at MGIMS in February The registry covers an estimated population of 1.2 million people from Wardha district based on the 2011 census estimates. 18 The registry data showed that breast cancer was the most common cancer among women in Wardha district in , accounting for 27% of all the cancers in women with an age-adjusted rate of 19.8 cases per population. 19 Study Participants A total of 384 cases of primary breast cancer were diagnosed at Kasturba Hospital in of which 3 were male. We included only women who were (a) diagnosed with infiltrating carcinoma of the breast, (b) willing to participate in the study, and (c) able to respond in person to the study questionnaire. Of the 381 women with breast cancer, 73 women had already died in Seventy-six women could not be contacted and personally interviewed because they lived in isolated locations and 14 women were lost to follow-up. Three women did not agree to participate in the study. Two cases of primary breast sarcoma and one of lymphoma of the breast were excluded from the study. Finally, 212 women consented to be personally interviewed in this study. Of them, 156 lived in Wardha district and 56 came from districts outside Wardha and adjoining states. All the 212 participating women were diagnosed with breast cancer after self-reporting to health care facilities. None of them were screen-detected cases. Instrument Design The semistructured questionnaire in this study included 25 questions on 4 different sections. The first section included the sociodemographic characteristics of the participants such as age, religion, education, occupation, marital status, and income. The second collected information on their access to health care facilities at primary and tertiary level. The third section collected data about past history of breast disease, family history of breast cancer, or any other cancers. The questionnaire also included questions on participants awareness of breast cancer and their knowledge of breast self-examination. In the fourth section, 8 questions about the appearance of symptoms and time interval of seeking medical attention after noticing the first symptoms of breast cancer were asked. Open-ended questions were asked about the causes of delay, if any, in obtaining a diagnosis. The questionnaire was pilot-tested among 10 women with breast cancer in Kasturba Hospital, and as no significant changes were made in the final questionnaire, we included these women in the data analysis. Patient Recruitment and Interview Procedures Patients contact information was procured from the records of the hospital information system and cancer registry. If phone numbers were available, patients were contacted by social workers over the telephone, informed about the study and the date and time of the interview was mutually agreed upon. Social workers traveled to the residence of the patients and conducted personal interviews with the participants. In addition, patients who came for follow-up visits to the surgery outpatient department for radiotherapy or chemotherapy sessions were enrolled and interviewed by social workers in the premises of Kasturba Hospital ensuring privacy of the participants and confidentiality of the interview. A face-to-face interview was conducted by 2 female trained social workers using the semistructured questionnaire. Women were asked to recall the date, month, and year when they first perceived symptoms of breast cancer as abnormal. The date of the first medical consultation for symptoms of breast cancer was also enquired. To obtain a better accuracy, these dates were linked

4 Gangane et al 75 to family occasions or popular religious festivals if possible. The time interval between the appearance of the first symptom and the first medical consultation was calculated in weeks and months. All dates were subsequently reconfirmed from patients clinical records. Patient delay in this study was defined as more than 3 months between the date of appearance of the first symptoms and the date of initial consultation with a health worker or a doctor. 9 Reasons for delay in seeking diagnosis or treatment were first obtained by asking open-ended questions to the patient. Patients gave one or more reasons to this question. These answers were later recoded into major categories which were reconfirmed with the patients using close ended questions. The clinical stage of the disease was available for 202 of the 212 participants. Patients were divided into four groups based on the TNM staging system for malignant tumors. 20 Because of the low number of patients in categories 2 and 4, stages 1 and 2 were combined as an early stage category and stages 3 and 4 as an advanced stage category. Statistical Analysis All variables were treated as categorical. The associations between these categorical variables and diagnosis delay among breast cancer patients were assessed using chi-square tests. All significant variables (at P <.25) were included in subsequent multivariable logistic regression to estimate the adjusted odds ratios of factors associated with patient delay. All statistical analyses were performed using the STATA software version Ethics The study protocol was approved by the Institutional Ethics Committee of Mahatma Gandhi Institute of Medical Sciences, Sevagram in All interviews were conducted after obtaining the written informed consent of the patients. Results Of the 212 women with breast cancer who participated in this study, 103 (48.5%) experienced a delay of more than 3 months between the appearance of the first symptoms and the time of first reporting to the health services. The range of time lag between appearance of symptoms and first consultation extended from 0 to 150 weeks with a mean of 8 months. Among women with diagnosis delay, the mean time lag was 63.8 ± 62.0 weeks (median = 31 weeks), and the corresponding numbers were 5.4 ± 3.7 weeks (median = 5 weeks) among women with no diagnosis delay. Table 1 outlines the sociodemographic characteristics of the delay and nondelay subgroups. The majority of the women in this study were younger than 50 years, identified Hindu as religion, were housewives, or casual workers, had low education level, were married, had previous history of breast disease, were unaware about breast cancer and breast self-examination, and were at later stage of the breast cancer. The bivariate analysis showed that age at diagnosis was significantly associated with patient delay. Patients aged younger than 40 years experienced lesser delays in seeking medical consultation compared with patients older than 60 years. Similarly, the difference in delay was found to be significant (P <.25) among patients according to religion, education, previous history of breast disease, cost of travel to primary health center (PHC), cost of travel to tertiary care hospital, and enough money to access health care. No differences in delay were found among patients according to occupation, marital status, income groups, family history of cancer, awareness of breast cancer as a disease, and awareness of breast self-examination (P >.25). More important, it was also observed that only 18.4% of all patients (n = 39) were aware of breast cancer as a disease and only

5 76 Asia-Pacific Journal of Public Health 28(1) Table 1. Sociodemographic Characteristics, Clinical Stage at Initial Presentation, and Access to Health Care of Study Subjects According to Patient Delay. n (%) (N = 212) Delay <3 Months (n = 109); n (%) Delay >3 Months (n = 103); n (%) P Age in years at diagnosis (21.7) 30 (27.5) 16 (15.5) (36.8) 37 (33.9) 41 (39.8) (25.0) 32 (29.4) 21 (20.4) >60 35 (16.5) 10 (9.2) 25 (24.3).005 Religion Hindu 169(79.7) 83(76.1) 86(83.5) Others 43 (20.3) 26(23.8) 17 (16.5).184 Occupation Manual workers 72 (33.9) 37 (33.9) 35 (33.9) Housewives/casual workers 132(62.3) 68 (62.4) 64 (62.1) Industrial/office workers 8 (03.8) 4 (3.7) 4 (3.8).997 Education Higher secondary and above 46(21.7) 28 (25.7) 18 (17.5) Below higher secondary (can read and 116 (54.7) 62 (56.9) 54 (52.4) write) Illiterate 50 (23.6) 19 (17.4) 31 (30.1).066 Marital status Married 178(83.9) 95 (87.2) 83 (80.6) Divorced/widowed 30 (14.1) 12 (11.0) 18 (17.5) Unmarried 4 (1.9) 2 (1.8) 2(1.9).398 Average monthly family income (Indian rupees, INR) < (47.2) 49 (44.9) 51 (49.5) (41.5) 45 (41.3) 43 (41.7) > (11.3) 15 (13.8) 9 (8.7).492 Previous history of breast disease Yes 166 (78.3) 89 (81.6) 77 (74.8) No 41 (19.3) 19 (17.4) 22 (21.4) More than once 5 (2.3) 1 (0.9) 4 (3.9).257 Family history of breast cancer Yes 17 (8.0) 8 (7.3) 9 (8.7) No 195 (91.9) 101 (92.7) 94 (91.3).708 Family history of cancer Yes 28 (13.2) 16 (14.7) 12 (11.6) No 184 (86.8) 93 (85.3) 91 (88.3).515 Awareness of breast cancer as a disease Yes 39 (18.4) 22 (20.2) 17 (16.5) No 173 (81.6) 87 (79.8) 86 (83.5).490 Awareness of breast self-examination Yes 14 (6.6) 8(7.3) 6 (5.8) No 198 (93.4) 101 (92.7) 97 (94.2).657 Clinical stage Stage 1 7 (3.1) 6 (5.9) 1 (1.0) Stage 2 73 (36.1) 49 (48.0) 24 (24.0) Stage 3 107(52.9) 40 (39.2) 67 (67.0) Stage 4 15 (7.4) 7 (6.9) 8 (8.0).000 (continued)

6 Gangane et al 77 Table 1. (continued) n (%) (N = 212) Delay <3 Months (n = 109); n (%) Delay >3 Months (n = 103); n (%) P Distance in kilometers from residence to primary health center (77.4) 83 (76.2) 81 (78.6) (17.9) 22 (20.2) 16 (15.5) (4.7) 4 (3.7) 6 (5.8).548 Cost of travel to primary health center in Indian rupees, INR (47.6) 42 (38.5) 59 (57.3) (52.4) 67 (61.5) 44 (42.7) Distance in kilometers from residence to tertiary care hospital (26.4) 28 (25.7) 28 (27.2) (69.3) 76 (69.7) 71 (68.9) (4.3) 5 (4.6) 4 (3.9).946 Cost of travel to tertiary care hospital in Indian rupees, INR (49.5) 49 (45.0) 56 (54.4) (50.5) 60 (55.1) 47 (45.6).171 Do you think you have enough money to access health care? Yes 95 (44.8) 54 (49.5) 41 (39.8) No 90 (42.5) 45 (41.3) 45 (43.7) Don t know 27(12.7) 10 (9.2) 17 (16.5).180 Who did you first consult on discovering the initial symptoms? Private practitioner (allopathic medicine) 155 (73.1) 77 (70.6) 78 (75.7) Government-run primary health center 25 (11.8) 14 (12.8) 11 (10.7) Others (alternative medicine) 32 (15.1) 18 (16.5) 14 (13.6) % of all patients (n = 14) had heard about breast self-examination. No differences for these factors were found between the delay and nondelay subgroups. The majority of patients (n = 155, 73.1%) first sought medical advice from private practitioners rather than from the government-run PHCs (n = 25, 11.8%). Some patients (n = 32, 15.1%) sought advice from practitioners of alternative medicine other than allopathic medicine (Table 1). However, this difference in health care seeking patterns was not statistically significant between patients with and without delay. Table 2 shows the initial symptoms experienced by patients with breast cancer before they sought medical help. Patients often presented with more than one symptom. The commonest clinical symptom was the presence of a painless mass in the breast (92.4%). A small proportion of women (4.7%) noticed a lump under their armpits, while 2.8% of women presented with painful breast lumps. 3.3% of women had complaints of nipple discharge, and the same percentage noticed change in shape of their breasts. Only 2.3% women complained of redness or swelling over the skin of the breast. However there was no significant difference between women with and without delay in seeking medical consultation in relation to initial presenting symptoms. Details of the clinical stage of the disease were available for 202 (95.2%) of the 212 patients. When we initially analyzed clinical stage against patient delay, we found that the odds ratio (OR) for stage 2 was 2.9 (95% CI = ). For stage 3, OR was 10.1 (95% CI = ), while it was 6.9 (95% CI = ) for stage 4. However, as the number of patients in stage 1 and 4 were small, we clubbed patients with stage 1 and 2 as early clinical stage; and stages 3 and 4 as late stage. The odds of late stage clinical disease were almost 3.5 times (95% CI = ) more with patient delay of more than 3 months as compared with early-stage disease. Thus significantly higher number of patients with delay presented had advanced clinical stage of the disease (P =.000).

7 78 Asia-Pacific Journal of Public Health 28(1) Table 2. Symptoms Experienced by Patients of Breast Cancer Related to Delay in Seeking Medical Advice. n (%) (N = 212) Delay <3 Months (n = 109): n (%) Delay >3 Months (n = 103); n (%) P Painless mass in breast 196 (92.4) 96 (88.1) 100 (97.1).38 Lump under armpit 10 (4.7) 3 (2.7) 7 (6.8) Change in breast shape 7 (3.3) 3 (2.7) 4 (3.9) Nipple discharge 7 (3.3) 3 (2.7) 4 (3.9) Painful mass in breast 6 (2.8) 2 (1.8) 4 (3.9) Redness/swelling over breast 5 (2.3) 2 (1.8) 3 (2.9) Pain in arm or back 4 (1.8) 4 (3.7) 0 (0) Ulcer over breast 1 (0.4) 1 (0.9) 0 (0) Weakness 1 (0.4) 0 (0) 1 (0.9) Note: Patients often presented with more than one symptom. So column totals will not add up to 100%. On analysis of the different reasons for delay in seeking medical attention stated by patients (n = 103), the commonest reason was found to be was the painlessness of the breast lump (n = 63, 61.2%). Other reasons for ignoring the breast lump included poor financial situation impeding ability to bear hospital costs (n = 18, 17.5%), the lack of disease awareness (n = 13, 12.6%), family priorities coming before health (n = 7, 6.8%), the fear and anxiety of being detected with cancer (n = 11, 10.7%), and fear of mutilating treatment (n = 2, 1.9%). One patient thought that it was a milk nodule and another attributed it to trauma. Three patients had used some other alternative therapies. Factors at P value of <.25 in the bivariate analysis were included in a multivariable logistic regression analysis (Table 3). The significant factors which were found to be associated with patient delay were age of the patient >40 years and cost of travel to the PHC. Similarly, patients older than 60 years had 5 times higher odds to experience delay when compared with those younger than 40 years. Higher cost of travel had a positive impact on access to care and those who had to spend more (Indian rupees [INR] 11-60) on traveling to a PHC had significantly lesser odds of delay than those who had to spend INR 1 to 10. The bivariate association between illiteracy and delay was significant, but the significance disappeared when the results were adjusted to other variables. Previous history of breast disease had very high odds of associating with delay but was again not statistically significant. Discussion One of the causes of late stage detection of breast cancer is patient delay in accessing health care facilities. Almost half (48.3%) of the patients in our study reported a delay of more than 3 months in seeking medical advice since they first experienced symptoms of breast cancer. This pattern seems to be relatively common in India and other authors have reported similar observations. About 54% of women with breast cancer in Thiruvananthapuram, which lies in the southernmost part of India, reported patient delay of more than 3 months, 22 while the corresponding number was 57% in Delhi. 16 Other hospital-based studies from low and middle-income countries have shown a lower prevalence of patient delay of more than 3 months compared to our study, except a study from Nigeria, which reported delay in 82% of patients. 16 Another study from north Pakistan found that 39% of their patients presented after a delay of more than 3 months 23 while in Thailand only 10.6% of women reported delay. 13 Patient delays of 25% and 20.3% have been reported in studies from Egypt 15 and Colombia, 14 respectively.

8 Gangane et al 79 Table 3. Factors Related to Patient Delay in Breast Cancer Patients: Logistic Regression Analysis With Crude and Adjusted Odds Ratios (ORs) and Their 95% CIs (N = 212). Factors Crude OR (95% CI) Adjusted OR (95% CI) Age, years ( ) 2.2 ( ) ( ) 1.7 ( ) > ( ) 4.9 ( ) Religion Hindu 1 1 Others 0.6 ( ) 0.5 ( ) Education Higher secondary and above 1 1 Below higher secondary (can read and write) 1.3 ( ) 2.2 ( ) Illiterate 2.5 ( ) 2.7 ( ) Previous history of breast disease Yes 1 1 No 1.3 ( ) 1.5 ( ) More than once 4.6 ( ) 8.2 ( ) Cost of travel to primary health center in Indian rupees (INR) ( ) 0.4 ( ) Cost of travel to tertiary care hospital in INR ( ) 0.6 ( ) Enough money to access health care Yes 1 1 No 1.3 ( ) 0.8 (0.3-2) Don t know 2.2 ( ) 0.7 ( ) Studies from high-income countries with organized screening programs report even lower percentages. In a study of early-stage breast cancer patients in the United States, about 26.4% of African Americans and 17.5% of white patients experienced more than 3 months patient delay. 24 In England, delay was observed only among 8.4% of breast cancer patients. 25 High breast cancer mortality rates in LMICs are largely attributable to disease presentation in late stages. This leads to poor survival outcomes when combined with limited capacity for proper diagnosis and therapy. 26 About 50% to 70% of breast cancer patients in India present with locally advanced or metastatic disease at the time of diagnosis. 27 In our study, we also observed that almost 60% of those patients with delay in seeking medical attention presented with advanced clinical stage of disease. The only sociodemographic factor that was associated with patient delay in our study, was older age at the time of diagnosis. Our study shows that women older than 60 years tended to postpone medical consultation 5 times more than younger women. A systematic review found strong evidence for increased risk of delay being associated with older age. 9 Similar findings have been reported from several countries where older women tended to procrastinate for longer durations 10,14,17 as they attributed these symptoms to aging or comorbid conditions. Older patients also tend to overlook and/or neglect lesions in the breast, these tumors are usually found first by physicians; this underlies the important role of primary care physicians in detection of breast cancer in the elderly. 28

9 80 Asia-Pacific Journal of Public Health 28(1) Access to health care has financial implications and the cultural context is completely different in India. Women older than 60 years in India live with their children, and are often dependent on their children and families financially and for being escorted to hospitals. The impact of these factors on delayed access to medical consultations has not been studied and needs to be explored further. One important aspect, which has not been frequently studied, is the impact of distance and cost of travel to primary and tertiary care health care facilities on patient delay. We observed that the distance from the patient s residence to the PHC or tertiary care hospital was not a significant factor associated with patient delay in seeking medical attention. However, surprisingly, as the cost of travel to the PHC increased, delay in seeking medical attention decreased significantly. One possible explanation for this finding could be that rural patients traveled longer distances and paid more in order to reach a recognized health facility only when they considered it worthwhile to spend that amount on health. A qualitative study might be necessary to understand the reasons behind this finding. The commonest clinical presentation in our patients was the presence of a painless mass in the breast (92.4%). Patients tend to downplay the significance of this symptom as harmless as it was not debilitating or painful. This usually led to delay in accessing medical consultation. Our findings reinforce the need for cancer control programs to focus on making women breast aware, so that they would seek medical attention even with the appearance of minor symptoms. Most patients (73.1%) in this study first sought medical advice from private practitioners rather than from government-run PHCs. Although the extent of utilization of health care in India varies substantially between states and districts, the private sector accounts for 82% of all outpatient visits with no significant variations across income groups. 29 Despite exploitative and prohibitive prices in the private sector, they are preferred. Longer waiting times, lack of privacy, impersonal approach of physicians, and poor quality of care are often reasons why government hospitals are avoided. 30 The majority of private sector institutions are single-doctor dispensaries with very little infrastructure. These private practitioners do not have access to updated standard protocols for management of cancers and the quality of care they provide is often suboptimal. 29 There is a need to introduce appropriate interventions and update the knowledge and skills of these practitioners in order to provide quality care. The importance of health education and health awareness in this population is reemphasized by our findings that only 18% of women were aware of breast cancer as a disease and only 6.6% had heard about breast self-examination. There is a strong need to focus on education and convey the positive message that breast cancer is treatable. Because of the cost and uncertainty surrounding breast cancer screening, the emphasis should be on prevention. 31 Another approach in breast cancer control program reemphasized from findings in present study could be of preventing delay in reporting leading to down-staging of cancer. A major strength of this study is that all information was collected through personal interviews conducted by local social workers and efforts were made to validate this information from patient records. Recall bias is a known limitation of survey-based studies. We tried to overcome this bias partially by correlating the date of the beginning of the symptoms with religious festivals and important family events. However, we are aware that maybe other biases could be operating. A potential bias in the study could have arisen from the exclusion of the patients who died before this study was conducted or those who were lost to follow-up. The patients who died were probably in more advanced stages of the disease and may also have had difficulties in getting proper treatment because of financial or other reasons. Excluding these cases could possibly have led to underreporting for some of our results. Similarly, we could not contact some patients because they lived in isolated locations and this may have led to underreporting of the problem of travel costs to PHCs.

10 Gangane et al 81 Conclusions Our study found that health-seeking behavior in relation to breast cancer in rural India is a major concern. Older age of patients was the only significant finding associated with patient delay in multivariate analysis. In bivariate analysis, patient delay was significantly associated with advanced stage of disease. Targeted health education is imperative in order to make women, especially in rural areas, breast aware about the significance of painless breast masses. This will reduce patient delay and help in early detection of breast cancer. There is a need to gather similar evidence from different parts of the country to strengthen strategies to shorten patient delay and implement a rigorous national breast cancer screening program. Declaration of Conflicting Interests The author(s) declared no potential conflicts of interest with respect to the research, authorship, and/or publication of this article. Funding The author(s) disclosed receipt of the following financial support for the research, authorship, and/or publication of this article: This work was partly supported by the Umeå Centre for Global Health Research, funded by FAS, the Swedish Council for Working Life and Social Research (Grant no ). References 1. International Agency for Research on Cancer. Globocan Estimated cancer incidence, mortality and prevalence worldwide in Retrieved from aspx. Accessed February 10, National Centre for Disease Informatics and Research. National Cancer Registry Programme: Time Trends in Cancer Incidence Rates Bengaluru, India: Indian Council of Medical Research; National Centre for Disease Informatics and Research. National Cancer Registry Programme: Consolidated Report of Hospital-Based Cancer Registries, Bengaluru, India: Indian Council of Medical Research; Mannava P, Abdullah A, James C, Dodd R, Annear PL. Health systems and non-communicable diseases in the Asia-Pacific region: a review of the published literature. Asia Pac J Public Health. 2015;27:NP1-NP Howlader N, Noone AM, Krapcho M, et al, eds. SEER Cancer Statistics Review, Bethesda, MD: National Cancer Institute. Retrieved from Accessed February 10, US Preventive Service Task Force. Breast cancer screening. org/uspstf/uspsbrca.htm. Accessed February 10, National Health Service. NHS breast screening programme for England. nhs.uk/breastscreen/. Accessed February 10, Canadian Task Force on Preventive Health Care. Screening for breast cancer. ca/ctfphc-guidelines/2011-breast-cancer/. Accessed February 10, Ramirez AJ, Westcombe AM, Burgess CC, Sutton S, Littlejohns P, Richards MA. Factors predicting delayed presentation of symptomatic breast cancer: a systematic review. Lancet. 1999;353: Arndt V, Sturmer T, Stegmaier C, Ziegler H, Dhom G, Brenner H. Patient delay and stage of diagnosis among breast cancer patients in Germany a population based study. Br J Cancer. 2002;86: Forbes LJL, Warburton F, Richards MA, Ramirez AJ. Risk factors for delay in symptomatic presentation: a survey of cancer patients. Br J Cancer. 2014;111: Innos K, Padrik P, Valvere V, et al. Identifying women at risk for delayed presentation of breast cancer: a cross-sectional study in Estonia. BMC Public Health. 2013;13: Poum A, Promthet S, Duffy SW, Parkin DM. Factors associated with delayed diagnosis of breast cancer in northeast Thailand. J Epidemiol. 2014;24:

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