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Global Public Health: An International Journal for Research, Policy and Practice Publication details, including instructions for authors and subscription information: http://www.tandfonline.com/loi/rgph20
Social barriers to diagnosis and treatment of breast cancer in patients presenting at a teaching hospital in Ibadan, Nigeria a
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Liese Pruitt , Tolulope Mumuni , Eugene Raikhel , Adeyinka d
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Ademola , Temidayo Ogundiran , Adeniyi Adenipekun , Imran b
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Morhason-Bello , Oladosu A. Ojengbede & Olufunmilayo I.
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Olopade a
Pritzker School of Medicine, University of Chicago, Chicago, IL, USA b
Centre for Population and Reproductive Health, College of Medicine, University of Ibadan, Ibadan, Nigeria c
Department of Comparative Human Development, University of Chicago, Chicago, IL, USA d
Department of Surgery, College of Medicine, University of Ibadan, Ibadan, Nigeria e
Department of Radiotherapy, College of Medicine, University of Ibadan, Ibadan, Nigeria f
Center for Clinical Cancer Genetics & Global Health, Department of Medicine, University of Chicago, Chicago, IL, USA Published online: 02 Dec 2014.
To cite this article: Liese Pruitt, Tolulope Mumuni, Eugene Raikhel, Adeyinka Ademola, Temidayo Ogundiran, Adeniyi Adenipekun, Imran Morhason-Bello, Oladosu A. Ojengbede & Olufunmilayo I. Olopade (2014): Social barriers to diagnosis and treatment of breast cancer in patients presenting at a teaching hospital in Ibadan, Nigeria, Global Public Health: An International Journal for Research, Policy and Practice, DOI: 10.1080/17441692.2014.974649 To link to this article: http://dx.doi.org/10.1080/17441692.2014.974649
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Global Public Health, 2014 http://dx.doi.org/10.1080/17441692.2014.974649
Social barriers to diagnosis and treatment of breast cancer in patients presenting at a teaching hospital in Ibadan, Nigeria
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Liese Pruitta, Tolulope Mumunib, Eugene Raikhelc, Adeyinka Ademolad, Temidayo Ogundirand, Adeniyi Adenipekune, Imran Morhason-Bellob, Oladosu A. Ojengbedeb* and Olufunmilayo I. Olopadef* a Pritzker School of Medicine, University of Chicago, Chicago, IL, USA; bCentre for Population and Reproductive Health, College of Medicine, University of Ibadan, Ibadan, Nigeria; cDepartment of Comparative Human Development, University of Chicago, Chicago, IL, USA; dDepartment of Surgery, College of Medicine, University of Ibadan, Ibadan, Nigeria; eDepartment of Radiotherapy, College of Medicine, University of Ibadan, Ibadan, Nigeria; fCenter for Clinical Cancer Genetics & Global Health, Department of Medicine, University of Chicago, Chicago, IL, USA
(Received 4 January 2014; accepted 22 September 2014) Globally, breast cancer is the most frequent malignancy in women, and stage at diagnosis is a key determinant of outcome. In low- to middle-income countries, including Nigeria, advanced stage diagnosis and delayed treatment represent a significant problem. That social barriers contribute to delay has been noted in previous research; however, few specific factors have been studied. Using semi-structured interviews, this study identifies social barriers to diagnosis and treatment for patients who presented at University College Hospital Ibadan, Nigeria. Transcripts from the interviews were coded and analysed thematically. Thirty-one patients and five physicians were interviewed. The median age of patients was 51 (range: 28 to above 80), 83% were Christian and 17% were Muslim. Preliminary analysis showed that delays in diagnosis reflected a lack of education as well as the utilisation of nonphysician medical services such as pharmacists. Delays in treatment were often due to fear of unanticipated surgery and cost. The majority of women did not know the cause of their breast cancer, but some believed it was caused by a spiritual affliction. This study suggests that further education and awareness of breast cancer for both patients and providers is needed in order to increase early stage diagnosis. Keywords: breast cancer; Nigeria; qualitative research; social barriers to healthcare; non-communicable diseases
Introduction The cancer burden in low- to middle-income countries (LMIC) is increasing, and the survival rates in LMIC are much poorer than those seen in high-income nations (Farmer et al., 2010). Furthermore, most of the research to understand the social impact of cancer has focused on the USA and Europe (Odigie et al., 2010). In order to address the needs of cancer patients across the globe, we need to understand diverse local behaviours and beliefs related to cancer outside of an American or European context. Breast cancer is the most frequent malignancy affecting women worldwide (Jemal et al., 2011), and the stage of diagnosis is a key determinant of final outcome for breast *Corresponding authors. Emails: [email protected]; [email protected] © 2014 Taylor & Francis
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cancer patients (Richards, Smith, Ramirez, Fentiman, & Rubens, 1999). In the LMIC, delayed treatment seeking and advanced stage diagnosis represent a significant problem (Adesunkanmi, Lawal, Adelusola, & Durosimi, 2006). Breast cancer is the most common cancer affecting women in Nigeria, and delayed presentation has been observed for four decades (Oluwatosin, 2010). Furthermore, the incidence of breast cancer in Nigeria is increasing (Jedy-Agba et al., 2012). Nigeria is the most populous country in Africa with an estimated population of 177 million people. It is a country affected by significant inequality and 70% of the population lives in poverty (Central Intelligence Agency, 2013). The healthcare system in Nigeria is complex and incorporates a wide range of providers including public system employees, private providers, non-governmental and community-based organisations, and religious and traditional care providers. The Nigerian healthcare system is financed by a combination of tax revenue, out-of-pocket payment, donor funding and health insurance. Challenges facing the Nigerian healthcare system include limited institutional capacity, poor health infrastructure, and a corrupt, unstable economic and political context (Olakunde, 2012; Onwujekwe & Uzochukwu, 2005). There are many potential barriers that prevent women from seeking treatment upon first noticing breast cancer symptoms. These include economic and logistical barriers (Anyanwu, Egwuonwu, & Ihekwoaba, 2011), as well as cultural and social factors such as stigma or poor healthcare-seeking behaviours. The effects of these cultural and social barriers have been noted in previous studies; however, the identification of specific factors and the extent of their influence have never been explored in depth (Anyanwu et al. 2011; Ukwenya, Yusufu, Nmadu, Garba, & Ahmed, 2008). Strategies for addressing late stage presentation have been developed previously in the USA. Racial minority groups have higher rates of late stage presentation than Caucasian women, and a range of programmes has been developed to address this issue (Lannin, Mathews, Mitchell, & Swanson, 2002). A review of projects designed to change screening behaviours in minority populations in the USA concluded that the most effective interventions were guided by anthropological study of the target community. Studies structured in this manner were more effective in changing screening rates than those utilising traditional behaviour change indicators (Erwin, Spatz, Stotts, & Hollenberg, 1999; Pasick & Burke, 2008). The importance of a culturally tailored approach in a global context was emphasised in the consensus statement from the Breast Health Global Initiative, which discussed the importance of qualitative inquiry in the design of interventions in order to understand the local attitudes and barriers to care (Harford et al., 2012). The purpose of this study was to use qualitative methods to assess what cultural and social barriers influence delayed breast cancer diagnosis and to understand healthcare-seeking behaviours of women presenting for care at a tertiary hospital in Ibadan, Nigeria.
Methods The study is based on the Nigerian Breast Cancer Study, an on-going case–control study of breast cancer in Ibadan, Southwest Nigeria that has been in the field since 1998 with approval by the institutional review boards of the University of Ibadan and the University of Chicago as previously described (Adebamowo et al., 2003; Huo et al., 2009).
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Research participants Patients were recruited in the radiotherapy and surgery clinics at University College Hospital (UCH), Ibadan, Nigeria in July 2011. All women with a diagnosis of breast cancer were eligible regardless of stage of diagnosis as long as they were 18 years of age or older. Patients from all ethnic groups and language groups were eligible as long as they spoke a common language with the translator available. Physician participants were recruited from the residents in the radiotherapy department.
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Interview procedure When breast cancer patients completed their scheduled treatment, they were informed about the study and offered the opportunity to participate. Patient interviews took place in empty consultation rooms in the clinical setting. All of the interviews were semistructured, so deviation from the interview guide was permitted to ask follow-up questions or pursue topics introduced by the subject. The patient interview guide was based on the McGill Illness Narrative Interview (Groleau, Young, & Kirmayer, 2006) although due to the more focused nature of this research and the time constraints on patients, the scope of the questions was reduced. The interviews focused on how women first found their breast cancer, their healthcare-seeking behaviours, any delays they had experienced in care, beliefs about disease causation, and experiences with stigma. Interviews were conducted with the assistance of a gender and dialect concordant translator who was experienced in public health work and audio-recorded. Physician interviews were conducted in English by LP and audio-recorded. These interviews focused on perceived reasons for delays in care, as well as perception of breast cancer in the community.
Data analysis Audio-recorded interviews conducted in Yoruba were translated and transcribed wordfor-word into English by the translator. Interviews conducted in English were transcribed word-for-word by LP. Each participant was assigned an identification code to protect his or her identity. A thematic analysis was performed and conceptual models of barriers to care were developed (Figures 1 and 2). Data from the interviews were analysed using QSR International’s NVivo 10 software by LP and MT. Both researchers coded every interview and a Cohen’s Kaplan coefficient was calculated for all themes and all interviews, weighted by interview length, with a combined value of 0.78.
Results Demographics Thirty-one female breast cancer patients were recruited from the radiotherapy and surgery outpatient clinics and inpatient wards at UCH. The median age of patients was 51 (range: 28 to -above 80), 83% were Christian and 17% were Muslim. Seven had no formal education and nine had a university or polytechnic degree while the remaining patients had an intermediate educational level. They came from a wide range of towns and cities from across southern Nigeria (Figure 3). Many languages were spoken by participants the most common being Yoruba (n = 18), English (n = 15), Ibo (n = 6) and pidgin (n = 3).
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Figure 1. Conceptual model of healthcare-seeking patterns of women with breast symptoms to diagnosis with breast cancer.
Five resident physicians in the radiotherapy department were interviewed. Three were males and two were females. They ranged in age from 35 to 38 years. Four were Christian and one was Muslim. Barriers to diagnosis Healthcare-seeking behaviours between the initial recognition of symptoms and eventual diagnosis with and treatment for breast cancer were complex (Figures 1 and 2). Delays in diagnosis were often related to complex patterns of healthcare-seeking as well as a lack of awareness that symptoms might be serious (Figure 1). Some patients initially dismissed their symptoms, others sought alternative care and others went directly to the orthodox medical system. Once care within the orthodox system was sought significant barriers remained. Some patients declined treatment, others were offered inappropriate care and some were referred to a tertiary medical centre where they were definitively diagnosed with breast cancer. Dismissal of symptoms Despite noticing a problem in their breast, many of the women interviewed were not immediately concerned and did not initially seek care. Multiple women described their initial conviction that the lump was not a serious medical issue. One woman stated:
Figure 2.
Conceptual model of barriers to breast cancer treatment.
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Map of Nigeria showing the hometowns of women interviewed.
I didn’t do anything because, I didn’t know what breast cancer is; I thought it was one of those diseases that comes and goes; I didn’t know it was something to take very serious. It was when I got to UCH that I was told about it and how deadly it is if one does not take her treatment in order as recommended; I didn’t know all these before.
Many women initially ascribed the cause of the lump to be a boil, which they gave as one reason they did not worry or seek medical care. One woman said, ‘I noticed a lump like the size of novalgin tablet. I didn’t … count it to be anything I thought it was a boil and I didn’t tell anyone’. It was only when the symptoms failed to disappear that they became concerned. Others noted that the lump was painless and for this reason they did not believe it to be a serious condition. One woman explained, ‘the lump was small like pimples and was painless, so I ignored it’. Several women gave a narrative about all of the breast problems they had ever experienced, which they linked together into a single illness narrative. Because their past breast problems had resolved without major intervention, they initially felt that their new symptoms would also resolve. Seeking alternative care Only a few of the women acknowledged that they initially sought care outside the orthodox medical system. The types of alternative medicine described were predominantly herbal and spiritual. One woman described, ‘I thought the lump was a boil, so I bought rub and used it to rub it, hoping that the boil will disappear. I also bought herbs to use for the stomach-ache. I thought it was diarrhoea’. Other patients who used herbs
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chose this remedy because it had successfully helped them with a breast problem in the past. One woman described going to a traditional spiritual healer for her symptoms before seeing a healthcare worker because her mother-in-law believed the lump was caused by poison, yet when the alternative treatment was not successful she found her way to an orthodox medical provider. She said:
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I didn’t know what it was, my mother-in-law believed it was a symptom of poison, she took me to a healer; when I got an idea of what it might be from a billboard; the chemist I talked to promised to refer me; but he didn’t until I decided to meet a doctor myself in February 2009.
Physicians placed a significant emphasis on the role of alternative treatment seeking in delaying diagnosis of breast cancer. One physician felt that not only do patients see alternative practitioners, but that they actively try and hide this from their physicians. She said, ‘Some of them will not let us know that they have gone to the herbalist because they probably think it won’t go down well with us’. Seeking orthodox medical care Many of the women rapidly sought out orthodox medical care once they noticed symptoms. The decision to seek orthodox care was frequently influenced by how easily accessible a healthcare practitioner was; women sought out a local practitioner who they knew or who lived in close proximity. This was often a community-based provider such as a chemist or a nurse rather than a physician. A physician, frustrated by delays, described a typical sequence of practitioners that a patient might speak with, ‘Yes, most commonly they talk to a family relative, they talk to the nurse next door, they will talk to the chemist, the pharmacist, and then probably eventually their church members, pastors, imams, and then we are almost always the last’. Declined treatment Once orthodox testing and treatment were recommended, some patients declined to follow through on recommended testing. One woman described how she was so frustrated with the many tests required by the tertiary hospital that she gave up and resumed self-treatment. She stated: the doctor only told me to go to UPTH; when I got to UPTH they were telling me to go and do HIV tests and some other tests and their tests at times take 3 months before you see result. So I got pissed off and went home to use drugs, and since it was not paining.
Inappropriate medical care Women frequently sought initial care from non-physician community healthcare provider including nurses and chemists. Multiple women described being given oral medications or injections, usually of antibiotics, sometimes for months or years before they were referred or made an independent decision to seek care elsewhere. One woman who described years of treatment for a lump with medications by multiple healthcare providers. She said: I went to maternity centre at Agba community; the health personnel there gave me injection and said the lump would disappear. After a while, I went back to the maternity to complain
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that the lump in still there and bigger than before. She gave me injection again and some drugs, which I was [always] taking.
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Despite her best efforts to seek orthodox care, this woman’s referral was delayed by inappropriate care. Delays after referral to a tertiary medical centre Even once a patient was referred to or chose to go to a secondary or tertiary facility barriers to diagnosis remained. In addition to inappropriate treatment, women faced system delays in receiving their test results and had difficulty accessing care due to strikes by various members of the healthcare team including consultants and residents. One woman described her challenges in scheduling her surgery stating: I had a minor surgery in which the lump was removed and taken for test. It took 2 weeks and 2 days before the result came out. The doctor then booked me for surgery in January 2009, he said he already had appointments for the rest of the year, September to December 2008.
Physicians also noted these challenges. One stated: We will have some places where histologies are not even carried out … and if histologies are not carried out, they will not even send the patient to us. They do the surgery, they discard the specimen, so the patient goes home and doesn’t know if [she] should come for the specialist care.
Return to alternative care After receiving a breast cancer diagnosis, some women chose to leave the orthodox care system and go back to seeking alternative care. One woman said, ‘I didn’t believe the result of the biopsy, so I went to look for care elsewhere. I went to a traditional healer’. Physicians also described this pattern of going back and forth between the alternative and orthodox medical systems. One physician stated: I can remember a scenario where a particular patient came in. She actually presented early enough … She was offered mastectomy and she was like ‛God forbid, how can I part with my breast?’ The next thing she did was to discuss with her own spiritual healer and start praying about it … Only for her to present when it was fungating. And a lot of people will have that same story to tell.
Several women believed that their illness was caused by a spiritual affliction. One described a prophecy that had been told to her about her cancer. She said, ‘My cancer is a spiritual attack, it is caused by witches and wizards, I [knew] it would happen. I was told that cancer arrow would be fashioned’. Because they believed the cause to be spiritual, they believed seeking spiritual care was the most logical choice.
Delays in treatment Once a breast cancer diagnosis was made, multiple social and personal factors acted to delay the initiation or completion of breast cancer treatment (Figure 2). Denial, fear of surgery – particularly of mastectomy – strikes by hospital staff, and the costs of treatment all potentially delay treatment. Even after treatment was begun, the latter three factors could still delay or even prevent a full course of treatment.
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Denial Upon diagnosis, a reaction described by several women was complete denial of their condition. One woman blamed inaccurate test results, ‘I didn’t believe it. I told the doctor the result he brought for me was not my result. So, I went away from him’. Another patient still denied that she had cancer insisting, even while receiving radiotherapy treatments, that ‘[t]he doctor never said it was cancer, he said it was a lump’. Physicians also described the role denial plays in reducing their abilities to help their patients. One physician stated: sometimes they will have even come early, the diagnosis is made, and they just run away. They don’t want to accept it. Denial … A lot of them are in that particular phase of their treatment. Denial. They go and don’t come back for MONTHS. By the time they come back, they come with very advanced diseases.
The belief that breast cancer is inevitably fatal and the lack of examples of survivorship may have contributed to this denial. A common word used in Yoruba for cancer is jejere, which means something that devours you (Oluwatosin, 2006), and for these women it was isolating and presumed to be deadly. Most of the women denied knowing anyone with breast cancer. Those who did know someone usually knew someone who had died from the disease. Only one woman described knowing a long-term survivor of breast cancer. Furthermore, when asked if they knew of any famous Nigerian women with breast cancer, very few could name any, and the only name mentioned multiple times was the wife of a former President whose death may have been hyped by wide media reports. Fear of surgery Another common theme that emerged was that when the women presented to a physician they were not anticipating surgical treatment for their breast problem. Many described shock and fear when they were told they should have surgery. One woman said: When the doctor that told me the only solution is surgery I was afraid, I didn’t want my breast to be cut off. I didn’t go back to him, I went to another doctor again that was giving me drugs that will kill the cell instead of surgery, but the lump was getting bigger and later spread to the other breast.
Despite the progression of her disease, she continued to believe that the solution did not lie in surgical treatment stating, ‘According to the bible in Jeremiah 30:17; the word of God says that “I shall be whole again,” I believe that they will not cut it and the lump will go’. Family members often played an important role in whether or not a patient overcame her fear of surgery and proceeded with a mastectomy. One woman’s husband did not give permission for surgery, as he was worried about the outcome. She stated, ‘When it was time to go for the major operation my husband refused. He said I would die if they cut my breast’. In contrast, another woman described how the support of her brother was crucial stating: I cried when the doctor told me it was cancer that I would need surgery; my brother encouraged me and said since I have stopped child bearing surgery to remove a breast should not make me feel too bad; that I am going to be okay; if not for my brother, I don’t know what would have happened.
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Clearly, there is an interpersonal component of choosing to have a mastectomy, but the relationship is complex as family members can play both an encouraging and discouraging role. Physicians also noted that fear of surgery, any surgery not specifically mastectomy, was a common occurrence. One said, ‘Some think that if they go through surgery they will die, ok, so yes they know they have cancer they probably want something done, but when they think of surgery they have this misconception about surgery’.
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Strikes by hospital staff Systemic barriers outside the patient’s control also played a significant role in treatment delays. Multiple patients described delays due to strikes by hospital staff. One woman described how a strike had pushed back her surgery by months, ‘When I made up my mind for the surgery around August 2010, there was a strike in UCH, so I couldn’t do it then; until February this year’. One patient also described being turned away when the machine for delivering radiation treatments was not functioning. When asked specifically about system and institutional delays, the physicians all acknowledged that they exist; however, these barriers were not brought up without prompting. None of the physicians mentioned the effects that strikes might have on patients. One physician was so uncomfortable with discussing system delays that he would only discuss it with the audio-recorder switched off. Cost Another significant factor leading to delay of treatment was cost. All medical expenses had to be paid out of pocket by the patient and her family. Treatments were delayed while women raised funds for surgery, chemotherapy or radiation. As one patient described, ‘I was to come to UCH after the surgery, but I could not afford to come; the money we borrowed for surgery was yet to be paid, and to come to UCH, I will have to borrow again’. Despite their need for financial support, almost half of the women mentioned that they had told very few people about their diagnosis. One woman agreed to do the interview but asked not to be audio-recorded due to privacy concerns. Several women acknowledged that this privacy came at a cost: they were less able to call on churches and family that might otherwise provide emotional and financial support. One woman said, ‘My church normally supports people financially to pay surgery cost and other medical fees, but I didn’t tell my church about it’. Others had asked for loans without revealing the reason they needed funds. Cost was the primary barrier to treatment discussed by the physicians. They described how their hands are tied when their patients do not have the funds to pay for treatment. One physician stated: Finance … becomes another issue … An average Nigerian is poor … so the finances are difficult to meet up with the cost of the treatment … So it can be very very disturbing. You want to help but there is no money to do what you want to do.
Discussion Our study shows that barriers to timely breast cancer care in Nigeria are complex and occur at many levels including but not limited to patient behaviours. The barriers to care identified in this study are consistent with the environmental and behavioural factors
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described in a socio-ecological framework, which presumes that health behaviours are shaped not only by an individual but also the social factors around them (Glanz & Rimer, 2005; McLeroy, Bibeau, Steckler, & Glanz, 1988; Reifsnider, Gallagher, & Forgione, 2005). Our study identified intertwined barriers to breast cancer care at the policy-level, community-level, institutional-level, interpersonal-level and individual-level. The individual-level factors contributing to delay include a lack of awareness about the existence of and symptoms of breast cancer in the female population in Nigeria, which is consistent with previous studies in the general population in Southern Nigeria (Okobia, Bunker, Okonofua, & Osime, 2006). October is the designated breast cancer awareness month in Nigeria (Ugwu, 2013), but without a National Cancer Control Policy, awareness programmes are uncoordinated and do not appear to have effectively reached the entire female population. Many patients delayed seeking care because, despite identifying a breast mass, they did not associate it with the possibility of a serious illness. This finding is also consistent with studies of patients with a variety of cancers in the USA and Europe. A qualitative synthesis of 32 studies identified that recognition of symptoms, especially in the absence of pain, strongly influenced help-seeking behaviours and delays in help-seeking (Smith, Pope, & Botha, 2005). Furthermore, Nigerian women were unprepared for the types of treatment that would be recommended, especially surgery. Patients frequently described the surprise they felt when surgical treatment was recommended. This surprise suggests that fear of mastectomy does not have an impact on the initial healthcare-seeking because they were not aware that mastectomy was a common treatment modality. This is in contrast to previous work describing breast cancer in Nigeria which suggested that fear of mastectomy had an impact on stage of disease at diagnosis (Adesunkanmi et al., 2006). Nevertheless, our patient interviews indicate that fear of mastectomy surgery was a significant barrier to appropriate treatment. Of additional concern is a previous study in Northern Nigeria that demonstrated significant negative social consequences for women who underwent mastectomy (Odigie et al., 2010). Our interviews revealed that family members played an important role in delaying or encouraging surgery, which shows that care decisions have complex interpersonal dimensions. Another individual-level barrier discussed is alternative care. Previous work has frequently placed patients’ alternative healthcare-seeking behaviours at the centre of the causes of delayed breast cancer diagnosis in Nigeria (Anyanwu et al., 2011). A previous study of complementary and alternative medicine (CAM) use by cancer patients in Nigeria put usage of CAM at nearly two-thirds of patients (Ezeome & Anarado, 2007). This suggests that patients in our study may have been reluctant to disclose alternative treatment usage in the context of a recorded interview; this view was endorsed by the physicians interviewed. It is also possible that women who use CAM primarily never present to a tertiary medical centre. A much more common narrative than CAM use was accessing the orthodox medical system with a non-physician healthcare worker as the primary point of care. Multiple patients told stories of being treated improperly for months to years by these practitioners before being referred, if at all, for diagnosis and treatment at a larger medical centre. This shows the importance of addressing community and institutional-level barriers as well as individual-level barriers. Several previous studies in Nigeria have indicated that professional women’s knowledge about the disease is limited, even among well-educated women such as nurses and teachers (Akhigbe & Omuemu, 2009; Odusanya, 2001; Odusanya & Tayo, 2001). However, little more has been done to explore the knowledge
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and awareness level of community-based rather than hospital-based male or female healthcare providers. Institutional and policy-level delays within the healthcare system contribute to delays in care at both the level of diagnosis and the level of treatment. Patients were turned away from hospitals due to strikes and dysfunctional treatment equipment, or had to wait months for a test result or an appointment for surgery. In recent years, strikes by physicians, over working conditions, and enumeration have become more frequent and have had significant effects on the ability of hospitals to treat patients (Akinyemi & Atilola, 2013; Umukoro, 2012). Because the healthcare system relies mainly on out-ofpocket payments, ability to pay also played a significant role. Clearly in order to develop a streamlined system of care, these barriers, as well as patient behaviours and attitudes, will have to be addressed. Our interviews show that patients primarily knew women who had died of breast cancer, and there are very few examples of famous Nigerian women who have had breast cancer and even fewer who have survived. The one famous Nigerian mentioned by multiple interviewees as having had breast cancer, actually died from ovarian cancer (Okanlawon, Fabiyi, & Falola, 2009). In the USA, the openness of famous women about their diagnosis of breast cancer and their survival, is often referenced as a turning point in the culture and awareness of breast cancer (Olson, 2002). One can imagine prominent survivors in Nigeria would help change community-level perceptions of the fatality of the disease and the need to keep the disease secret. Multiple patients admitted that by maintaining secrecy about their diagnosis they reduced their financial and social support. Strengths and limitations of the study Despite recruiting patients from a single tertiary care centre, the patients recruited represented a wide geographic range across southern Nigerian. Because of the geographic diversity of our patient sample, this study is generalisable to women who live in big cities across Southern Nigeria, however, given the diversity of ethnic groups within Nigeria it is difficult to generalise further. A broad spectrum of educational backgrounds was represented as well as a significant range of ages. Both major religions in the area were also present. Information about the social class based on income of the women was not ascertained because many participants were informally employed and there was resistance to disclosing one’s income during our interviews. Due to the location of recruitment, our study does not capture the experiences of patients who never make it to tertiary care for breast cancer treatment. Therefore, we know little about the barriers to care for women who are never formally diagnosed. The medical setting may also have reduced willingness to speak about CAM for fear of being judged by their physicians or the belief that such an admission might affect their treatment. Furthermore, follow-up questions were limited by the use of a translator.
Conclusions Our interviews show that it is important to understand not only healthcare-seeking behaviours but also institutional- and system-level barriers to find critical points of contact with the healthcare system as targets for education. Making assumptions or generalisations about the patterns of care for a particular ailment may lead researchers away from productive avenues for education and improvement in care. While the use of alternative therapies may represent a significant delay that was not captured here, based
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on these data, understanding delays within the biomedical system appears to be more significant and easier to target for improvement. Community healthcare workers, such as pharmacists, play an important role in healthcare-seeking behaviours. Understanding patterns of healthcare-seeking behaviours in women more broadly is needed to better understand the areas in which healthcare education may be most effective. It is also necessary to understand the level of awareness and knowledge of breast cancer among community healthcare practitioners. This is a group of educated individuals who may be able to have a large impact by reaching multiple women for every healthcare worker educated. They could also refer women more quickly to hospital facilities with the resources to provide high quality care. While undertaking an American-style screening programme for breast cancer that relies on mammography is not feasible in a low-income setting, clinical down-staging of the disease remains a realistic goal (Corbex, Burton, & Sancho-Garnier, 2012). Training of new community healthcare workers in low-income settings in sub-Saharan Africa specifically to screen women for breast cancer has proven effective (Abuidris et al., 2013). This study raises the possibility that a modified version of this type of model, which here may involve the education of existing healthcare workers, should be explored in Nigeria. Lastly, cancer care is multidisciplinary and expensive in any health system. The strength of a health system can be judged by the outcomes in managing chronic diseases such as cancer. Women are now surviving long enough to develop breast cancer without the necessary health infrastructure to support their care. Nigeria has a gross domestic product per capita of $2800 (Central Intelligence Agency, 2013), but the Nigerian healthcare system has been underfunded for decades. Given the recent emergence of Nigeria as the leading economy in Africa, the time is ripe for the country to implement a National Cancer Control Plan and invest in evidence-based and cost-effective interventions at multiple levels to reduce the burden of breast cancer. Even if healthcare providers at the community and/or primary care level promptly refer breast cancer patients for tertiary care, without access to high functioning hospitals to improve surgical outcomes, women will remain fearful of surgery. The Nigerian Government has endorsed health insurance schemes to cover catastrophic illnesses like cancer as a priority area for future investments in health care. Breast and cervical cancer demonstration projects can be used to integrate women’s health beyond provision of reproductive services. References Abuidris, D. O., Elsheikh, A., Ali, M., Musa, H., Elgaili, E., Ahmed, A. O., … Mojammed, S. I. (2013). Breast-cancer screening with trained volunteers in a rural area of Sudan: A pilot study. Lancet Oncology, 14, 363–370. doi:10.1016/S1470-2045(12)70583-1 Adebamowo, C. A., Ogundiran, T. O., Adenipekun, A. A., Oyesegun, R. A., Campbell, O. B., Akang, E. E., … Olopade, O. I. (2003). Obesity and height in urban Nigerian women with breast cancer. Annals of Epidemiology, 13, 455–461. doi:10.1016/S1047-2797(02)00426-X Adesunkanmi, A. R. K., Lawal, O. O., Adelusola, K. A., & Durosimi, M. A. (2006). The severity, outcome and challenges of breast cancer in Nigeria. The Breast, 15, 399–409. doi:10.1016/j. breast.2005.06.008 Akhigbe, A. O., & Omuemu, V. O. (2009). Knowledge, attitudes and practice of breast cancer screening among female health workers in a Nigerian urban city. BMC Cancer, 9, 203–212. doi:10.1186/1471-2407-9-203 Akinyemi, O., & Atilola, O. (2013). Nigerian resident doctors on strike: Insights from and policy implications of job satisfaction among resident doctors in a Nigerian teaching hospital. The International Journal of Health Planning and Management, 28, e46–e61. doi:10.1002/hpm.2141
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Anyanwu, S. N. C., Egwuonwu, O. A., & Ihekwoaba, E. C. (2011). Acceptance and adherence to treatment among breast cancer patients in eastern Nigeria. The Breast, 20(Suppl. 2), 1–3. doi:10.1016/j.breast.2011.01.009 Central Intelligence Agency. (2013). The world factbook (2013–2014). Washington, DC: Author. Corbex, M., Burton, R., & Sancho-Garnier, H. (2012). Breast cancer early detection methods for low and middle income countries, a review of the evidence. The Breast, 21, 428–434. doi:10.1016/j.breast.2012.01.002 Erwin, D. O., Spatz, T. S., Stotts, R. C., & Hollenberg, J. A. (1999). Increasing mammography practice by African American women. Cancer Practice, 7, 78–85. doi:10.1046/j.1523-5394. 1999.07204.x Ezeome, E. R., & Anarado, A. N. (2007). Use of complementary and alternative medicine by cancer patients at the University of Nigeria teaching hospital, Enugu, Nigeria. BMC Complementary and Alternative Medicine, 7, 28–35. doi:10.1186/1472-6882-7-28 Farmer, P., Frenk, J., Knaul, F. M., Shulman, L. N., Alleyne, G., Armstrong, L., … Seffrin, J. R. (2010). Expansion of cancer care and control in countries of low and middle income: A call to action. The Lancet, 376, 1186–1193. doi:10.1016/S0140-6736(10)61152-X Glanz, K., & Rimer, B. K. (2005). Theory at a glance: A guide for health promotion practice (2nd ed.). Retrieved from http://www.cancer.gov/cancertopics/cancerlibrary/theory.pdf Groleau, D., Young, A., & Kirmayer, L. J. (2006). The McGill illness narrative interview (MINI): An interview schedule to elicit meanings and modes of reasoning related to illness experience. Transcultural Psychiatry, 43, 671–691. doi:10.1177/1363461506070796 Harford, J. B., Otero, I. V., Anderson, B. O., Cazap, E., Gradishar, W. J., Gralow, J., … Badwe, R. A. (2012). Problem solving for breast health care delivery in low and middle resource countries (LMCs): Consensus statement from the breast health global initiative. The Breast, 20, 520–529. doi:10.1016/j.breast.2011.02.007 Huo, D., Kim, H.-J., Adebamowo, C. A., Ogundiran, T. O., Akang, E. E., Campbell, O. B., … Olopade, O. I. (2008). Genetic polymorphisms in uridine diphosphoglucuronosyltransferase 1A1 and breast cancer risk in Africans. Breast Cancer Research and Treatment, 110, 367–376. doi:10.1007/s10549-007-9720-7 Jedy-Agba, E., Curado, M. P., Ogunbiyi, O., Oga, E., Fabowale, T., Igbinola, F., … Adebamowo, C. A. (2012). Cancer incidence in Nigeria: A report from population-based cancer registries. Cancer Epidemiology, 36, e271–e278. doi:10.1016/j.canep.2012.04.007 Jemal, A., Bray, F., Center, M. M., Ferlay, J., Ward, E., & Forman, D. (2011). Global cancer statistics. CA: A Cancer Journal for Clinicians, 61, 69–90. doi:10.3322/caac.20107 Lannin, D. R., Mathews, H. F., Mitchell, J., & Swanson, M. S. (2002). Impacting cultural attitudes in African-American women to decrease breast cancer mortality. The American Journal of Surgery, 184, 418–423. Retrieved from http://americanjournalofsurgery.com/ McLeroy, K. R., Bibeau, D., Steckler, A., & Glanz, K. (1988). An ecological perspective on health promotion programs. Health Education Quarterly, 15, 351–377. doi:10.1177/109019818801 500401 Odigie, V. I., Tanaka, R., Yusufu, L. M. D., Gomna, A., Odigie, E. C., Dawotola, D. A., & Margaritoni, M. (2010). Psychosocial effects of mastectomy on married African women in northwestern Nigeria. Psycho-Oncology, 19, 893–897. doi:10.1002/pon.1675 Odusanya, O. O. (2001). Breast cancer: Knowledge, attitudes, and practices of female schoolteachers in Lagos, Nigeria. The Breast Journal, 7, 171–175. doi:10.1046/j.1524-4741.1998.41 0062.x-i1 Odusanya, O. O., & Tayo, O. O. (2001). Breast cancer: Knowledge, attitude and practice among nurses in Lagos, Nigeria. Acta Oncologica, 40, 844–848. doi:10.1080/02841860152703472 Okanlawon, S., Fabiyi, O., & Falola, F. (2009, December 28). Maryam Babangida dies at 61. The Punch. Okobia, M. N., Bunker, C. H., Okonofua, F. E., & Osime, U. (2006). Knowledge, attitude and practice of Nigerian women towards breast cancer: A cross-sectional study. World Journal of Surgical Oncology, 4, 11. doi:10.1186/1477-7819-4-11 Olakunde, B. O. (2012). Public health care financing in Nigeria: Which way forward? Annals of Nigerian Medicine, 6, 4–10. doi:10.4103/0331-3131.100199 Olson, J. S. (2002). Bathsheba’s breast. Baltimore, MD: The Johns Hopkins University Press.
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Oluwatosin, O. A. (2006). Rural women’s perception of breast cancer and its early-detection measures in Ibadan, Nigeria. Cancer Nursing, 29, 461–466. doi:10.1097/00002820-20061100000006 Oluwatosin, O. A. (2010). Assessment of women’s risk factors for breast cancer and predictors of the practice of breast examination in two rural areas near Ibadan, Nigeria. Cancer Epidemiology, 34, 425–428. doi:10.1016/j.canep.2010.04.005 Onwujekwe, O., & Uzochukwu, B. (2005). Socio-economic and geographic differentials in costs and payment strategies for primary healthcare services in southeast Nigeria. Health Policy, 71, 383–397. doi:10.1016/j.healthpol.2004.06.006 Pasick, R. J., & Burke, N. J. (2008). A critical review of theory in breast cancer screening promotion across cultures. Annual Review of Public Health, 29, 351–368. doi:10.1146/annurev. publhealth.29.020907.143420 Reifsnider, E., Gallagher, M., & Forgione, B. (2005). Using ecological models in research on health disparities. Journal of Professional Nursing, 21, 216–222. doi:10.1016/j.profnurs.2005.05.006 Richards, M., Smith, P., Ramirez, A., Fentiman, I., & Rubens, R. (1999). The influence on survival of delay in the presentation and treatment of symptomatic breast cancer. British Journal of Cancer, 79, 858–864. doi:10.1038/sj.bjc.6690137 Smith, L. K., Pope, C., & Botha, J. L. (2005). Patients’ help-seeking experiences and delay in cancer presentation: A qualitative synthesis. The Lancet, 366, 825–831. doi:10.1016/S0140-6736 (05)67030-4 Ugwu, P. (2013, October 24). Jumia supports breast cancer foundation with pink Week. Nigeria Communications Week. Retrieved from http://nigeriacommunicationsweek.com.ng/e-business/ jumia-supports-breast-cancer-foundation-with-pink-week Ukwenya, A. Y., Yusufu, L. M. D., Nmadu, P. T., Garba, E. S., & Ahmed, A. (2008). Delayed treatment of symptomatic breast cancer: The experience from Kaduna, Nigeria. South African Journal of Surgery, 46, 106–110. Retrieved from http://www.sajs.org.za Umukoro, N. (2012). Governance and public health care in Nigeria. Journal of Health Management, 14, 381–395. doi:10.1177/0972063412468970
Global Public Health: An International Journal for Research, Policy and Practice Publication details, including instructions for authors and subscription information: http://www.tandfonline.com/loi/rgph20
Social barriers to diagnosis and treatment of breast cancer in patients presenting at a teaching hospital in Ibadan, Nigeria a
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Liese Pruitt , Tolulope Mumuni , Eugene Raikhel , Adeyinka d
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Ademola , Temidayo Ogundiran , Adeniyi Adenipekun , Imran b
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Morhason-Bello , Oladosu A. Ojengbede & Olufunmilayo I.
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Olopade a
Pritzker School of Medicine, University of Chicago, Chicago, IL, USA b
Centre for Population and Reproductive Health, College of Medicine, University of Ibadan, Ibadan, Nigeria c
Department of Comparative Human Development, University of Chicago, Chicago, IL, USA d
Department of Surgery, College of Medicine, University of Ibadan, Ibadan, Nigeria e
Department of Radiotherapy, College of Medicine, University of Ibadan, Ibadan, Nigeria f
Center for Clinical Cancer Genetics & Global Health, Department of Medicine, University of Chicago, Chicago, IL, USA Published online: 02 Dec 2014.
To cite this article: Liese Pruitt, Tolulope Mumuni, Eugene Raikhel, Adeyinka Ademola, Temidayo Ogundiran, Adeniyi Adenipekun, Imran Morhason-Bello, Oladosu A. Ojengbede & Olufunmilayo I. Olopade (2014): Social barriers to diagnosis and treatment of breast cancer in patients presenting at a teaching hospital in Ibadan, Nigeria, Global Public Health: An International Journal for Research, Policy and Practice, DOI: 10.1080/17441692.2014.974649 To link to this article: http://dx.doi.org/10.1080/17441692.2014.974649
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Global Public Health, 2014 http://dx.doi.org/10.1080/17441692.2014.974649
Social barriers to diagnosis and treatment of breast cancer in patients presenting at a teaching hospital in Ibadan, Nigeria
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Liese Pruitta, Tolulope Mumunib, Eugene Raikhelc, Adeyinka Ademolad, Temidayo Ogundirand, Adeniyi Adenipekune, Imran Morhason-Bellob, Oladosu A. Ojengbedeb* and Olufunmilayo I. Olopadef* a Pritzker School of Medicine, University of Chicago, Chicago, IL, USA; bCentre for Population and Reproductive Health, College of Medicine, University of Ibadan, Ibadan, Nigeria; cDepartment of Comparative Human Development, University of Chicago, Chicago, IL, USA; dDepartment of Surgery, College of Medicine, University of Ibadan, Ibadan, Nigeria; eDepartment of Radiotherapy, College of Medicine, University of Ibadan, Ibadan, Nigeria; fCenter for Clinical Cancer Genetics & Global Health, Department of Medicine, University of Chicago, Chicago, IL, USA
(Received 4 January 2014; accepted 22 September 2014) Globally, breast cancer is the most frequent malignancy in women, and stage at diagnosis is a key determinant of outcome. In low- to middle-income countries, including Nigeria, advanced stage diagnosis and delayed treatment represent a significant problem. That social barriers contribute to delay has been noted in previous research; however, few specific factors have been studied. Using semi-structured interviews, this study identifies social barriers to diagnosis and treatment for patients who presented at University College Hospital Ibadan, Nigeria. Transcripts from the interviews were coded and analysed thematically. Thirty-one patients and five physicians were interviewed. The median age of patients was 51 (range: 28 to above 80), 83% were Christian and 17% were Muslim. Preliminary analysis showed that delays in diagnosis reflected a lack of education as well as the utilisation of nonphysician medical services such as pharmacists. Delays in treatment were often due to fear of unanticipated surgery and cost. The majority of women did not know the cause of their breast cancer, but some believed it was caused by a spiritual affliction. This study suggests that further education and awareness of breast cancer for both patients and providers is needed in order to increase early stage diagnosis. Keywords: breast cancer; Nigeria; qualitative research; social barriers to healthcare; non-communicable diseases
Introduction The cancer burden in low- to middle-income countries (LMIC) is increasing, and the survival rates in LMIC are much poorer than those seen in high-income nations (Farmer et al., 2010). Furthermore, most of the research to understand the social impact of cancer has focused on the USA and Europe (Odigie et al., 2010). In order to address the needs of cancer patients across the globe, we need to understand diverse local behaviours and beliefs related to cancer outside of an American or European context. Breast cancer is the most frequent malignancy affecting women worldwide (Jemal et al., 2011), and the stage of diagnosis is a key determinant of final outcome for breast *Corresponding authors. Emails: [email protected]; [email protected] © 2014 Taylor & Francis
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cancer patients (Richards, Smith, Ramirez, Fentiman, & Rubens, 1999). In the LMIC, delayed treatment seeking and advanced stage diagnosis represent a significant problem (Adesunkanmi, Lawal, Adelusola, & Durosimi, 2006). Breast cancer is the most common cancer affecting women in Nigeria, and delayed presentation has been observed for four decades (Oluwatosin, 2010). Furthermore, the incidence of breast cancer in Nigeria is increasing (Jedy-Agba et al., 2012). Nigeria is the most populous country in Africa with an estimated population of 177 million people. It is a country affected by significant inequality and 70% of the population lives in poverty (Central Intelligence Agency, 2013). The healthcare system in Nigeria is complex and incorporates a wide range of providers including public system employees, private providers, non-governmental and community-based organisations, and religious and traditional care providers. The Nigerian healthcare system is financed by a combination of tax revenue, out-of-pocket payment, donor funding and health insurance. Challenges facing the Nigerian healthcare system include limited institutional capacity, poor health infrastructure, and a corrupt, unstable economic and political context (Olakunde, 2012; Onwujekwe & Uzochukwu, 2005). There are many potential barriers that prevent women from seeking treatment upon first noticing breast cancer symptoms. These include economic and logistical barriers (Anyanwu, Egwuonwu, & Ihekwoaba, 2011), as well as cultural and social factors such as stigma or poor healthcare-seeking behaviours. The effects of these cultural and social barriers have been noted in previous studies; however, the identification of specific factors and the extent of their influence have never been explored in depth (Anyanwu et al. 2011; Ukwenya, Yusufu, Nmadu, Garba, & Ahmed, 2008). Strategies for addressing late stage presentation have been developed previously in the USA. Racial minority groups have higher rates of late stage presentation than Caucasian women, and a range of programmes has been developed to address this issue (Lannin, Mathews, Mitchell, & Swanson, 2002). A review of projects designed to change screening behaviours in minority populations in the USA concluded that the most effective interventions were guided by anthropological study of the target community. Studies structured in this manner were more effective in changing screening rates than those utilising traditional behaviour change indicators (Erwin, Spatz, Stotts, & Hollenberg, 1999; Pasick & Burke, 2008). The importance of a culturally tailored approach in a global context was emphasised in the consensus statement from the Breast Health Global Initiative, which discussed the importance of qualitative inquiry in the design of interventions in order to understand the local attitudes and barriers to care (Harford et al., 2012). The purpose of this study was to use qualitative methods to assess what cultural and social barriers influence delayed breast cancer diagnosis and to understand healthcare-seeking behaviours of women presenting for care at a tertiary hospital in Ibadan, Nigeria.
Methods The study is based on the Nigerian Breast Cancer Study, an on-going case–control study of breast cancer in Ibadan, Southwest Nigeria that has been in the field since 1998 with approval by the institutional review boards of the University of Ibadan and the University of Chicago as previously described (Adebamowo et al., 2003; Huo et al., 2009).
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Research participants Patients were recruited in the radiotherapy and surgery clinics at University College Hospital (UCH), Ibadan, Nigeria in July 2011. All women with a diagnosis of breast cancer were eligible regardless of stage of diagnosis as long as they were 18 years of age or older. Patients from all ethnic groups and language groups were eligible as long as they spoke a common language with the translator available. Physician participants were recruited from the residents in the radiotherapy department.
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Interview procedure When breast cancer patients completed their scheduled treatment, they were informed about the study and offered the opportunity to participate. Patient interviews took place in empty consultation rooms in the clinical setting. All of the interviews were semistructured, so deviation from the interview guide was permitted to ask follow-up questions or pursue topics introduced by the subject. The patient interview guide was based on the McGill Illness Narrative Interview (Groleau, Young, & Kirmayer, 2006) although due to the more focused nature of this research and the time constraints on patients, the scope of the questions was reduced. The interviews focused on how women first found their breast cancer, their healthcare-seeking behaviours, any delays they had experienced in care, beliefs about disease causation, and experiences with stigma. Interviews were conducted with the assistance of a gender and dialect concordant translator who was experienced in public health work and audio-recorded. Physician interviews were conducted in English by LP and audio-recorded. These interviews focused on perceived reasons for delays in care, as well as perception of breast cancer in the community.
Data analysis Audio-recorded interviews conducted in Yoruba were translated and transcribed wordfor-word into English by the translator. Interviews conducted in English were transcribed word-for-word by LP. Each participant was assigned an identification code to protect his or her identity. A thematic analysis was performed and conceptual models of barriers to care were developed (Figures 1 and 2). Data from the interviews were analysed using QSR International’s NVivo 10 software by LP and MT. Both researchers coded every interview and a Cohen’s Kaplan coefficient was calculated for all themes and all interviews, weighted by interview length, with a combined value of 0.78.
Results Demographics Thirty-one female breast cancer patients were recruited from the radiotherapy and surgery outpatient clinics and inpatient wards at UCH. The median age of patients was 51 (range: 28 to -above 80), 83% were Christian and 17% were Muslim. Seven had no formal education and nine had a university or polytechnic degree while the remaining patients had an intermediate educational level. They came from a wide range of towns and cities from across southern Nigeria (Figure 3). Many languages were spoken by participants the most common being Yoruba (n = 18), English (n = 15), Ibo (n = 6) and pidgin (n = 3).
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Figure 1. Conceptual model of healthcare-seeking patterns of women with breast symptoms to diagnosis with breast cancer.
Five resident physicians in the radiotherapy department were interviewed. Three were males and two were females. They ranged in age from 35 to 38 years. Four were Christian and one was Muslim. Barriers to diagnosis Healthcare-seeking behaviours between the initial recognition of symptoms and eventual diagnosis with and treatment for breast cancer were complex (Figures 1 and 2). Delays in diagnosis were often related to complex patterns of healthcare-seeking as well as a lack of awareness that symptoms might be serious (Figure 1). Some patients initially dismissed their symptoms, others sought alternative care and others went directly to the orthodox medical system. Once care within the orthodox system was sought significant barriers remained. Some patients declined treatment, others were offered inappropriate care and some were referred to a tertiary medical centre where they were definitively diagnosed with breast cancer. Dismissal of symptoms Despite noticing a problem in their breast, many of the women interviewed were not immediately concerned and did not initially seek care. Multiple women described their initial conviction that the lump was not a serious medical issue. One woman stated:
Figure 2.
Conceptual model of barriers to breast cancer treatment.
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Map of Nigeria showing the hometowns of women interviewed.
I didn’t do anything because, I didn’t know what breast cancer is; I thought it was one of those diseases that comes and goes; I didn’t know it was something to take very serious. It was when I got to UCH that I was told about it and how deadly it is if one does not take her treatment in order as recommended; I didn’t know all these before.
Many women initially ascribed the cause of the lump to be a boil, which they gave as one reason they did not worry or seek medical care. One woman said, ‘I noticed a lump like the size of novalgin tablet. I didn’t … count it to be anything I thought it was a boil and I didn’t tell anyone’. It was only when the symptoms failed to disappear that they became concerned. Others noted that the lump was painless and for this reason they did not believe it to be a serious condition. One woman explained, ‘the lump was small like pimples and was painless, so I ignored it’. Several women gave a narrative about all of the breast problems they had ever experienced, which they linked together into a single illness narrative. Because their past breast problems had resolved without major intervention, they initially felt that their new symptoms would also resolve. Seeking alternative care Only a few of the women acknowledged that they initially sought care outside the orthodox medical system. The types of alternative medicine described were predominantly herbal and spiritual. One woman described, ‘I thought the lump was a boil, so I bought rub and used it to rub it, hoping that the boil will disappear. I also bought herbs to use for the stomach-ache. I thought it was diarrhoea’. Other patients who used herbs
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chose this remedy because it had successfully helped them with a breast problem in the past. One woman described going to a traditional spiritual healer for her symptoms before seeing a healthcare worker because her mother-in-law believed the lump was caused by poison, yet when the alternative treatment was not successful she found her way to an orthodox medical provider. She said:
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I didn’t know what it was, my mother-in-law believed it was a symptom of poison, she took me to a healer; when I got an idea of what it might be from a billboard; the chemist I talked to promised to refer me; but he didn’t until I decided to meet a doctor myself in February 2009.
Physicians placed a significant emphasis on the role of alternative treatment seeking in delaying diagnosis of breast cancer. One physician felt that not only do patients see alternative practitioners, but that they actively try and hide this from their physicians. She said, ‘Some of them will not let us know that they have gone to the herbalist because they probably think it won’t go down well with us’. Seeking orthodox medical care Many of the women rapidly sought out orthodox medical care once they noticed symptoms. The decision to seek orthodox care was frequently influenced by how easily accessible a healthcare practitioner was; women sought out a local practitioner who they knew or who lived in close proximity. This was often a community-based provider such as a chemist or a nurse rather than a physician. A physician, frustrated by delays, described a typical sequence of practitioners that a patient might speak with, ‘Yes, most commonly they talk to a family relative, they talk to the nurse next door, they will talk to the chemist, the pharmacist, and then probably eventually their church members, pastors, imams, and then we are almost always the last’. Declined treatment Once orthodox testing and treatment were recommended, some patients declined to follow through on recommended testing. One woman described how she was so frustrated with the many tests required by the tertiary hospital that she gave up and resumed self-treatment. She stated: the doctor only told me to go to UPTH; when I got to UPTH they were telling me to go and do HIV tests and some other tests and their tests at times take 3 months before you see result. So I got pissed off and went home to use drugs, and since it was not paining.
Inappropriate medical care Women frequently sought initial care from non-physician community healthcare provider including nurses and chemists. Multiple women described being given oral medications or injections, usually of antibiotics, sometimes for months or years before they were referred or made an independent decision to seek care elsewhere. One woman who described years of treatment for a lump with medications by multiple healthcare providers. She said: I went to maternity centre at Agba community; the health personnel there gave me injection and said the lump would disappear. After a while, I went back to the maternity to complain
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that the lump in still there and bigger than before. She gave me injection again and some drugs, which I was [always] taking.
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Despite her best efforts to seek orthodox care, this woman’s referral was delayed by inappropriate care. Delays after referral to a tertiary medical centre Even once a patient was referred to or chose to go to a secondary or tertiary facility barriers to diagnosis remained. In addition to inappropriate treatment, women faced system delays in receiving their test results and had difficulty accessing care due to strikes by various members of the healthcare team including consultants and residents. One woman described her challenges in scheduling her surgery stating: I had a minor surgery in which the lump was removed and taken for test. It took 2 weeks and 2 days before the result came out. The doctor then booked me for surgery in January 2009, he said he already had appointments for the rest of the year, September to December 2008.
Physicians also noted these challenges. One stated: We will have some places where histologies are not even carried out … and if histologies are not carried out, they will not even send the patient to us. They do the surgery, they discard the specimen, so the patient goes home and doesn’t know if [she] should come for the specialist care.
Return to alternative care After receiving a breast cancer diagnosis, some women chose to leave the orthodox care system and go back to seeking alternative care. One woman said, ‘I didn’t believe the result of the biopsy, so I went to look for care elsewhere. I went to a traditional healer’. Physicians also described this pattern of going back and forth between the alternative and orthodox medical systems. One physician stated: I can remember a scenario where a particular patient came in. She actually presented early enough … She was offered mastectomy and she was like ‛God forbid, how can I part with my breast?’ The next thing she did was to discuss with her own spiritual healer and start praying about it … Only for her to present when it was fungating. And a lot of people will have that same story to tell.
Several women believed that their illness was caused by a spiritual affliction. One described a prophecy that had been told to her about her cancer. She said, ‘My cancer is a spiritual attack, it is caused by witches and wizards, I [knew] it would happen. I was told that cancer arrow would be fashioned’. Because they believed the cause to be spiritual, they believed seeking spiritual care was the most logical choice.
Delays in treatment Once a breast cancer diagnosis was made, multiple social and personal factors acted to delay the initiation or completion of breast cancer treatment (Figure 2). Denial, fear of surgery – particularly of mastectomy – strikes by hospital staff, and the costs of treatment all potentially delay treatment. Even after treatment was begun, the latter three factors could still delay or even prevent a full course of treatment.
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Denial Upon diagnosis, a reaction described by several women was complete denial of their condition. One woman blamed inaccurate test results, ‘I didn’t believe it. I told the doctor the result he brought for me was not my result. So, I went away from him’. Another patient still denied that she had cancer insisting, even while receiving radiotherapy treatments, that ‘[t]he doctor never said it was cancer, he said it was a lump’. Physicians also described the role denial plays in reducing their abilities to help their patients. One physician stated: sometimes they will have even come early, the diagnosis is made, and they just run away. They don’t want to accept it. Denial … A lot of them are in that particular phase of their treatment. Denial. They go and don’t come back for MONTHS. By the time they come back, they come with very advanced diseases.
The belief that breast cancer is inevitably fatal and the lack of examples of survivorship may have contributed to this denial. A common word used in Yoruba for cancer is jejere, which means something that devours you (Oluwatosin, 2006), and for these women it was isolating and presumed to be deadly. Most of the women denied knowing anyone with breast cancer. Those who did know someone usually knew someone who had died from the disease. Only one woman described knowing a long-term survivor of breast cancer. Furthermore, when asked if they knew of any famous Nigerian women with breast cancer, very few could name any, and the only name mentioned multiple times was the wife of a former President whose death may have been hyped by wide media reports. Fear of surgery Another common theme that emerged was that when the women presented to a physician they were not anticipating surgical treatment for their breast problem. Many described shock and fear when they were told they should have surgery. One woman said: When the doctor that told me the only solution is surgery I was afraid, I didn’t want my breast to be cut off. I didn’t go back to him, I went to another doctor again that was giving me drugs that will kill the cell instead of surgery, but the lump was getting bigger and later spread to the other breast.
Despite the progression of her disease, she continued to believe that the solution did not lie in surgical treatment stating, ‘According to the bible in Jeremiah 30:17; the word of God says that “I shall be whole again,” I believe that they will not cut it and the lump will go’. Family members often played an important role in whether or not a patient overcame her fear of surgery and proceeded with a mastectomy. One woman’s husband did not give permission for surgery, as he was worried about the outcome. She stated, ‘When it was time to go for the major operation my husband refused. He said I would die if they cut my breast’. In contrast, another woman described how the support of her brother was crucial stating: I cried when the doctor told me it was cancer that I would need surgery; my brother encouraged me and said since I have stopped child bearing surgery to remove a breast should not make me feel too bad; that I am going to be okay; if not for my brother, I don’t know what would have happened.
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Clearly, there is an interpersonal component of choosing to have a mastectomy, but the relationship is complex as family members can play both an encouraging and discouraging role. Physicians also noted that fear of surgery, any surgery not specifically mastectomy, was a common occurrence. One said, ‘Some think that if they go through surgery they will die, ok, so yes they know they have cancer they probably want something done, but when they think of surgery they have this misconception about surgery’.
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Strikes by hospital staff Systemic barriers outside the patient’s control also played a significant role in treatment delays. Multiple patients described delays due to strikes by hospital staff. One woman described how a strike had pushed back her surgery by months, ‘When I made up my mind for the surgery around August 2010, there was a strike in UCH, so I couldn’t do it then; until February this year’. One patient also described being turned away when the machine for delivering radiation treatments was not functioning. When asked specifically about system and institutional delays, the physicians all acknowledged that they exist; however, these barriers were not brought up without prompting. None of the physicians mentioned the effects that strikes might have on patients. One physician was so uncomfortable with discussing system delays that he would only discuss it with the audio-recorder switched off. Cost Another significant factor leading to delay of treatment was cost. All medical expenses had to be paid out of pocket by the patient and her family. Treatments were delayed while women raised funds for surgery, chemotherapy or radiation. As one patient described, ‘I was to come to UCH after the surgery, but I could not afford to come; the money we borrowed for surgery was yet to be paid, and to come to UCH, I will have to borrow again’. Despite their need for financial support, almost half of the women mentioned that they had told very few people about their diagnosis. One woman agreed to do the interview but asked not to be audio-recorded due to privacy concerns. Several women acknowledged that this privacy came at a cost: they were less able to call on churches and family that might otherwise provide emotional and financial support. One woman said, ‘My church normally supports people financially to pay surgery cost and other medical fees, but I didn’t tell my church about it’. Others had asked for loans without revealing the reason they needed funds. Cost was the primary barrier to treatment discussed by the physicians. They described how their hands are tied when their patients do not have the funds to pay for treatment. One physician stated: Finance … becomes another issue … An average Nigerian is poor … so the finances are difficult to meet up with the cost of the treatment … So it can be very very disturbing. You want to help but there is no money to do what you want to do.
Discussion Our study shows that barriers to timely breast cancer care in Nigeria are complex and occur at many levels including but not limited to patient behaviours. The barriers to care identified in this study are consistent with the environmental and behavioural factors
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described in a socio-ecological framework, which presumes that health behaviours are shaped not only by an individual but also the social factors around them (Glanz & Rimer, 2005; McLeroy, Bibeau, Steckler, & Glanz, 1988; Reifsnider, Gallagher, & Forgione, 2005). Our study identified intertwined barriers to breast cancer care at the policy-level, community-level, institutional-level, interpersonal-level and individual-level. The individual-level factors contributing to delay include a lack of awareness about the existence of and symptoms of breast cancer in the female population in Nigeria, which is consistent with previous studies in the general population in Southern Nigeria (Okobia, Bunker, Okonofua, & Osime, 2006). October is the designated breast cancer awareness month in Nigeria (Ugwu, 2013), but without a National Cancer Control Policy, awareness programmes are uncoordinated and do not appear to have effectively reached the entire female population. Many patients delayed seeking care because, despite identifying a breast mass, they did not associate it with the possibility of a serious illness. This finding is also consistent with studies of patients with a variety of cancers in the USA and Europe. A qualitative synthesis of 32 studies identified that recognition of symptoms, especially in the absence of pain, strongly influenced help-seeking behaviours and delays in help-seeking (Smith, Pope, & Botha, 2005). Furthermore, Nigerian women were unprepared for the types of treatment that would be recommended, especially surgery. Patients frequently described the surprise they felt when surgical treatment was recommended. This surprise suggests that fear of mastectomy does not have an impact on the initial healthcare-seeking because they were not aware that mastectomy was a common treatment modality. This is in contrast to previous work describing breast cancer in Nigeria which suggested that fear of mastectomy had an impact on stage of disease at diagnosis (Adesunkanmi et al., 2006). Nevertheless, our patient interviews indicate that fear of mastectomy surgery was a significant barrier to appropriate treatment. Of additional concern is a previous study in Northern Nigeria that demonstrated significant negative social consequences for women who underwent mastectomy (Odigie et al., 2010). Our interviews revealed that family members played an important role in delaying or encouraging surgery, which shows that care decisions have complex interpersonal dimensions. Another individual-level barrier discussed is alternative care. Previous work has frequently placed patients’ alternative healthcare-seeking behaviours at the centre of the causes of delayed breast cancer diagnosis in Nigeria (Anyanwu et al., 2011). A previous study of complementary and alternative medicine (CAM) use by cancer patients in Nigeria put usage of CAM at nearly two-thirds of patients (Ezeome & Anarado, 2007). This suggests that patients in our study may have been reluctant to disclose alternative treatment usage in the context of a recorded interview; this view was endorsed by the physicians interviewed. It is also possible that women who use CAM primarily never present to a tertiary medical centre. A much more common narrative than CAM use was accessing the orthodox medical system with a non-physician healthcare worker as the primary point of care. Multiple patients told stories of being treated improperly for months to years by these practitioners before being referred, if at all, for diagnosis and treatment at a larger medical centre. This shows the importance of addressing community and institutional-level barriers as well as individual-level barriers. Several previous studies in Nigeria have indicated that professional women’s knowledge about the disease is limited, even among well-educated women such as nurses and teachers (Akhigbe & Omuemu, 2009; Odusanya, 2001; Odusanya & Tayo, 2001). However, little more has been done to explore the knowledge
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and awareness level of community-based rather than hospital-based male or female healthcare providers. Institutional and policy-level delays within the healthcare system contribute to delays in care at both the level of diagnosis and the level of treatment. Patients were turned away from hospitals due to strikes and dysfunctional treatment equipment, or had to wait months for a test result or an appointment for surgery. In recent years, strikes by physicians, over working conditions, and enumeration have become more frequent and have had significant effects on the ability of hospitals to treat patients (Akinyemi & Atilola, 2013; Umukoro, 2012). Because the healthcare system relies mainly on out-ofpocket payments, ability to pay also played a significant role. Clearly in order to develop a streamlined system of care, these barriers, as well as patient behaviours and attitudes, will have to be addressed. Our interviews show that patients primarily knew women who had died of breast cancer, and there are very few examples of famous Nigerian women who have had breast cancer and even fewer who have survived. The one famous Nigerian mentioned by multiple interviewees as having had breast cancer, actually died from ovarian cancer (Okanlawon, Fabiyi, & Falola, 2009). In the USA, the openness of famous women about their diagnosis of breast cancer and their survival, is often referenced as a turning point in the culture and awareness of breast cancer (Olson, 2002). One can imagine prominent survivors in Nigeria would help change community-level perceptions of the fatality of the disease and the need to keep the disease secret. Multiple patients admitted that by maintaining secrecy about their diagnosis they reduced their financial and social support. Strengths and limitations of the study Despite recruiting patients from a single tertiary care centre, the patients recruited represented a wide geographic range across southern Nigerian. Because of the geographic diversity of our patient sample, this study is generalisable to women who live in big cities across Southern Nigeria, however, given the diversity of ethnic groups within Nigeria it is difficult to generalise further. A broad spectrum of educational backgrounds was represented as well as a significant range of ages. Both major religions in the area were also present. Information about the social class based on income of the women was not ascertained because many participants were informally employed and there was resistance to disclosing one’s income during our interviews. Due to the location of recruitment, our study does not capture the experiences of patients who never make it to tertiary care for breast cancer treatment. Therefore, we know little about the barriers to care for women who are never formally diagnosed. The medical setting may also have reduced willingness to speak about CAM for fear of being judged by their physicians or the belief that such an admission might affect their treatment. Furthermore, follow-up questions were limited by the use of a translator.
Conclusions Our interviews show that it is important to understand not only healthcare-seeking behaviours but also institutional- and system-level barriers to find critical points of contact with the healthcare system as targets for education. Making assumptions or generalisations about the patterns of care for a particular ailment may lead researchers away from productive avenues for education and improvement in care. While the use of alternative therapies may represent a significant delay that was not captured here, based
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on these data, understanding delays within the biomedical system appears to be more significant and easier to target for improvement. Community healthcare workers, such as pharmacists, play an important role in healthcare-seeking behaviours. Understanding patterns of healthcare-seeking behaviours in women more broadly is needed to better understand the areas in which healthcare education may be most effective. It is also necessary to understand the level of awareness and knowledge of breast cancer among community healthcare practitioners. This is a group of educated individuals who may be able to have a large impact by reaching multiple women for every healthcare worker educated. They could also refer women more quickly to hospital facilities with the resources to provide high quality care. While undertaking an American-style screening programme for breast cancer that relies on mammography is not feasible in a low-income setting, clinical down-staging of the disease remains a realistic goal (Corbex, Burton, & Sancho-Garnier, 2012). Training of new community healthcare workers in low-income settings in sub-Saharan Africa specifically to screen women for breast cancer has proven effective (Abuidris et al., 2013). This study raises the possibility that a modified version of this type of model, which here may involve the education of existing healthcare workers, should be explored in Nigeria. Lastly, cancer care is multidisciplinary and expensive in any health system. The strength of a health system can be judged by the outcomes in managing chronic diseases such as cancer. Women are now surviving long enough to develop breast cancer without the necessary health infrastructure to support their care. Nigeria has a gross domestic product per capita of $2800 (Central Intelligence Agency, 2013), but the Nigerian healthcare system has been underfunded for decades. Given the recent emergence of Nigeria as the leading economy in Africa, the time is ripe for the country to implement a National Cancer Control Plan and invest in evidence-based and cost-effective interventions at multiple levels to reduce the burden of breast cancer. Even if healthcare providers at the community and/or primary care level promptly refer breast cancer patients for tertiary care, without access to high functioning hospitals to improve surgical outcomes, women will remain fearful of surgery. The Nigerian Government has endorsed health insurance schemes to cover catastrophic illnesses like cancer as a priority area for future investments in health care. Breast and cervical cancer demonstration projects can be used to integrate women’s health beyond provision of reproductive services. References Abuidris, D. O., Elsheikh, A., Ali, M., Musa, H., Elgaili, E., Ahmed, A. O., … Mojammed, S. I. (2013). Breast-cancer screening with trained volunteers in a rural area of Sudan: A pilot study. Lancet Oncology, 14, 363–370. doi:10.1016/S1470-2045(12)70583-1 Adebamowo, C. A., Ogundiran, T. O., Adenipekun, A. A., Oyesegun, R. A., Campbell, O. B., Akang, E. E., … Olopade, O. I. (2003). Obesity and height in urban Nigerian women with breast cancer. Annals of Epidemiology, 13, 455–461. doi:10.1016/S1047-2797(02)00426-X Adesunkanmi, A. R. K., Lawal, O. O., Adelusola, K. A., & Durosimi, M. A. (2006). The severity, outcome and challenges of breast cancer in Nigeria. The Breast, 15, 399–409. doi:10.1016/j. breast.2005.06.008 Akhigbe, A. O., & Omuemu, V. O. (2009). Knowledge, attitudes and practice of breast cancer screening among female health workers in a Nigerian urban city. BMC Cancer, 9, 203–212. doi:10.1186/1471-2407-9-203 Akinyemi, O., & Atilola, O. (2013). Nigerian resident doctors on strike: Insights from and policy implications of job satisfaction among resident doctors in a Nigerian teaching hospital. The International Journal of Health Planning and Management, 28, e46–e61. doi:10.1002/hpm.2141
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