Background
In Uganda and most low- and middle-income countries (LMICs), there are no organized population-based cervical screening programs, largely due to financial and human resource restraints [
1,
2]. Consequently, cervical cancer patients in low- and middle–income countries (LMIC) report late for medical care [
3-
5], experience less treatment benefits and have poor survival [
6,
7]. Little is known about the reasons why cancer patients present to healthcare at a later stage in the LMICs than the high-income countries (HICs). In our recent Ugandan interview study, healthcare professionals suggested that advanced stage at diagnosis could be related to many challenges including patient factors such as inadequate awareness about cervical cancer symptoms, and healthcare factors such as inadequate skills to diagnose cervical cancer, inaccessibility of primary and secondary healthcare facilities, and a lack of specialized clinicians including pathologists and gynaecological oncologists [
8].
Analysis of national survey data on common cancers in the UK showed that patient and primary care intervals (defined respectively as the time from the patient first noticing a symptom, to presenting to primary care, and the time from then to being referred to a specialist) were much longer than referral and secondary care intervals (the time from being referred to being diagnosed) [
9]. In a qualitative study set in Australia, rural cancer patients delayed seeking healthcare because of long distances to health facilities [
10]. These findings suggest a need to better understand the patient and primary care intervals in order to design interventions for prompt healthcare seeking and diagnosis. However, transferring findings from studies in the HICs to the LMICs needs be done with caution because of the contextual differences between the healthcare systems of the HICs and LMICs. And yet in Uganda and most sub-Saharan African countries, there are few data from qualitative studies assessing the help-seeking process for cervical cancer [
11,
12].
Qualitative studies, particularly when guided by theoretical models, can provide useful insights into patient views, and guide interventions on help-seeking for cancers and other conditions [
13,
14].The Andersen model has been a fairly widely used theoretical approach which posits that patients go through a number of stages, referred to as delays, when they experience persistent and or worsening bodily sensations or symptoms [
15,
16]. The Andersen model was recently reviewed for its application to cancer studies, and refined into the Model of Pathways to Treatment [
16,
17]. This model proposes that an individual’s route through symptom appraisal and help-seeking is a nonlinear, iterative process with definable events, intervals (appraisal, help-seeking, diagnostic, and pre-treatment) and processes [
16,
17].
This study aimed to explore the process of symptom appraisal and help-seeking for symptoms of cervical cancer in Uganda using the Model of Pathways to Treatment as a framework for analysis. Understanding the patient journey to presentation along the pathway to diagnosis and treatment of cervical cancer can allow the identification of the critical intervals and barriers within the pathway, elucidate the nature of the barriers, and inform targeted interventions to minimize such barriers and improve timely presentation and diagnosis of symptomatic cervical cancer.
Methods
Design
An interview-based, qualitative design was chosen because it provided us an opportunity to explore cervical cancer patients’ symptoms experiences, and gain detailed understanding about their symptom-appraisal and help-seeking [
18,
19].
Setting
Patients attending care at a private-not-for-profit (PNFP) and a public Regional Referral Hospital, both in Gulu, northern Uganda.
Recruitment
Cervical cancer patients diagnosed within three months and attending care in the gynaecology clinics and wards were recruited to take part in a survey to determine stage distribution and factors associated with advanced stage cervical cancer. Patients were approached by the research nurse assistant, after clinical diagnosis of cervical cancer and during in-patient admission for examination under anaesthesia (EUA) and histological confirmation. The nurse was trained in aspects of the study including objectives, recruitment and consent procedures, and basic facts about cervical cancer including prevention methods, risk factors, symptoms and treatment modalities. The date of the EUA for diagnosis and staging of cervical cancer provided the date of diagnosis. Among women identified via a survey as willing to be interviewed, we purposively sampled patients who were not too unwell (as determined by the research assistant in consultation with the attending gynaecologists) to participate in an interview and who spoke the local language. Other exclusion criteria included asymptomatic patients identified with suspected cervical cancer through screening, and patients who had disabilities making communication difficult such as hearing and speech problems or a clinical diagnosis of a mental illness. We recruited in two phases. The first phase lasted six weeks and started at the beginning of the survey in August 2012. Ten patients completed the survey during this time period, nine spoke the local language, and we interviewed six of these nine patients. The data collected from these first six patients were transcribed, translated and analysis started to identify emerging themes. We also sought to identify deviant or disconfirming cases to inform further data collection. The second phase of data collection was undertaken from May 2013 for 8 weeks. The same purposive sampling approach was used, and among the 24 patients who completed the survey during this time period, 23 were identified as speaking the local language, of whom12 agreed to be interviewed. As the preliminary analysis suggested that two participants who were aware of their HIV positive status attributed their initial symptoms differently and undertook a different help-seeking pathway from the other women, they were considered deviant cases. In the second phase one further HIV positive participant was interviewed; no new themes emerged, therefore we considered that we had achieved saturation of data and were able to stop recruitment at that point.
Interview guide
An interview guide was used to aid data collection (Table
1). The development of the guide was informed by the constructs in the General Model of Total Patient Delay [
20]. It included items on recognition and appraisal of symptoms, durations and causal attributions of symptoms, immediate actions taken to deal with symptoms, where care was sought and why, people consulted, triggers for help-seeking, intervals between various actions taken, and items on perceptions about cervical cancer causes, group at risk, personal perceived risk for cervical cancer, and perceptions of treatment practices and outcomes. The guide was developed in English then translated to Acholi, the local language widely spoken in the study area. Two people (a social scientist and an educationist) independently performed the translations. The two Acholi versions were discussed and merged into one document which was back translated into English to evaluate accuracy in translation and preserve conceptual equivalence. The guide was refined accordingly before translation back into Acholi.
Table 1
In-depth interview guide
1. Disease labelling and symptoms; Appraisal stage
| (a) Please tell me about the illness you have which is now known to be cervical cancer. | (i) What were the first symptoms at onset of the illness? |
| (b) What did the symptoms mean to you? | (i) Did the symptoms mean a serious disease or just some common disease that did not require immediate action? |
| (c) What did you do when you recognized these symptoms? | (i) Did you talk to somebody about your symptoms? |
| | (ii) Who were these others you consulted? |
| | (iii) What were you told about the symptoms in terms of causes, consequences and management? |
2. Considered consequences of the disease; Illness stage
| (a) What made you feel that you needed to seek care out of your home? | (i) Where did you first go to seek care with these symptoms? |
| | (ii) Why did you go there? |
| | (iii) Where else did you go for treatment? |
| (b) How was the decision made? | (i) Who were involved in the decision making process on seeking care? |
| | (ii) What were considered? – including severity, availability of money, previous experience with the disease. |
3. Behavioural stage
| (a) From the time you recognized that the symptoms were serious enough and needed visiting a health worker | (i) How long did you take to go to the hospital? |
| | (ii) Why did you take the time you took? |
| (b) Were you referred to this hospital? How long did it take you to come to this hospital from that time of referral? | |
| (c) Why did it take you that time? | |
4. Diagnostic stage
| (a) When you came to this hospital, how long did it take to have the result of the test for cancer back? | |
| (b) Why did it take the time it took for you to receive the result? | |
5. Curability; Treatment stage
| (a) After receiving your cancer result, how long did it take you to receive the needed treatment? | (i) Tell us the time in days or weeks or months that passed from time you got cancer result to time when you got treatment you think was for treating the cancer itself. |
| (b) Do you think that this kind of cancer can get cured? | (i) If you think it can get cured (or cannot cure), why do you think so? |
Interviews
Fourteen interviews were conducted by ADM with the help of two trained research assistants. At each interview, there were two people – the interviewer and an assistant who made field notes and operated a digital audio-recorder. The research assistants are university graduates with experiences in social sciences research and HIV patient counselling. Each research assistant also conducted two interviews; both had also participated in the translation and pretesting of the interview guide. Interviews lasted between 45 and 90 minutes. During the interviews participants’ recall of significant dates such as onset of symptoms and timing of their decision to seek healthcare was helped by the use of significant landmark events [
21] including Christmas, Easter, independence day, onset of the civil war and encampment, the date of other co-morbidities such as HIV diagnosis and start of antiretroviral therapy, dates of births of children or first born, and dates of presidential elections.
All interviews began with an open-ended question, “Please tell me about the illness you have which is now known to be cervical cancer”; followed by prompt questions, “What were the first symptoms, when did the first symptoms start, what did you think was causing the problem and what have you done about the symptoms since onset up to the time you came to this hospital?” Participants were allowed to discuss their experiences without interference. The interview guide was used to facilitate the discussions for all patients. Detailed field notes and audio recordings were used to ensure capture of both verbal and non-verbal aspects of the interviews. All interviews were undertaken in a quiet room within the hospital premises. Interviews were completed within three months of the diagnosis of cervical cancer, and the majority of participants were interviewed in Luo/Acholi. Participants’ cross-checking and repeat interviews were not done. However, during the interviews, responses provided were summarized and read back to participants who confirmed or amended responses at the end of each section in the guide.
Interviews continued until the 18th patient when concurrent analysis revealed that data saturation had been reached and there were no new themes emerging [
22].
Data analysis
Transcription and analysis was an iterative process, starting after the first four interviews and continuing throughout data collection. Field notes and recorded interviews were transcribed and translated verbatim into English by the male research assistant who was present at 16 of the 18 interviews. All transcripts were reviewed against audio recordings by ADM (conversant with local language and English) to ensure accuracy in data capture, transcription and translation. The English versions of the transcripts were then read several times by ADM and ESO to gain familiarity with the data before they independently developed codes. A codebook for analysis was developed through consensus in a meeting between ADM and ESO. Data were analyzed using thematic analysis technique [
23,
24] with the aid of ATLAS.ti v6.1 software. Sub-themes and themes were agreed on through consensus in a series of meetings between the authors. ADM and ESO shared and revised the subthemes and themes with the research assistants in a one-day meeting to ensure that themes contained all the important issues expressed during interviews. Further data collection and analysis were informed by the themes from earlier interviews.
During data analysis and reporting we used the Model of Pathways to Treatment to provide the theoretical underpinning for the different intervals in the help-seeking trajectory [
16,
17]. We focused on the first two parts of the model; the appraisal interval which starts from the onset of symptoms to perceiving that one is ill and needs to visit a healthcare professional, and the help-seeking interval which starts from the decision to seek care to eventually visiting the healthcare professional. Total time to diagnosis comprise the time from appraisal through help-seeking to diagnosis of cancer. Intervals were calculated in months based on patient’s recall. Unfortunately exact dates of first visits to the peripheral primary care health professionals were difficult to recall accurately by patients and we could also not independently confirm, therefore total time to diagnosis rather than presentation is reported [
25]. Mid-months and mid-years were used as dates of events when necessary.
Throughout the Results section, representative verbatim quotes are referred to by the patient’s study number (1 – 18), total time to diagnosis in months and FIGO cancer stage.
Ethical approval
Makerere University School of Medicine Research & Ethics Committee (SOMREC) and the Uganda National Council of Science and Technology (UNCST) provided approval for this study. Further institutional approvals were provided by the institutional review committees (IRCs) of Lacor and Gulu hospitals. Written individual informed consents were obtained from participants before interviews. Verbal consents to audio record interviews were also obtained from each participant. We provided participants with modest amount of money not exceeding 5.0 USD in lieu of refreshments following interviews.
Discussion
This paper reports findings from one of the first studies exploring symptom appraisal and help-seeking for symptomatic cervical cancer among patients in the low-income sub-Saharan country, Uganda. There is evidence that help-seeking for some women with cervical cancer symptoms started immediately following symptom recognition and appraisal. More women had a longer time to presentation depending on; the nature of initial symptoms (onset, severity and persistence); the individual’s interpretations of the initial symptom/s and advice from lay people and family members; their perceived personal risk of cervical cancer; the existence of co-morbidities including HIV; and false reassurance from the primary care healthcare professionals first encountered. Our findings are consistent with evidence from high-income countries that help-seeking for illnesses depend on many factors including the individual’s social and cultural context [
15], and the health care system.
Abnormal vaginal bleeding (including post-menopausal and/or post-coital), vaginal discharge and lower abdominal pain were the most common first symptoms reported by participants. Although these symptoms are recognized symptoms of cervical cancer [
26], they also occur very commonly with other conditions including pelvic inflammatory diseases (PID) [
27] and sexually transmitted diseases [
28]. Failure to recognize the seriousness of symptoms, or attributing symptoms to other more common conditions, has been shown to delay appropriate help-seeking for symptoms of other cancers in the UK [
29,
30]. Furthermore, prompt recognition of potential cancer symptoms is associated with earlier diagnosis of breast, colorectal and lung cancers in the UK [
31].
The majority of participants attributed initial symptoms of vaginal discharge and itching to STDs including syphilis and/or gonorrhoea. The availability of plausible alternative explanations for symptoms prolonged the participants’ appraisal and help-seeking intervals. Furthermore, some participants had delayed diagnoses due to long-term treatment of these STDs. As cervical cancer symptoms occur in the pelvic region, participants may have attributed their symptoms as STDs; even more, they may have assumed that cervical cancer could be treated with the same regimens they have used for self-management of STDs. Once symptoms are interpreted as STDs, delay in help-seeking may be even longer because STDs have generally been stigmatized in most communities including Uganda [
32,
33]. Again, this suggests the importance of cancer symptom awareness campaigns and interventions to reduce stigma and discriminations associated with illnesses.
Cervical cancer awareness campaigns also need to promote prompt healthcare seeking among women with any gynaecological symptoms to allow early detection of cervical cancer. When STDs are common, they may occur concurrently with cervical cancer and patients may not be aware of subtle symptoms changes. Some participants had long duration of symptoms, for example, participant P1 reported symptoms over 140 months. She was HIV positive and a widow. While she attributed all her symptoms to cervical cancer, it is possible that these symptoms were due to other genital infections such as Chlamydia that are common among HIV positive women [
34].
Participants who perceived their initial symptoms as not due to a serious disease, or whose symptoms were painless, intermittent or mild, were likely to take a longer time to seek professional care. These findings are similar to those found by Emery and colleagues who interviewed rural Western Australian patients soon after diagnosis with breast, lung, colorectal and prostate cancers [
10], and in the UK, where non-recognition of the seriousness of symptoms was the main patient-mediated factor that increased time to presentation for most cancers [
29]. Other factors we identified as influencing the help-seeking duration were the distance to the nearest hospital, lack of money for travels and care, presence of co-morbidities such as HIV/AIDS, and perceived personal risk to cervical cancer. Most participants who did not perceive personal risk for cervical cancer minimized their cervical cancer symptoms, delayed seeking healthcare, and decided their symptoms were due to common benign diagnoses. This is consistent with results from interview studies with people recently diagnosed with cancer in high-income countries such as rural Australia [
10], and the Netherlands [
35]. It is important to develop cancer symptom awareness campaigns that include risk factors for cervical cancer and the people at increased risk so that women can correctly attribute their own symptoms and appropriately seek healthcare.
We found that consultations with lay people and family members usually shortened time to professional help-seeking. Similarly, rural women who discussed their breast symptoms with lay colleagues presented within a shorter time interval in rural Australia [
10]. In the UK, it was reported that sanctioning of initial interpretations by significant others fostered immediate help-seeking while keeping silent about symptoms, either because of low expectations of inputs from lay colleagues, or fear of people talking about their symptoms, delayed professional health seeking [
29]. Targeted health messages should aim to reduce perceived self-stigma associated with cervical cancer symptoms and STDs so that women may freely discuss their symptoms with family members and friends, and get encouragement by peers to seek appropriate care promptly.
The symptoms that triggered prompt help-seeking were severe abdominal pain, heavy vaginal bleeding, and/or excessive foul smelling vaginal discharges. These symptoms probably cause reasonable perceived threat to life and thus compel patients to seek healthcare as articulated in the health belief model [
36]. The one participant who attributed her initial symptoms to cervical cancer also sought professional healthcare promptly. However, in a substantial minority of participants, women had prolonged diagnostic journeys despite recognizing the seriousness of their symptoms and seeking help promptly. An example was P5 (39 months, 2B) who sought care at an established health facility within one week of noting her first symptom but took more than 3 years to receive her diagnosis. Such a long diagnostic interval raises concern about the need to augment healthcare professional training around the recognition of common cancer symptoms including those for cervical cancer.
Strengths and limitations
The main strength of this study is the use of validated theoretical models to underpin the data collection - the General Model of Total Patient Delay- and data analysis - the Model of Pathways to Treatment. The use of semi-structured interviews enabled patients to speak freely about their illness experiences from onset to diagnosis. Conducting interviews within three months of diagnosis is likely to have minimized recall bias.
The study is limited by use of retrospective recall to determine the exact dates of symptoms onset and decision to seek medical help. It was often difficult for the participants to accurately report the timing of their symptoms, or whether symptoms were actually due to cervical cancer. Misattribution of many different earlier symptoms may occur when the symptoms are common and shared by many diseases, and/or when the symptoms are chronic and long-standing [
25]. However, in a qualitative study such as this, the inability to accurately determine the length of the appraisal, help-seeking and diagnostic intervals does not affect the value of patient perceptions about the help-seeking journey. Other potential sources of bias included the male gender of ADM and one of the research assistants, participation bias by more motivated patients and interpretations based on previous experiences. The female research assistant was involved to temper the effect of male interviewers while interpretative bias was minimized by discussion of themes by the authors who have different training, experiences and research backgrounds.
Clinical and research implications
Our findings have important implications for care, research and policy. Regarding improvement in care, it is crucial to encourage women to seek professional help once self-help has failed to relieve symptoms. It is concerning that vaginal bleeding starting more than one year after previous menstrual bleeding were trivialized; rather than recognizing as a symptom of disease, post-menopausal bleeding was considered either as a restart of menstruation or something not serious. This may suggest a lack of awareness of menstrual cycle, meaning of menopause, and symptoms of cervical cancer. Interventions to create and /or increase community awareness about menstruation, normal and abnormal menopausal changes, and symptoms of cervical cancer may serve to avert prolonged delays to diagnosis resulting from alternative benign explanations or trivializations of symptoms of cancer. In the UK, general practitioners recognized the need to increase women’s awareness of gynaecological symptoms as a way of promoting prompt help-seeking [
37]. There is also evidence from LMICs that creating public awareness about cancer improves early diagnosis of cervical cancer with women presenting with more early stage disease in the intervention areas [
38-
40].
The Ugandan healthcare system comprises several layers of expert training but it appears that some healthcare professionals at the lower level of training may also have clinical challenges in detecting symptoms and signs of cervical cancer, and referring appropriately for definitive diagnosis. In this study most participants visited the lower level healthcare facilities several times before eventually getting referral to the study hospitals. Similar findings of healthcare professionals accounting for delay in diagnosis and/or referral were reported in a South Africa study [
12]. Both studies support the call for appropriate training of these lower level healthcare professionals to identify potential symptoms and signs of cervical cancer, acquire clinical techniques to diagnose cervical cancer, and/or promptly refer patients with symptoms suggestive of cervical cancer to centres where diagnostic capabilities exist.
Interventions such as further education for healthcare professionals have been shown to contribute to down-staging of cancers and are affordable especially where population based screening are not available [
41]. Further researches to assess the clinical and cost effectiveness of down-staging through enhanced education is needed in the sub Saharan African countries where there is high incidence of cervical cancer. If found applicable, then it could be important for policymakers in the LMICs to further adopt such measures to increase the proportion of invasive cancers diagnosed at early stages.
With regards to further evidence needed from research, quantitative studies to accurately determine appraisal, help-seeking and diagnostic intervals using validated models, and to compare the respective intervals with cancer stage at diagnosis, is needed in the LMICs. These would provide evidence for policymakers on promoting awareness for symptoms of cervical and other cancers. These would also provide further evidence to underpin programmed further training and education for healthcare professionals, particularly in the lower level healthcare facilities in Uganda.
Conclusions
Cervical cancer patients present with symptoms that are frequently attributed to normal bodily changes or common illnesses including sexually transmitted diseases. Lay consultations with family and community members tend to encourage self-management and early help-seeking, while not disclosing symptoms may delay help-seeking. Awareness campaigns to increase awareness of cervical cancer symptoms at population level, and educational programs for healthcare professionals, may help to improve early symptom recognition and timely help-seeking and diagnosis among people with symptoms suspicious of cervical cancer.
Our study is one of the first such studies from a LMIC, and contributes evidence to the key factors that influence symptoms recognition, interpretation and appraisal, and professional help-seeking for symptoms of cervical cancer in a low-income country.
Acknowledgements
The authors would like to thank all the patients who volunteered and shared their personal experiences of cancer symptoms that became invaluable data for this study. The authors are grateful to the research assistants, Willy Olango and Arach Jesca for diligently interviewing the patients and transcribing interviews. Authors acknowledge the advice of Prof. Martin Roland, Dr. Georgios Laratzopoulos, Assoc. Prof. Elizeus Rutebemberwa and Dr. Juliet Kiguli during study design and conduct.
Competing interest
The authors declare that they have no competing interest.
Authors’ contributions
ADM led study design, data collection, analysis and drafting of manuscript. ESO participated in study design and data analysis. HW participated in the study design and critical review of manuscript. FMW participated in data analysis and reviewed manuscript for coherence and important intellectual content. All authors read and approved the final manuscript and agreed on its submission.
ADM is a clinical oncologist and a lecturer at the School of Medicine, College of Health Sciences, Makerere University. OSE is Senior Lecturer and Medical Anthropologist at the Department of Psychiatry, School of Medicine, Makerere University. HW is a Professor of Pathology at Department of Pathology, School of Biomedical Sciences, College of Health Sciences, Makerere University and Director, Kampala Cancer Registry. FMW is a GP and Clinician Scientist at The Primary Care Unit, Department of Public Health & Primary Care, University of Cambridge, UK.