A total of 14,184 studies were identified by the literature search. After exclusion of duplicate studies and studies outside the scope of our review, only 67 studies were retrieved for full-text review. A total of 28 studies were eligible for inclusion in the review (Figure 1).
1. Study characteristics
The main characteristics of the included studies are summarized in Table 1. Among the 28 studies included in the review, 11 were quantitative, 12 were qualitative, and five were studies with mixed methods (quantitative and qualitative approaches). They were conducted across 13 countries in sub-Saharan Africa. Thirteen (46%) studies were conducted in East Africa, 10 (35%) in West Africa, 3 (10%) were conducted in Southern Africa and 2 (7%) were multi-country studies mixing countries from three parts of sub-Saharan Africa (East, West and southern Africa). The study publication dates ranged from 2013 to 2020. The sample sizes of the studies ranged from 64 to 1429 for the quantitative and mixed studies. Eleven (69%) quantitative and mixed studies were cross-sectional surveys, while three were cohort studies. The qualitative articles used focus group discussions and in-depth interviews to explore different factors influencing treatment time in breast cancer patients. In 21 (75%) studies, their study populations exclusively included women with breast cancer, whether newly diagnosed or not, whereas the seven other studies included physicians, health care workers, family members and women without breast cancer. The average (mean/median) age of the women with breast cancer was 40 and over in the large majority of studies.
2. Factors influencing time to treatment in breast cancer patients
There were a total of 36 barriers and eight facilitators identified across all studies. Factors identified in each study and classified according to the WHO Health Systems Framework’s six building blocks are summarized in Table 2 and Table 3, respectively. Among the barriers, misdiagnosis was the most common (16 studies), followed by provider attitude (11 studies) and the high cost of investigation and treatment (11 studies). The appearances of other barriers and facilitators ranged from one to seven times.
Health service delivery
Health service delivery was addressed by 23 of the studies included in the review, and the factors identified can be grouped into two major themes: logistic and infrastructure.
Logistical difficulties included different waiting times for an appointment (medical or specialist consultation), investigations (imaging, biopsy), test results, referral or treatment (surgery, radiotherapy) [23–31]. A long waiting time for test results, more specifically for the biopsy results, was a factor influencing the time to treatment in 11 included studies [24, 26–30, 32–36]. Seven included studies reported that referral was delayed for women who had visited other health facilities 1 to 4 times or more before visiting the diagnostic centre [23, 24, 30, 36–39]. In one of these studies, for instance, more than 80% of 499 patients had at least 3 visits before diagnosis, and repeat visits in the referral system appear to have been caused by misdiagnosis and delays in appointments and test results . Pace et al. found that patients who visited other healthcare facilities ≥5 times before diagnosis were more likely to experience system delays of ≥6 months (OR, 2.69; 95% CI, 1.24–5.84; p = 0.01) . Studies have also shown that the type of healthcare facility and the type of health worker visited at the first consultation had an impact on diagnosis and treatment delays [39, 40], and women who first visited a community health centre or general practitioner experienced longer delays than those who first saw a specialist (surgeon or oncologist) [39, 40]. Being referred by an oncologist or surgeon or having received the first consult evaluation in a public hospital have been identified as factors facilitating diagnosis and access to treatment [39, 40]. Logistic problems also included poor organization and unavailability or shortage of breast cancer services [30, 31, 41].
The geographical inaccessibility of healthcare facilities and the insufficiency of diagnostic centres are part of the infrastructure problems [28–31, 41]. In Uganda, for instance, one patient interviewed said, ‘The health centre nearby the community does not offer screening services, and someone may find it hard to leave this place [Ssisa sub-county] to go to Kampala; but if they bring the services closer to the community, some will find it easier to visit them.’ [Semi-structured #2] .
Misdiagnosis, Misinterpretation and Mismanagement
Among health workforce factors, misdiagnosis was the most common and appeared in 16 studies [24, 25, 29, 30, 32, 34–36, 38–40, 42–46]. Patients reported being inappropriately reassured by health workers that their breast lump was benign without a biopsy or with an incorrect biopsy interpretation.
“… I noticed something, a small lump on my breast … I woke up in the morning and went to my doctor.He told me it could be a tumour.I asked him if it could be a cancer because I heard about it on TV.He told me it is not a cancer.” (P07)
Symptom misinterpretation and misdiagnosis were the most frequent reasons for prolongation of the primary care interval. In six studies, caregivers mismanaged breast cancer patients by giving incorrect medical prescriptions or incorrect advice [27, 28, 30, 36, 43, 44]. For instance, Pruitt et al. reported that the majority of women described receiving oral medication or injections, usually antibiotics, sometimes for months or years before being referred or making an independent decision to seek care elsewhere .
‘I went to the Referral Hospital in XXX. They gave me drugs which I took for 3 months. During that period, I did not see any amelioration…3 months later I went back to my doctor and he gave me other prescriptions for blood analyses…' (Patient 7).
Olayide Agodirin et al. found that the rate of long primary care intervals was higher among patients who received incorrect advice (81%, 44 of 54) than among those who received correct advice (67%, 100 of 148) (OR 2.1, 95% CI 1.0-4.6) .
Poor knowledge and skills
Misdiagnosis is often attributed to poor knowledge and lack of health workers training about breast cancer; most health workers provided incorrect information to patients [30, 32, 35, 41]. Some of them were unable to examine the patient appropriately . As an illustration, in one focus group, a health worker said: ‘For me, I have never gotten training on breast cancer detection but I just hear that breast cancer is very dangerous and it is good for someone to go for check-ups but I have never received training on breast cancer examination.’ [FGD CHWs #7] .
Attitude of health workers
The attitude of providers was also an important factor influencing women's access to treatment. Some studies reported that poor attitudes and corruption among health workers were factors that accounted for delays in the start of definitive treatment. Patients also said some health workers disrespect them, refused to answer their questions or did not treat them well, which forced them to delay the start of treatment , while others had good communication with health care providers, which made it easier for them to manage their breast cancer .
Strikes and shortage of caregivers
The shortage of health workers and strikes were also identified as factors delaying women's access to breast cancer treatment [25, 27, 28, 32, 36, 42, 44]. Studies have reported that various hospital departments turned women away because a doctor was not available . 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 .
Six key elements were identified among financing-related factors: high costs of treatment and investigations, lack of insurance or limited insurance coverage, expensive private insurance and discrimination by private insurance. The high cost of treatment was reported as an important factor influencing women's access to breast cancer treatment in 11 studies [27–31, 38, 46–50]. One woman in the study reported by Sanuade et al. said, ‘The chemo is expensive. The trauma and money you spend is a problem too. If you do not have at least 200 Ghana cedis, you cannot buy the drugs. When someone hears all this, the individual would opt for herbal medicine or prayer. So, as for me, I think that lack of money is a factor. I paid 1000 Ghana cedis to use the chemo machine. If you do not have money you would go home. So, money is a serious factor.’’ (FGD 4-R1) .
Lack of or limited insurance coverage was also mentioned as a barrier to care. In the study conducted by Subramanian et al. in Kenya, 78% out of 400 women with breast cancer reported borrowing money from family or friends to cover out-of-pocket medical and related expenses . In another study conducted in the Ivory Coast, 36% out of 126 patients declared having had a delayed diagnosis due to lack of financial resources . Many women reported having no insurance coverage [47–49]. For instance, Okoronkwo et al. found that 71.8% out of 194 patients studied in Nigeria did not have health insurance coverage .
Medication access and technologies
Unavailability of drugs and equipment failure were the most common factors among those related to medication access and technologies [28, 30, 32, 44, 46, 47]. Diagnostic assessments were not available in small health centres, and multiple visits were required for X-rays or blood tests or to obtain a biopsy sample, according to interviewees. Various hospital departments turned women away because the computer was broken or the X-ray machine was not working [28, 30, 32]. Study results also identified drug shortages as an important factor in treatment delay [32, 44, 46].
For instance, key informants in one study conducted in Uganda reported that the existing health system is not equipped to manage breast cancer .
Leadership and Governance
Lack of cancer policy, low prioritization of non-communicable diseases, and lack of provider training on breast cancer were the common factors identified in the included studies . Key informants in one study conducted in Uganda highlighted the lack of cancer policy-providing guidelines for cancer management across each spectrum of the cancer care continuum .
‘There is no such policy on cancer screening or cancer prevention; there’s nothing like that.’ [key Informant #6] .
The information system was addressed by only one study among those included in the review . The key factor identified was the delay in administrative procedures. In this study, conducted in Rwanda, 27% out of 113 women interviewed said that, to receive public insurance coverage for care provided at a district hospital, a referral form from a health centre was required. Many patients described the need for a transfer form as a reason for the delay.
3. Quality appraisal of the included studies
The majority of the quantitative studies were rated as good quality based on the NIH study quality assessment tools for Observational Cohort and Cross-Sectional Studies (Supplementary data, Table S1). Most qualitative studies were of high quality on the CASP checklists (Supplementary data, Table S2). There were no low-quality among studies. Based on the four components (methodological limitations, relevance, adequacy, and coherence) of the CERQual approach, the confidence in the evidence for most of the qualitative findings (16 of 21) was rated as low. (Supplementary data, Table S3).