Delays in presentation, diagnosis, and treatment in Sudanese women with breast cancer: a cross-sectional study

Abstract Background The poor prognosis of breast cancer in Sudan could be due to delayed treatment and diagnosis at an advanced stage. Our study aimed to assess the extent of delays from onset of symptoms to treatment in Sudanese women with breast cancer, as well as identify factors contributing to these delays. Materials and Methods We conducted a multi-center cross sectional study between March and April 2023. Data were collected from the medical records and interviews with women with breast cancer in the two main oncology centers in Sudan. Linear regression was used to identify the predictors of delayed presentation. Results We interviewed 601 women with breast cancer. The majority of women (50.1%) were diagnosed at locally advanced or metastatic disease. The median interval from the onset of symptoms to receiving oncologic treatment was 221 days (IQR = 92, 496). The longest delay was the presentation delay 61 (31 244) days. The median duration for diagnosis delay and treatment delay was 21 (10.57) days and 27 (10.64) days, respectively. Predictors of early presentation included, being young (β = −5.3; 95% CI = 0.06 to 10), married (β = −264; 95% CI = −427 to −101), divorced (β = −306; 95% CI = −549 to −63), or widowed (β = −320; 95% CI = −-543 to −97), urban residence (β = −107; 95% CI = −213 to −2.3), and seeking traditional healer (β = −204; 95% CI = −383 to −26). Conclusion Most Sudanese women with breast cancer experience significant patient delays, often presenting at advanced stages. Factors like being single, older, and living in rural areas contribute to these delays. Increasing breast cancer education, improving healthcare access and addressing sociodemographic barriers can potentially expedite diagnosis and improve outcomes.


Introduction
Breast cancer is the most common cancer globally, with approximately 80% of deaths occurring in low-and middleincome countries (LMICs). 1 Its incidence rates in Sub-Saharan Africa are on the rise, driven by lifestyle transformations, urbanization, and reduced birth rates. 2,3The 5-year survival of breast cancer is more than 90% in high-income countries (HICs); however, it varies in African countries. 4In Uganda, it ranges from 35% to 50%, while in Mali it is <20%. 5In Sudan, breast cancer is the most common cancer with 5-year e772 The Oncologist, 2024, Vol. 29, No. 6 survival of 58%. 6Low survival rates in sub-Saharan Africa are largely attributable to late-stage at presentation. 3Women with breast cancer in Sudan and other African countries are more likely to be diagnosed at advanced stages compared to women in HICs. 7,8Up to two-thirds of women with breast cancer in Sudan were diagnosed with stage III or IV 6,[9][10][11] .Early diagnosis and treatment improve breast cancer survival 11 ; however, cultural beliefs, cancer stigma and scarcity of screening and diagnostic services contribute to delayed diagnosis in Africa. 2 There is a lack of data on the extent of delays from onset of symptoms to treatment in Sudanese women with breast cancer, as well as factors contributing to these delays.The Identification these factors would improve early detection and survival rates.

Participants, study design and settings
We conducted a descriptive cross-sectional study including women with breast cancer treated between March and April 2023 at the two main cancer treatment hospitals in Sudan, Khartoum Oncology Hospital and the National Cancer Institute, that offer comprehensive care for cancer patients.

Data collection tool
A questionnaire was developed based on the study's objectives and scientific literature.It underwent a review by a panel of experts to ensure its validity and relevance.Suggestions for improvement were implemented.A pilot study involving 31 random patients with breast cancer was conducted to refine the questionnaire based on feedback received.The questionnaire comprises three sections: The sociodemographic information, breast cancer-related traits and the timing of presentation, diagnosis, treatment, and factors that may contribute to delayed intervals.Trained doctors interviewed patients using the Kobo-collect survey tool to ensure quality.Medical records were also reviewed for additional data.

Patient and system delay's definitions
Delay occurring in the context of cancer treatment can be categorized into two types: The presentation delay and health system delay.Presentation delay refers to the interval between the onset of symptoms and the initial medical consultation.Health system delay refers to the time between the first medical consultation and the initiation of cancer treatment.Health system delay can be further divided into diagnosis delay, which is the time between initial medical consultation and the histopathologic confirmation, and treatment delay, which is the time between the confirmation of the diagnosis and the initiation of oncologic treatment. 11

Statistical analysis
Data were analyzed using the R software version 4.2.2.The Krustal-Wallis test was used to assess the association between delays intervals and the stage and between the diagnosis interval and the type of healthcare personnel visited.A multiple linear regression analysis was used to test the association between presentation delay and different factors.Variables with a P-value < .25 in the univariate linear regression were included in the multiple linear regression models.A P-value of ≤ .05 was considered statistically significant.

Results
A total of 601 women with breast cancer gave consent and were interviewed.Table 1 shows characteristics of the study population.Most women had clinical stage III (39.3%), and 55.5 % initially consulted a general surgeon for their breast symptoms (Table 2).The majority (82.9%) stated they did not perform monthly breast self-examination (BSE).Additionally, 82% had limited awareness about the risk factors of breast cancer.However, 61.2% were aware that early treatment improves breast cancer cure rate.Almost all participants (98%) stated they noticed a problem in their breasts themselves (Table 2).The median duration of the overall delay was 221 days (IQR, 92-496).The longest delay was the presentation delay 61 (IQR, 31-244) days (Figure 1).The independent predictors of early presentation were being young, married, divorced, or widowed, urban residence, seeking traditional healer (Table 3).
The association between clinical stages and categories of delays is shown in Table 4.The only statistically significant difference was observed between the median the stages (P < .001),with stage 1 having the longest diagnosis interval (49 days), followed by stage 4 (34 days), then stage 2 (19 days) and stage 3 (19 days).
The healthcare personnel initially visited by the participants significantly affected the median diagnosis interval (P < .001).The longest median interval was 36 days for general practitioner/family doctor, while the shortest was 9 days for oncologists (Figure 2).
The frequently reported reasons for patients delay included underestimating breast symptoms and not considering the possibility of having breast cancer (31.6%), not being bothered by breast lesion (27.3%), lack of awareness about the availability of curative treatment for breast cancer (7%), lack of knowledge about cancer (7%), and misinterpreting symptoms due to previous history of benign breast condition (3%) (Supplementary Table S1).
The leading cause of delayed diagnosis was the failure of doctors to suspect cancer at initial consultation (7.5%).This was followed by delays in receiving biopsy results (4.7%), financial challenges (4.7%), and fear related to the receiving of a cancer diagnosis (4.7%) (Supplementary Table S2).Fear of undergoing cancer treatment was the main cause (14%) of delayed treatment, followed by financial challenges (5.2%) (Supplementary Table S3).

Discussion
Our findings show that the median interval between first discovery of breast symptoms and treatment initiation exceeded 18 months, which was long enough to lower the survival.The greatest delay occurred between symptom discovery and first presentation, with a median of 61 days.6][17] While cancer control programs typically aim for a patient delay of 30 or 14 days, 13,18 the absence of a national breast cancer screening program in Sudan makes achieving this goal challenging. 19The frequently reported reasons for patients delay in this study were underestimating breast symptoms, lacking awareness about breast cancer and misinterpreting symptoms.Similar reasons were reported in LMICs. 12his highlights the needs for early diagnosis approach focusing on the promotion of the awareness of early signs and symptoms among the public.We found that married women were more likely to seek medical care earlier than unmarried women, a finding that is in lines with a previous meta-analysis. 20We also observed that older women and those residing rural areas experienced significant longer delay in seeking medical care for breast symptoms, a trend that aligns with a study from Ethiopia. 21This delay be attributed to older women perceive breast changes as a normal postmenopausal phenomenon.These finding underscore the importance of breast cancer awareness campaigns, particularly for those at higher risk.The use of trained volunteers to conduct clinical breast examinations in rural area of Sudan has been proven to be a simple yet effective strategy for early symptoms detection. 22 our study, 98% of breast cancer cases were self-detected by the women, a figure slightly higher than the 90% reported in Ethiopia. 23This underscores the importance of BSE as a primary mechanism for breast cancer detection.However, only 17% of our study participants perform BSE monthly, a rate comparable to that reported across Africa. 24Therefore, it is vital to enhance women's practice of BSE by promoting early detection programs that focus on improving the technique and frequency of BSE.
In this study, women with breast abnormalities tend to seek medical help when they experience pain, similar to previous studies. 25,26It is important to note that pain may not be the only present symptom for breast cancer, rather the symptom drives patients to seek medical care.
The median duration for both diagnosis and treatment delays in this study was deemed satisfactory, falling within the recommended 1-month time frame. 18several factors contributed to these delays, including fear of cancer treatment, financial challenges, delays in receiving biopsy results and the social stigma associated with cancer diagnosis.Furthermore, limited access to mammography and image-guided biopsy is pose a barrier to early diagnosis in Sudan 19 .Misinterpretation of symptoms and misdiagnosis by doctors were also significant factors leading to prolonged intervals in Africa.We observed an association between health system delay and the medical specialty of the provider that was consulted, with the longest interval being for general practitioners.This is particularly relevant in resource-limited setting where the majority of patients first contact a general practitioner, who may not be familiar with breast cancer screening and diagnostic guidelines.Therefore, educating general practitioners and improving referral procedures are crucial to facilitate the early diagnosis and treatment of breast cancer.
Our study reveals an association between cancer stage and diagnosis interval, with the longest diagnostic delay observed in stage 1 compared to other stages.This delay in diagnosing small tumors could be attributed to the limited access to diagnostic services and specialized physicians. 19However, previous studies examining the associations between delay and tumor stage have yielded inconsistent results. 11,27his study focuses on the delay in the context of breast cancer management, a topic that has not been widely studied in LMICs.It took place in Sudan's two main cancer hospitals, making it a representative sample of Sudanese women with breast cancer.However, it is important to acknowledge the limitations of this study, including the potential for recall bias.

Conclusion
The majority of Sudanese women with breast cancer are receiving treatment at advanced stages after significant delays.The patient's delay plays a crucial role in this overall delay.Key predictors of this delay include being single, older, and residing in a rural area.There is a pressing need for more education on breast cancer, particularly for those at higher risk.Furthermore, enhancing access to healthcare services, especially in non-urban areas, and addressing sociodemographic barriers could potentially facilitate earlier diagnosis and improve outcomes.

Figure 1 .
Figure 1.Average intervals of presentation, diagnosis, and treatment.

Table 1 .
Sociodemographic characteristics of the study participants.

Table 2 .
Breast cancer-related characteristics of the study participants.

Table 3 .
Linear regression of socio-demographic data and breast cancer presentation interval.

Table 4 .
Median presentation, diagnosis, treatment, and overall intervals by UICC stage at time of diagnosis (N = 601).