Demographic Pattern, Tumor Size and Stage of Breast Cancer in Africa: A Meta-analysis

Abstract

Purpose: Understanding the epidemiology of breast cancer (BC) in Africa, as well as regional variation is essential for planning future intervention. Our objective was to describe summary estimates of socio-demographic and clinical characteristics of BC in Africa, thus providing researchers and policymakers baseline data for planning diagnostic and treatment programs to improve BC outcomes in the future.
Method: We screened African publications on BC between 2010 and 2019 in PubMed, AJOL, Google, ScienceDirect, and ResearchGate to estimate the distribution of socio-demographic and clinical tumor characteristics. The meta-analysis used the random effect model.
Result: Eighty articles were eligible, including 33,199 total patients. Overall, 58% of patients were <50 years old. In East Africa, 38% (95% CI 31-45) were diagnosed before 40 years. Conversely, in Southern Africa, 37% were diagnosed after 60 years, with Caucasian-like age distribution. The overall prevalence of male BC was high (3%), with East Africa having the highest prevalence (5% (95% CI 5.0-6.0)). Only 2% (95% CI 1-2) of patients were diagnosed with carcinoma-in-situ. Invasive tumors were 7% stage I, 26% stage II, 50% stage III, and 17% stage IV. Seventy per-cent (95% CI 60-80) had clinical nodal involvement. The smallest tumors were in North Africa. The largest and most advanced tumors were in West Africa. Trend analysis showed decreasing age, an increasing population of unmarried BC patients, a relatively high proportion of uneducated BC patients, and a stable proportion of late-stage disease in the last decade.
Conclusion: Regional variation in the presentation of BC throughout Africa necessitates region/country-specific targets for improving BC control. 

Introduction

According to 2018 global cancer statistics [1], breast cancer (BC) is one of the two most common adult cancers, accounting for nearly 25% of cancers in women worldwide. Africa has disproportionately high age-standardized mortality due to BC [2]. The World Health Organization (WHO) and other experts in the field [3] recommend early diagnosis combined with timely and effective treatment as cost-effective measures for improving BC outcomes in Africa. Understanding the epidemiology of BC in Africa, as well as regional variation, is essential for planning future interventions.

Prior researches have aggregated data to better understand BC in Africa, but there is a notable gap in the existing literature. Previous meta-analyses described BC incidence, stage at presentation [4], and biological characteristics in sub-Saharan Africa (SSA). However, none of the existing reviews adequately summarize patient demographics, clinical pattern, or regional variation of BC. These factors are of significant prognostic value and are critical determinants of resource allocation that can allow for tailored screening, early detection, diagnostic and treatment programs to be adapted for specific local or regional contexts.

This meta-analysis aims to describe summary estimates of patient demographics, tumor size, and BC stage in Africa. A secondary aim is to compare the clinical pattern between African regions and countries. Our ultimate goal is to provide researchers and policymakers a baseline and region-specific targets for planning future interventions.

Method

This research aligned with the Preferred Reported Items for Systematic Reviews and Meta-analysis (PRISMA) recommendations [5]. The needs assessment and preliminary literature review [in PubMed, African Journal Online (AJOL), Cochrane library, and Prospero reference ID CRD42020153269] confirmed no similar meta-analysis was ongoing or previously conducted. The full literature search was performed in PubMed.gov between November 10, 2019, and December 31, 2019, using an iterative process with the search term “breast cancer AND country name” for each African country and only as “breast cancer” in AJOL. Hand-search was done on Google, Google Scholar, ScienceDirect, PubMed central, ResearchGate, and Academia. Snow-balling search was in the reference list of original articles and already published review articles. We sent an exclusive request email to authors for full articles not available online or to clarify data.

Article screening and data extraction

Full-text screening used predetermined Population, Intervention, Control, Outcome, Time, Study design (PICOTS) criteria (Table 1).

Author AO performed the article title and abstract screening while AO and AI performed the full article review independently. The same authors also conducted data extraction. The authors discussed to resolve any disagreement.

Quality assessment

Five quality assessment variables were designed using domains in the Strengthening the Reporting of Observational Studies in Epidemiology (STROBE) checklist [6]. The quality assessment classified the report into one of 5 levels, A-E, depending on the quality score, with A being the highest score of five and E being a score of one or zero. The quality score was not used in meta-analytical weighing.

Statistical analysis

The primary outcome was the summary estimate of each outcome variable defined in our PICOTS criteria. The meta-analytical procedure was conducted in MetaXL (www.epigear.com) add-in for Microsoft Excel. A random-effect model was implemented to obtain summary estimates using the double arcsine transformation to avoid overweighting studies with values close to 0 or 100%. I-squared [I2] values above 75% indicated high heterogeneity. Subgroup analysis was conducted based on the United Nations regional classification of African nations as Central Africa (CA), East Africa (EA), Northern Africa (NA), West Africa (WA), and Southern Africa (SNA). By-country analysis was also conducted to compare variables and explain the potential source of heterogeneity. We analyzed summary estimates of all variables where there were at least two observations for the continent, the region, or the country. The variables were analyzed as proportions of the total in each publication (n/N).

Tumor characteristics according to the clinical or pathologic AJCC, were analyzed separately. Results were presented in percentages with 95% confidence intervals (95% CI). The parent forest plots for all analyses are available in the supplementary file. Funding: No funding source.

Results

Full electronic search returned 5661 articles; 80 articles were eligible after the article selection process (Figure 1, Table 2).

Figure 1. Article Screening Flow Chart.

Result of article request; Four authors contacted for full-text responded [42, 86-88] yielding one eligible article. One [54] of 20 authors [7, 12, 31, 32, 36, 40, 49, 54, 60-62, 64, 74, 75, 77, 89-93] contacted for data on age distribution responded. Three authors [30, 39, 61] could not be reached to clarify data on age distribution, two could not be reached for data on educational status [39, 94], and one could not be reached for data on time to presentation [94]. Five authors contacted for data on stage distribution did not respond [48, 58, 60, 64, 70], and one could not be reached [95]. Three authors could not be reached to clarify data on tumor stage [30, 39, 61]. Two authors contacted for data on tumor size did not respond. One [37] of four authors contacted for data on marital status [37, 40, 70, 75] responded with usable data and one could not be reached [31, 74, 95]. Regional representation and summary of design; Twenty-four countries were represented from all five regions of Africa; CA-6, EA-19, NA-13, SNA-7, and WA-35. Three publications were in french [14, 62, 83]; all others were in English. Abbreviations, CA- Central Africa; EA- East Africa; WA-West Africa; NA- North Africa; WA-West Africa; SNA- Southern Africa; udy, retro- retrospective study’ survey- questionnaire-based survey

Each article contributed data for one country except Sengal et al. [7], which provided data for Sudan and Eritrea in one article. Two articles from South Africa [8, 9], Sudan [7, 10], and Central African Republic [11, 12] shared the same population of subjects but provided different data points (Table 2). Attempts to clarify incomplete or obscured data via email communications with authors yielded variable results as detailed in Table 2 footnote.

Twenty-three countries from all five regions of Africa contributed articles. WA contributed the largest number of articles (35 articles), followed by EA-19, NA-13, SNA-7, and CA 6. Nigeria contributed 23 articles, the largest from a single country (Figure 2).

Figure 2. Map of Africa Showing the Distribution of Study Subjects from each Country. The deeper blue shading represents a higher contribution, and lighter blue shading represents a lower contribution. The gray shadings represent no contribution.

There were 33,199 subjects in total. The minimum number of subjects in a study was 42 [13], and the maximum was 3044 [14]. The maximum number of subjects from one country was 5425, contributed by Nigeria (Figure 2). The majority of studies (n=39) were in the B quality assessment category; the study rationale was well stated in 84%, the design was adequate in 85%, and the participants were adequately stated in all studies. The study outcomes were adequately described in 77%, but the ease of data extraction was present in only 36% (Supplementary File). There was marked heterogeneity (>75%) in the overall summary estimates of the continent- wide analysis. The heterogeneity was significantly reduced or eliminated in most by-region and by-country analyses (Supplementary File).

Sex distribution

Twenty-five articles, including 11,476 subjects, contributed to the analysis of sex distribution. Ninety-seven per-cent (95% CI 97-98, I2 77%) of patients were female and 3% (95% CI 2.0-4.0%, I2 77) were male. EA had prevalence of male BC at 5% (95% CI 2.0-476%), more than double the prevalence in WA (2% (95% CI 2.0-2.0, I2-80%). Regional analysis was not feasible for NA, CA and SNA. By-country analysis showed a similar distribution of 2-3% in Nigeria, Tanzania, Eritrea, and Ghana. Single studies reported 2% male prevalence in Cameroon [14] and South Africa [15]. A single study from Ethiopia recorded male BC prevalence of 18% [16]. Subgroup analysis showed a rising trend in male BC incidence in the last ten years compared to the decade before. (Supplementary file).

Age distribution

Thirty-three articles (14,545 subjects) contributed to age distribution analysis. Overall, more than half of patients (58%) were diagnosed before the age of 50. Twenty-eight per-cent of patients (95% CI 24-31) were diagnosed before the age of 40, and 6.0% (95% CI 5.0-8.0, I2=90%) were diagnosed at 30 years or younger. The youngest patients were in EA, where 8% (95%CI 6.0-11, I2=82%) were diagnosed under the age of 30, 38% (95% CI 31-45, I2=85%) were diagnosed under the age of 40, and 64% were diagnosed before the age of 50. Conversely, in SNA, over 60% were diagnosed at the age of 50 or above, and 37% (95% CI 35-39, I2=0%) were diagnosed at the age of 60 or above. The age distribution analysis was possible for NA only in the 50-year cutoff, showing that the majority were also younger than 50 years (58%, (95% CI 44-72, I2=94%). (Figure 3, Supplementary file)

Figure 3. Age of Breast Cancer Patients in Africa.

By-country analysis showed Ethiopia had the youngest patients with 10% (95% CI 8.0-13, I2=63%) being younger than 30 years and 73% (95% CI 61-80, I2=87%) younger than 50 years (Figure 3 and Supplementary File). Temporal analysis revealed declining age of BC patients over time. Sixty per-cent of patients from 2010-2019 were less than 50 years of age, compared to 55% in 2000-2010 period. Eight per-cent of patients were less than 30 years of age from 2010-2019 compared to 4% in the 2000-2010 period (Figure 2, Supplementary file). Overall, 57% (95% CI 54-61, I2 87%) of patients were premenopausal. This was similar throughout regions with available data (56-60%). By-country analysis showed that Ghana had the highest prevalence of premenopausal patients (64% (95 % CI 42-83, I2=92%)) (Supplementary file).

Educational and marital status

Eleven publications (3747 subjects) contributed to the marital status analysis. Overall, 61% were married and 39% were unmarried, including 20% single. One study from CA [12] reported the highest proportion (74%) of unmarried singles; sensitivity analysis excluding this study saw the proportion of singles overall drop to 15%. The regional distribution of single patients was 11% EA, 14% WA, and 24% SNA. The largest unmarried population was in South Africa (57%) while the smallest was in Nigeria (27%). The temporal trend showed a slight increase in unmarried women diagnosed with BC in the last decade (41%) compared to the period between 2000-2010 (35%) (Table 3). Twelve articles (3,103 subjects) contributed to the educational status analysis. Thirty-eight per-cent of patients had none or primary education, 36% completed secondary education, and 26% completed tertiary education overall. The proportion of patients with secondary or tertiary level education was highest in SNA (75%) than EA (62%) and WA (62%). The proportion of patients with secondary or tertiary level education in the last decade (64%) was slightly higher than the overall analysis (62%) (Table 3). Subgroup analysis for 2000-2010 was not feasible. However, a single study from Nigeria in the 2000-2010 period recorded 52% secondary and tertiary education [17], another study from Nigeria with data between 2010 and 2012 recorded 66%, [18], and a separate study in Uganda including data between 2010 and 2013 [19] recorded 62%. (Supplementary file).

Laterality

Eight articles (2,947 subjects) contributed to the analysis of BC laterality in the continent. Most patients (97%) had unilateral BC, compared to 3% (95% CI 2.0-6.0 I2=80%) who had bilateral BC. The highest prevalence of bilateral BC was in Nigeria, 8% (95% CI 6.0-12 ) [20] and Tanzania (6%, 95%CI 4-8) [21]. A slightly higher proportion (51% (95% CI 46-55) were left-sided tumors (Table 3).

Stage distribution

Fifteen articles (9,185) contributed to carcinoma-in- situ analysis. Prevalence of carcinoma in-situ was generally low in all regions (CA- 4%, EA-2%, and NA-1%, SNA, and WA-1%). The highest proportion of carcinoma-in-situ in individual publications was 6% reported in Central African Republic and 5% in Malawi.

Overall, 98% of BCs were invasive based on analysis of 30 articles (10,352 subjects). Advanced BC (AJCC stage III or IV) accounted for 67%. Overall, 7% (95% CI 4.0-9.0, I2= 98%) of patients were diagnosed stage I disease, ranging from 2-10% in each region. Twenty-six per-cent of disease was stage II, ranging from 21-35% in each region, 50% of disease was stage III, ranging from 39-74% in each region, and 17% of disease was stage IV, ranging from 3-21% in each region. The earliest tumors were in NA; 74%, and 81% were Stage II or III in SNA and NA, respectively, while 70% or above were Stage III or IV in other regions (Figure 4 and Supplementary File).

Figure 4. AAA.

Trend analysis showed a decreasing prevalence of stage I (from 8% to 4%) and stage IV (from 24% to 12%) disease, with an increasing prevalence of stage II and III disease in the last decade (Figure 4).

Two articles (577 subjects) contributed to the clinical T-stage analysis, and seven articles (2151 subjects) contributed to the pathologic T-stage analysis. The majority of tumors were clinical T3 or T4, whereas the majority were pathologic T2 or T3. The prevalence of pathologic or clinical nodal positivity was 70% (99% CI 60-80), based on the analysis of 21 articles (8,357 subjects). WA had the highest prevalence of nodal disease (84%, 95% CI 71-94, I2=99%). By-country analysis showed that Nigeria (91%, 95% CI 75-100, I2=98) had the highest prevalence of lymph node positivity, and Eritrea (34%, 95% CI 28-41, I2=21) had the lowest.

Treatment modalities

Post hoc analysis of the treatment modalities in the continent showed that 72% of BC patients overall underwent surgery. Overall mastectomy prevalence was 71% (95% CI 51-88, I2=99%) while prevalence of breast-conserving surgery was 1.0% (95% CI 0-2, I2=0%). Eighty-three per-cent (64-96 I2=98%) of patients received chemotherapy, 18% (95% CI 4-33, I2 =94%) received radiotherapy, and 77% (95% CI 42-100 I2= 99) received hormonal therapy. Three studies reported routine hormonal therapy in all patients (see Supplementary File). There was no data on targeted-therapy.

Discussion

The African continent has a total population of approximately 1.34 billion inhabitants, accounting for 17% of the world’s population. The United Nations recognizes five African regions comprising 64 territories/ countries: EA (22 countries) 0.45 billion, WA (17 countries) 0.40 billion, NA (11 countries) 0.25 billion, CA (9 countries) 0.18 billion and SNA (5 countries) 0.07 billion. Together WA and EA account for more than 60% of Africa’s population, and South Africa (SA) alone accounts for 88% of the population of SNA.

We aggregated data from 80 articles published within the last decade, from 23 countries representing Africa’s regions. Our findings corroborated previous evidence that African BC patients are younger than those from Europe and the US. In this study, 6% of patients were <30 years of age compared to 0.43% in the UK, 28% were <40 years compared to 6.6% in the US [96, 97], and 58% were <50 years compared to 20% in Europe [98].

The age distribution of BC in South Africa showed a reverse pattern, mirroring the Caucasian age distribution seen in Europe. One explanation might be the proportion of Caucasian inhabitants in SA. Nonetheless, in four of the seven studies included from SA where the race was reported, 90% were Black patients (Table 1). However, it was not reported whether these patients might have been mixed-race Black patients. Even then, previous report suggests that black BC patients in SA are older than other races with BC in SA [99], though this may be partially- attributable to under-reporting.

The declining age of BC found in this study in the setting of the increasing age of Africa’s population overall [100] contradicts the view that the earlier age of BC onset can be entirely attributed to the younger population in Africa. Additionally, the elevated proportion of male breast cancer, 3% overall and 4% in the last decade, compared to approximately 1% reported globally [101, 102], and previously reported increased rates of triple negative disease raise questions regarding potential genetic predisposition and merit further investigation.

The early age of BC onset in Africa brings numerous challenges regarding screening, early diagnosis, and treatment compliance [103]. Young women may be less likely to complete the diagnostic process or treatment for BC due to social reasons, such as fertility issues and socio- cultural isolation. A report in Nigeria found that 31% of young women outrightly declined the diagnostic biopsy procedure, 60% of those who did not decline failed to return for the result of the biopsy, and only 45% of those offered mastectomy accepted treatment [103]. Future intervention should be directed toward improving early diagnosis and compliance with treatment in this patient population.

Even in high-income countries where screening is ubiquitous, it is recommended to begin after 40 years (or 50 according to some guidelines). A third of BC patients in Africa were <40 and would be missed by applying the same screening age guidelines as in the US. While population-based mammographic screening programs are not feasible in most African countries due to resource constraints, education of the general population, paired with clinical breast examination (CBE) has the ability to downstage clinically apparent disease, and age range recommendations should be based on available data.

Thirty-eight per-cent of breast cancer patients in this analysis had none or primary education, and education level varied widely by region. This underscores the importance of tailoring breast cancer education and breast health awareness for both patients and the general population to the local context, taking into account educational and cultural background.

Although unmarried BC patients’ population appears to be increasing in Africa, perhaps due to delaying marriage for education, the current predominantly married BC patient population still provides opportunities to include men as potential intervention targets. Reports suggest men are willing to support women in BC control [104, 105].

In this analysis, nearly 90% of tumors were greater than 2cm, half were greater than 5cm, and one-quarter had skin or chest wall involvement. This preponderance of clinically-detectable disease means that the vast majority of patients have the potential for earlier detection by CBE. Marked regional variations in tumor size and stage across regions, might be explained in part by differences in health systems. Coordinating and centralizing local resources provided affordable, comprehensive health financing, and helped to downstage BC in NA [106]. Increasing awareness and reducing the distance and bottlenecks between BC patients and specialists aided downstaging in SA [9]. Countries in SSA could benefit from the experience in NA and SA to attain the goals of downstaging invasive BC. The smaller pathologic T staging compared to the clinical T staging in our analysis might be linked to the widespread use of neoadjuvant chemotherapy or errors of clinical or pathologic measurement and requires further investigation.

The decreasing rate of stage IV disease over time (24% to 12% in the first decade vs. the second decade of this analysis) shows promise for a slow, but positive trend toward earlier diagnosis, which is one of the most important factors in improving outcomes. The generally low prevalence of carcinoma-in-situ, 2-4% in all regions, can be explained by the common lack of population- based screening. Population-based screening should not be considered until a health system has the resources and ability to effectively diagnose and treat clinically apparent disease. Nonetheless, it is important to note that the rise in the prevalence of small tumors (<1cm ) and carcinoma-in- situ (from 2% to >20% ) in developed countries was linked to screening [107]. In light of the emerging evidence supporting the use of ultrasound in detecting early BC in young women [96, 108, 109], when a health system is ready to consider targeted screening, ultrasound may be considered along with CBE.

The heterogeneity, narrow spread, and paucity of articles capturing some of the variables analyzed limit our findings. Notably, only SA contributed to the findings for SNA. Similarly, in a previous review [110], only SA contributed to the meta-analytical review of the stage at presentation in SNA because the literature on BC is scarce from other SNA countries. Also, the reporting of demographic variables was influenced by the region as articles from the same region reported similar data points in similar formats. The countries of WA and EA reported more information on patient demographics than in the other regions. Availability of data limited our ability to draw conclusions regarding certain critical variables of interest, such as immunohistochemistry or treatment modality by stage.

In conclusion, Africa has a common goal of downsizing and downstaging BC, which is achievable through the early diagnosis of clinically detectable disease. There is marked regional variation in the clinical pattern and patient demographics of BC in Africa, and the interventions developed should be tailored to the local context in each area, while allowing for countries and regions to benefit from shared knowledge and experiences.

Acknowledgements

Declaration Funding

The authors received no funding for this research

Conflict of interest/Competing interests

The authors declare no conflict of interest.

Availability of data and Materials:

All data used in this article are freely available

Authors Contribution

Agodirin Contributed to all aspect of the research, all authors contributed to approval. Aremu contributed to conception, data acquisition, extraction , and review. Rahman contributed to conception, data interpretation, drafting, review. Olatoke contributed to conception, data interpretation and review. Olaogun contributed to draft, review and data interpretation, Akande contributed to data interpretation, drafting and review. Romanoff contributed to data interpretation, drafting and review.

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