|
 
 |
| ORIGINAL RESEARCH REPORT |
|
| Year : 2019 | Volume
: 16
| Issue : 4 | Page : 111-119 |
|
Sociodemographic correlates and management of breast cancer in Radiotherapy Department, Lagos University Teaching Hospital: A 10-year review
Temitope Olatunji1, Anthonia Chima Sowunmi2, Kingsley Kayode Ketiku3, Oladapo B Campbell4
1 Department of Radiology, Lagos State University Teaching Hospital, Lagos, Nigeria
2 Department of Radiation Biology, Radiotherapy and Radiodiagnosis, College of Medicine, University of Lagos, Lagos, Nigeria
3 Department of Radiotherapy, Eko Hospital, Lagos, Nigeria
4 Department of Radiotherapy, College of Medicine, University of Ibadan, Ibadan, Nigeria
| Date of Web Publication | 22-Oct-2019 |
Correspondence Address:
Dr. Anthonia Chima Sowunmi
Department of Radiation Biology, Radiotherapy and Radiodiagnosis, College of Medicine, University of Lagos, Lagos
Nigeria
 Source of Support: None, Conflict of Interest: None  | Check |
DOI: 10.4103/jcls.jcls_82_18
Background: Worldwide, breast cancer is the most frequently diagnosed life-threatening malignant disease in women. Aim: The aim of the study was to determine the sociodemographic correlates and management of breast cancer in a tertiary hospital. Patients and Methods: Case notes of histologically confirmed breast cancer patients were retrieved, and data extracted were analyzed using the Statistical Package for the Social Sciences version 20 (SPSS Incorporation, Chicago, Illinois State, United States of America). Results: A total of 1141 cases were analyzed, of which 1132 (99.2%) were female and 9 (0.8%) were male, with a ratio of 1:126. The range was between 9 and 20 years. The mean age was 46.8 ± 12.2 years, whereas most of the cases were between 50 and 59 years (23.0%). The mean age at menarche was 14.7 ± 2.2 years, whereas less than two-third of the patients were between 13 and 16 years (63.4%). The mean age at first pregnancy was 24.3 ± 4.7 years, whereas majority of them were between 20 and 29 years (71.4%). The mean age at menopause was 49.0 ± 5.7 years, whereas more than a third of the patients were between 45 and 49 years (37.5%). The median number of children ever born was 4 (interquartile range [IQR]: 3–5). Majority of the patients are married (84.1%). The median duration of breastfeeding of the patients was 12 (IQR: 12–18) months. The mean body mass index was 28.6 ± 6.5, whereas about a third of them are obese (34.7%). Majority of the patients have unskilled occupation (51.1%). The test of association between sociodemographic characteristics and histology status revealed a significant association between age of patients (P = 0.013**), marital status (P = 0.027**), age at menarche (P = 0.009**), and number of children (P = 0.034**). The test of association between sociodemographic characteristics and stage of disease revealed a significant association between age at menarche (P = 0.018**), age at menopause (P = 0.041**), age at pregnancy (P = 0.036**), and body mass index (P = 0.028**). A total of 213 (30.9%) cases had combined treatment, 289 (59.4%) had a mastectomy, and 294 (71.6%) had radiotherapy. The treatment outcome revealed that 549 (48.1%) were lost to follow-up, 447 (39.2%) were dead, and 145 (12.7%) were alive after 2 years posttreatment. Conclusion: Sociodemographic characteristics such as age of patients, age at menarche, and marital status had a significant association with histology, whereas age at menarche, age at menopause, age at pregnancy, and body index mass had a significant association with stage of disease, therefore influencing health outcomes for breast cancer. Keywords: Awareness, breast cancer, risk factors, screening, sociodemographic
How to cite this article:
Olatunji T, Sowunmi AC, Ketiku KK, Campbell OB. Sociodemographic correlates and management of breast cancer in Radiotherapy Department, Lagos University Teaching Hospital: A 10-year review. J Clin Sci 2019;16:111-9 |
How to cite this URL:
Olatunji T, Sowunmi AC, Ketiku KK, Campbell OB. Sociodemographic correlates and management of breast cancer in Radiotherapy Department, Lagos University Teaching Hospital: A 10-year review. J Clin Sci [serial online] 2019 [cited 2023 May 30];16:111-9. Available from: https://www.jcsjournal.org/text.asp?2019/16/4/111/269722 |
| Introduction | |  |
Breast cancer is the most frequently diagnosed life-threatening malignant disease in women.[1],[2]
In Nigeria, women at risk of breast cancer increased steadily from approximately 24.5 million in 1990 to approximately 40 million in 2010 and are projected to rise above 50 million in 2020.[3]
Invasive ductal carcinoma accounts for the largest proportion of breast cancer. Other variants of breast cancer histology are sarcoma, medullary, tubular, papillary, and mucinous.[4]
Surgery and radiation therapy with adjuvant hormonal and chemotherapy are now considered as the primary treatment for breast cancer.[5]
It is important to apply a multidisciplinary team approach to breast cancer management due to the associated burden.
| Patients and Methods | | |
This is a 10-year review of the sociodemographic correlates and management of breast cancer in the Radiotherapy Department in Lagos University Teaching Hospital between January 2004 and December 2013. The case records were retrieved from the radiotherapy departmental records office to get the necessary information for the study.
Categories of patients captured in the study include all breast cancer patients that presented between 2004 and 2013. Furthermore, those with histopathologically confirmed cases of breast cancer and whose case notes contains adequate clinical data.
Breast cancer cases without histological diagnosis and case notes with incomplete data were excluded from the study.
| Results | | |
A total of 1141 cases were seen in the 10-year period of the study.
[Table 1] shows the summary of the sociodemographic characteristics of the patients. The mean age was 46.8 ± 12.2 years, whereas most of them were between 50 and 59 years (23.0%). The mean age at menarche was 14.7 ± 2.2 years, whereas less than two-thirds of the patients were between 13 and 16 years (63.4%). The mean age at first pregnancy was 24.3 ± 4.7 years, whereas majority of them were between 20 and 29 years (71.4%). The mean age at menopause was 49.0 ± 5.7 years, whereas more than a third of the patients were between 45 and 49 years (37.5%). The median number of children ever born was 4 (interquartile range [IQR]: 3–5). Majority of the patients are married (84.1%). The median duration of breastfeeding of the patients was 12 (IQR: 12–18) months. The mean body mass index was 28.6 ± 6.5, whereas about a third of them are obese (34.7%). Majority of the patients have unskilled occupation (51.1%).
The presentation of breast cancer at the center peaked in 2010 with 164 (14.37%), followed by 157 (13.76%) and 133 (11.66%) in 2009 and 2011, respectively. The lowest occurrence was in 2013, with 67 (5.87%) cases [Figure 1].
Breast laterality revealed 553 (48.5%) in the left breast, 79 (6.9%) were bilateral, while 501 (43.9%) in the right breast.
The most common histology recorded was invasive ductal carcinoma accounting for 986 (86.4%). Other histological types recorded were mucinous 36 (3.2%), invasive lobular carcinoma 47 (4.1%), medullary 38 (3.3%), phyllodes 15 (1.3%), and papillary 19 (1.7%) [Figure 2].
[Table 2] shows the test of association between sociodemographic characteristics and histology status. There was a significant association between age of patients (P = 0.013**), marital status (P = 0.027**), age at menarche (P = 0.009**), and number of children (P = 0.034**). | Table 2: Test of association between sociodemographic characteristics and histology status
Click here to view |
A total number of 998 (87.47%) of 1141 patients had the stage of their disease recorded. The prevalent stage of disease was Stage IV (425, 52.59%), followed by Stage III (396, 39.68%), Stage II (145, 14.53%), and Stage I (32, 3.21%) [Figure 3].
[Table 3] shows the test of association between sociodemographic characteristics and stage of disease. There was a significant association between age at menarche (P = 0.018**), age at menopause (P = 0.041**), age at pregnancy (P = 0.036**), and body mass index (P = 0.028**). | Table 3: Test of association between sociodemographic characteristics and stage of disease
Click here to view |
Immunohistochemistry test was done for 139 of the 1141 patients recorded. Estrogen receptor (ER) positive was the most prevalent with 58 (35.6%) cases, 43 (26.4%) had progesterone receptor (PR) positive, and 38 (23.3%) were human epidermal growth factor receptor (HER2) positive.
Molecular subtypes revealed that hormone receptor positive and HER2 negative (Lumina A) seen in 87 (53.2%) patients, were the most common, followed by ER negative, PR negative and HER2 negative combination referred to as (basal like/triple negative) accounted for 39 (23.8%), HER2-enriched type was 24 (14.63%), Lumina B (combinations of ER/PR negative) was 14 (8.54%).
214 (18.8%) of the 1141 lymph node statuses were recorded, but only 135 (63.2%) of the patients had lymph node metastasis.
153 (13.4%) of the patients in this study had a positive family history of breast cancer. 79 (6.9%) drank alcohol, 9 (0.8%) smoked, and 125 (11.1%) females used oral contraceptives.
Almost 176 (15.4%) patients had comorbidities with hypertension being the most common, accounting for 136 (77.3%), followed by diabetes in 13 (7.4%) and 27 (15.3%) had both hypertension and diabetes.
The most common mode of treatment administered was chemotherapy (123, 17.7%), whereas the most common combination therapy given was surgery, chemotherapy, and radiotherapy (230, 30.9%). The most frequent mode of surgery performed for both lone and combination therapy was mastectomy (299, 59.4%). Radical or curative radiotherapy administered in 294 (71.6%) patients was the most common form of radiotherapy treatment given [Table 4].
Chemotherapy treatment is the most common therapy administered and had 5-fluorouracil (5FU), epirubicin, and cyclophosphamide (FEC) (43.4%) as the most given regimen, other drug combinations were cyclophosphamide, adriamycin, and 5FU (CAF) (84, 15.7%) and cyclophosphamide, methotrexate, and 5FU (CMF) (37, 6.9%). Two – drug combination therapy revealed adriamycin and cyclophosphamide, (AC) (71, 13.4%) as the most common, followed by epirubicin and cyclophosphamide, (EC) (28, 5.2%). Taxane-based drugs which included docetaxel and paclitaxel in combinations with AC, EC, CMF, and FEC were seen in 76 (14.2%). Other types of drugs administered accounted for 21 (4.0%), and the drugs are vinorelbine, gemcitabine, carboplatin, cisplatin, and Xeloda.
The outcome of the treatment of patients after the 2nd year of follow-up showed that majority (48.1%) of patients who presented were lost to follow-up, closely followed by dead outcome (39.2%). Only 12.7% of patients were on follow-up.
Assessing the treatment response of 145 (12.7%) patients who were on follow-up, it was revealed that majority had a complete response (42.2%), 24.1% of patients had disease progression, 23.5% of patients had partial response, whereas 10.2% of patients had no response.
| Discussion | | |
The 10-year retrospective review revealed 1141 cases of breast cancer between January 1, 2004, and December 31, 2013. The presentation was low between 2012 and 2013 due to the protected industrial action by medical practitioners. In a study of breast cancer incidence in Nigeria, breast cancer was seen as the most prevalent cancer type across five cities.[6] The prevalence in this study is low when compared with other studies in Nigeria; this may be due to the one study location (Radiotherapy Department) considered.
Several studies done in Nigeria showed an annual incidence which varies with location. A total of 156 cases were seen in Maiduguri,[7] 116 cases in Ibadan,[8] 57 cases in Ilorin,[8] and 16 cases in Calabar.[9] The varying prevalence of breast cancer in different cities across Nigeria also showed the significance of awareness of breast cancer. The prevalence was seen to be high in urban centers than in suburban centers, whereas patients who presented at these suburban areas were of higher socioeconomic status.[9]
Breast cancer is known to be a disease that is prevalent in middle-aged women. The mean age of patients in this study was 46.8 ± 12.2 years, peak age group was 50–59 years (23.0%), accounting for the majority of the entire study population. The peak decade was the fifth decade (40–49 years) which is in consonance with several studies internationally and locally. Popoola et al. in Lagos [10] and Godwin et al. in Calabar [9] found the peak decade as the fourth decade, Parkin in Kenya and South Africa, and Clegg-Lamptey and Hodasi in Ghana [11] found the peak decade as the fifth decade. Eniojukan and Adepoju in Ibadan [8] also found the peak age group to be 31–50 years, which further buttressed the prevalence in young adult women. However, some other studies done among African and African–American women have reported a high prevalence of breast cancer among younger women.[12],[13] The reason for this disparity is yet to be fully investigated.
The male-to-female ratio of 1:126 found was in consonance with several studies, 99.2% of the entire population in this study were female, 98.3% was found in Ibadan, 96.8% was found in Ilorin, 97.5% in Maiduguri, whereas a study in Calabar found 100%, Ramasamy and Govinda and Russell in their study found that women are 100 times more commonly affected than men. This could be as a result of men having less estrogen and progesterone hormones that promote breast growth.[2],[14]
Majority (87.6%) were Yoruba and residents of the Southwestern part of Nigeria (93.5%) with Lagos residents accounting for 79.2% of the entire study population which is understandable due to the location of the institute. The occupation of these patients from this location was found to be majorly trading/business (52.7%) and civil servants (26.0%), a similar result from Calabar which supports findings of Eniojukan and Adepoju that those presenting with breast cancer are those who are economically capable to foot its management.[8]
The laterality of the diseases was left-sided bias (48.5%), whereas those found in the right and bilateral breasts were 43.9% and 6.9%, respectively. This is similar to Ekanem and Aligbe findings in Benin where left was 53.3%, right 45.7%, and bilateral 0.8%,[15] however, this was in disparity with findings in Gombe by Dauda et al., where left 71.1% and right 28.3%, and 0.6% bilateral.[16] In Tanzania, Ashley found 45.77% left, 48.04% right, and 6.19% bilateral.[17] Full reasons had not yet been established. However, the left breast is larger than the right breast consequently, which lends credence the logic that more breast tissue is present to be a risk for cancer development.[18] Tulinius et al. stated that excess risk of developing cancer remains for the left breast also for women who have lost one breast because of cancer.[13]
Invasive ductal carcinoma (not otherwise specified) was the most common histological diagnosis seen (82.8%), this is comparable with other studies locally and internationally.[19],[20],[21],[22],[23],[24],[25]
A common clinical finding that characterizes Nigerian breast cancer patients is late presentation, about eighty percent of those with recorded cancer stage presented late (Stage III and IV) in this study. Popoola in his findings revealed that late-stage breast cancer has distant metastatic involvement to sites such as lungs, spine, lymph node, and anterior chest wall.[10] Low awareness about early signs and symptoms of cancer, dearth of cancer specialists and diagnosticians, poor economic status, inadequate policies, and poor access to equipment to curtail the breast cancer menace are factors that contribute to the late presentation of patients, whereas complaints that characterize these presentations include lump, bleeding, lymph node-positive status, increasing lump size, and so on at the clinic which was symptoms of late-stage and metastatic breast cancer. In a pathological analysis of the proliferative activity in tumors of 300 Nigerian women, it was noted that mitotic indices were notably higher than the range of values typically reported from the Western world, and there is the possibility of inherently more aggressive tumor biology among African women.[26] While the goal of breast cancer screening is to detect cancer before symptoms commence, a study in Lagos revealed that self-breast examination which drives this objective home more is majorly practiced by educated persons.[27]
Immunohistochemistry started in 2008 in our center which gained popularity as the year progressed, of the 139 cases that recorded immunochemistry findings, the most common was ER positive (35.6%), PR positive, and HER2 positive were 26.4% and 23.3%, respectively, this is in consonance with a study done in Ibadan by Adebamowo et al. ER positive was the most common (65.1%) and the least HER positive (20.3%)[28] also a study in Ghana by Seshie et al. showed similar order as ER, PR, and HER2 receptor positivity was 32.1%, 25.6%, and 25.5%, respectively.[29] This was used in reclassifying the disease into molecular subtypes; the most common molecular subtypes were Lumina A (53.2%) followed by basal like/triple negative (23.8%). This is consistent with Adebamowo's study but in contrast to other studies by Bernard (basal like 49.4%)[29] and Huo in Nigeria and Senegal where the majority were basal like (27%).[30] Ma et al. in their study, found ER and PR positive to be significantly higher in Caucasian than in non caucasians.[31] Recent research through genomic has considered breast cancer to be heterogeneous, Lumina A subtype has the best survival in the first 5 years, whereas HER2 had the worst.[13] Breast cancer is regarded as a collection of separate diseases, and subtyping is regarded as essential to identify better new molecular prognostic, predictive, and/or therapeutic targets, an important step toward tailoring the treatment.
Positivity of the lymph nodes (63%) was seen to be higher than negative nodes involvement (37%) in this study which is similar to what Popoola found to have lymph node involvement (87.6%). Clinical and experimental data suggest that migration of tumor cells into the lymph node is greatly facilitated by lymphangiogenesis. This process is dynamic during embryogenesis but is relatively rare in adulthood. Enhanced lymph node lymphangiogenesis and lymph flow in tumor-draining lymphatic vessels have also been reported to contribute to metastatic spread (Ran et al., 2010).
The mean age at menarche of patients in this study was 14.67 ± 2.16 years, which is similar to mean age (15.06 ± 2.17 years) found by Eniojukan in Ibadan and Anyanwu in East Nigeria found 13.67 years, Vorobiof et al. found 14.7 years in rural Africans, 13.9 years in urban Black, and 12.6 years in Caucasians women in South Africa.[32] Majority (52%) of patients in this study attained menarche between 14 and 16 years, which is also similar to a study in India (14–14.5 years).[33] Attaining menarche at an early age in life exposes female patients to estrogen hormones, consequently exposes the patients to breast cancer.
The preponderance of menopausal status in this study was seen in the premenopausal female patients (81.3%) which is consistent with Eniojukan and Adepoju in Ibadan (62.5%),[8] Ganiy in his study found that Black women both within and outside Africa have a higher incidence of premenopausal breast cancer than Caucasians. For the menopausal patient, the average age of attaining menopause was 55 years,[34] however, 20% were menopausal at about average age of 48.86 years which is similar to other studies.[35],[36],[37] Late menopausal age increases the chances of developing breast cancer in female patients due to the prolonged estrogen exposure from age at menarche. As a result, longer estrogen window exposes female to a higher risk of breast cancer.
Majority of the patient were multiparous. This signifies that a large percentage have had either pregnancy or childbearing history.[8] Godwin in Calabar found 86.1% of patients in his study to be parous women, this is replicated in this study where about 70% of the patients were parous with an average age at first pregnancy of 24.26 years who had an average number of children of 3.75 ≈ 4 which range between 1 and 10 who were breastfed for an average of 13.73 ± 5.66 months. These reproductive characteristics are not peculiar to this study as Godwin [9] also found the same characteristics at a different study location in Calabar. Indian women were also seen to bear an average of 3–4 children [38] Okobia et al. in another study reported that women who were para 4 and above had a decreased risk for breast cancer. Childbearing and the high number of full-term pregnancies have been found to reduce the risk of breast cancer with risk-reducing by 30% for each full-term pregnancy compared to nulliparous women.[39] Studies in Nigeria have also associated high parity or multiparity with decreased risk for breast cancer.[40]
The duration of breastfeeding in this study ranged between 6 months and 2 years with a mean duration of 13.73 ± 5.66 months. Breastfeeding for a long duration has been associated with breast cancer risk reductions as great as 40%–60%.[41]
Only 7% of the population in this study took alcohol occasionally and <1% of the patients smoke; this is valid as smoking is not rampant among Nigerian females, and this is similar to a study done by Anyanwu in East Nigeria where nonsmokers were the entirety of the population and 15% were social drinkers [42] Alcohol appears to increase circulating levels of estradiol, Marsha reported that two drinks of ethanol a day elevate serum estrogens and exposure to estrogen increases the risk of breast cancer.
Only 125 (11.1%) admitted to having used oral contraceptives, long-term use of oral contraceptives is associated with increased risk of premenopausal women;[43] however, duration of usage was not captured in this study.
Majority of the patients were obese (40%). Obesity as an associated etiological factor of breast cancer is further bolstered here with similar findings in Ibadan.[8],[44] Obesity has been found to increase risks of breast cancer in postmenopausal women due to increase in estrogen exposure caused by aromatization in fatty tissues.[43]
Hypertension was seen to be the most common comorbidity (77.3%), followed by the combination of hypertension and diabetes (15.3%) which was similar in Zaria, stroke alongside diabetes was also found by Satariano and Ragland.[45]
The treatment modality revealed that chemotherapy was the most common lone treatment given (17.7%), followed by surgery (2.7%) and majority 213 (30.9%) received a combination of chemotherapy, surgery, and radiotherapy, 20.4% of patients had chemotherapy and surgery alone.[46],[47] Three-drug regimen received includes FEC (43.4%), CAF (15.7%), CMF (6.9%), the most common two-drug regimen given was AC (adriamycin and cyclophosphamide). 14.2% had taxane-based drugs, which is administered to patients that presented late or with triple-negative or recurrence diseases.[46],[47],[48] This correlates with the studies done by Vanderpuye et al. in Ghana, and this is because patients present late and most of the drugs used are conventional cheap drugs since patients pay out of pocket for their treatment.
145 (12.7%) of 693 (60.7%) patients were on follow-up posttreatment, and it revealed that 42.2% had a complete response, partial response 23.5%, disease progression 24.1%, and no response 10.2%.[49] This correlates with the study of Du Plessis et al. of South Africa simply because of limited numbers of standardized treatment centers, patients having to travel from a far distance to access treatment and coupled with financial constraints preventing them from coming for regular follow-ups and reviews.
| Conclusion | | |
Sociodemographic characteristics such as age of patients, age at menarche, and marital status had a significant association with histology, whereas age at menarche, age at menopause, age at pregnancy, and body index mass had a significant association with stage of disease, therefore, influencing health outcomes for breast cancer.
Financial support and sponsorship
Nil.
Conflicts of interest
There are no conflicts of interest.
| References | | |
| 1. | Jemal A, Bray F, Center MM, Ferlay J, Ward E, Forman D, et al. Global cancer statistics. CA Cancer J Clin 2011;61:69-90.  |
| 2. | Ramaswamy Md, Yenni G, Matthew A, Arquette MD, Lieber RL. The Washington Manual of Oncology. 1 st ed., Ch. 7. Breast Cancer. Lippincott Williams and Wilkins Published; 2002. p. 13-47. |
| 3. | Akarolo-Anthony SN, Ogundiran TO, Adebamowo CA. Emerging breast cancer epidemic: Evidence from Africa. Breast Cancer Res 2010;12 Suppl 4:S8. |
| 4. | Li CI, Uribe DJ, Daling JR. Clinical characteristics of different histologic types of breast cancer. Br J Cancer 2005;93:1046-52. |
| 5. | Jemal A, Siegel R, Ward E, Hao Y, Xu J, Murray T, et al. Cancer statistics, 2008. CA Cancer J Clin 2008;58:71-96. |
| 6. | Abdulkareem F. Epidemiology and Incidence of Common Cancers in Nigeria. Cancer Registration and Epidemiology Workshop; April, 2009. |
| 7. | Nggada HA, Gali BM, Bakari AA, Yawe-Terna EH, Tahir MB, Apari E, et al. The spectrum of female breast diseases among Nigerian population in Sahel climatic zone. J Med Med Sci 2011;2:1157-61. |
| 8. | Eniojukan JF, Adepoju T. An audit of the management and associated contextual correlates of clinical presentations of breast cancer in tertiary hospital in south west. IOSR J Pharm 2015;5:11-21. |
| 9. | Godwin AE, Gabriel UU, Martin AN, Ima-Abasi B, Victor JN, Udosen JE, et al. Histological type and tumour grade in Nigerian Breast Cancer; Relationship to Menarche, Family History of Breast Cancer, Parity, Age at First Birth and age at menopause. IOSR Journal of dental and medical science 2013;7:58-63. |
| 10. | Popoola AO, Ibrahim NA, Omodele FO, Oludara MA, Adebowale SA, Igwilo AI. Pattern of spread of breast cancer among patients attending cancer unit in Lagos state university teaching hospital. Asian J Med Sci 2012;4:89-94. |
| 11. | Clegg-Lamptey J, Hodasi W. A study of breast cancer in Korle Bu teaching hospital: Assessing the impact of health education. Ghana Med J 2007;41:72-7. |
| 12. | Kwong A, Mang OW, Wong CH, Chau WW, Law SC. Hong Kong Breast Cancer Research Group. Breast cancer in Hong Kong, Southern China: The first population-based analysis of epidemiological characteristics, stage-specific, cancer-specific, and disease-free survival in breast cancer patients: 1997-2001. Ann Surg Oncol 2011;18:3072-8. |
| 13. | Tulinius H, Sigvaldason H, Olafsdóttir G. Left and right sided breast cancer. Pathol Res Pract 1990;186:92-4. |
| 14. | Allum WH, Russell RCG, Williams NS. Chapter on breast cancer. In: Russell B and Love's Short Practice of Surgery. 23 rd ed. London: Arnold; 2000. p. 761. |
| 15. | Ekanem VJ, Aligbe JU. Histopathological types of breast cancer in Nigerian women: A 12-year review (1993-2004). Afr J Reprod Health 2006;10:71-5. |
| 16. | Dauda AM, Misauno MA, Ojo EO. Histopathological types of breast cancer in Gombe, North Eastern Nigeria: A seven-year review. Afr J Reprod Health 2011;15:109-11. |
| 17. | Burson AM, Soliman AS, Ngoma TA, Mwaiselage J, Ogweyo P, Eissa MS, et al. Clinical and epidemiologic profile of breast cancer in Tanzania. Breast Dis 2010;31:33-41. |
| 18. | Elumelu TN, Adenipekun AA, Abdulsalam AA, Bojude AD. Pattern of breast cancer metastasis at the radiotherapy clinic, Ibadan. A-ten year study. Rev J Am Sci 2011;7:906-12. |
| 19. | Nggada HA, Yawe KD, Abdulazeez J, Khalil MA. Breast cancer burden in Maiduguri, North Eastern Nigeria. Breast J 2008;14:284-6. |
| 20. | Gogo-Abite M, Nwosu SO. Histopathological characteristics of female breast carcinomas seen at the university of Port Harcourt teaching hospital, port Harcourt Nigeria. Niger J Med 2005;14:72-6. |
| 21. | El-Hawary AK, Abbas AS, Elsayed AA, Zalata KR. Molecular subtypes of breast carcinoma in Egyptian women: Clinicopathological features. Pathol Res Pract 2012;208:382-6. |
| 22. | Obose AA, Salem OA, Alrabayha M, Alghzawi K. Clinical features and prognostic factors of breast cancer in Jordan. RMJ 2007;32:50-2. |
| 23. | Shirley SE, Mitchell DI, Soares DP, James M, Escoffery CT, Rhoden AM, et al. Clinicopathologic features of breast disease in JAMAICA: Findings of the Jamaican breast disease study, 2000-2002. West Indian Med J 2008;57:90-4. |
| 24. | Mamoon N, Sharif MA, Mushtaq S, Khadim MT, Jamal S. Breast carcinoma over three decades in Northern Pakistan – Are we getting anywhere? J Pak Med Assoc 2009;59:835-8. |
| 25. | Sariego J. Patterns of breast cancer presentation in the United States: Does geography matter? Am Surg 2009;75:545-9. |
| 26. | Ikpatt OF, Kuopio T, Collan Y. Proliferation in African breast cancer: Biology and prognostication in Nigerian breast cancer material. Mod Pathol 2002;15:783-9. |
| 27. | Bertucci F, Finetti P, Birnbaum D. Basal breast cancer: A complex and deadly molecular subtype. Curr Mol Med 2012;12:96-110. |
| 28. | Adebamowo CA, Famooto A, Ogundiran TO, Aniagwu T, Nkwodimmah C, Akang EE, et al. Immunohistochemical and molecular subtypes of breast cancer in Nigeria. Breast Cancer Res Treat 2008;110:183-8. |
| 29. | Seshie B, Adu-Aryee NA, Dedey F, Calys-Tagoe B, Clegg-Lamptey JN. A retrospective analysis of breast cancer subtype based on ER/PR and HER2 status in Ghanaian patients at the Korle Bu teaching hospital, Ghana. BMC Clin Pathol 2015;15:14. |
| 30. | Huo D, Ikpatt F, Khramtsov A, Dangou JM, Nanda R, Dignam J, et al. Population differences in breast cancer: Survey in indigenous African women reveals over-representation of triple-negative breast cancer. J Clin Oncol 2009;27:4515-21. |
| 31. | Ma H, Lu Y, Malone KE, Marchbanks PA, Deapen DM, Spirtas R, et al. Mortality risk of black women and white women with invasive breast cancer by hormone receptors, HER2, and p53 status. BMC Cancer 2013;13:225. |
| 32. | Vorobiof DA, Sitas F, Vorobiof G. Breast cancer incidence in South Africa. J Clin Oncol 2001;19:125S-7S. |
| 33. | Navneet K, Attam A, Saha S, Bhargava SK. Breast cancer risk factor profile in indian women. J Int Med Sci Acad 2011;24:163-5. |
| 34. | Clavel-Chapelon F; E3N-EPIC Group. Differential effects of reproductive factors on the risk of pre-and postmenopausal breast cancer. Results from a large cohort of French women. Br J Cancer 2002;86:723-7. |
| 35. | Campbell OB, Agwimah R, Oduola BI, Alawale E. Radiotherapy management of breast cancer in 400 Nigerian. Niger Med J 1998;27:98-100. |
| 36. | Tamimi RM, Baer HJ, Marotti J, Galan M, Galaburda L, Fu Y, et al. Comparison of molecular phenotypes of ductal carcinoma in situ and invasive breast cancer. Breast Cancer Res 2008;10:R67. |
| 37. | Clark SE, Warwick J, Carpenter R, Bowen RL, Duffy SW, Jones JL. Molecular subtyping of DCIS: Heterogeneity of breast cancer reflected in pre-invasive disease. Br J Cancer 2011;104:120-7. |
| 38. | Okobia MN, Bunker CH, Okonofua FE, Osime U. Knowledge, attitude and practice of Nigerian women towards breast cancer: A cross-sectional study. World J Surg Oncol 2006;4:11. |
| 39. | Parkin DM 15. Cancers attributable to reproductive factors in the UK in 2010. Br J Cancer 2011;105 Suppl 2:S73-6. |
| 40. | Adebamowo CA, Ajayi OO. Breast cancer in Nigeria. West Afr J Med 2000;19:179-91. |
| 41. | Yang CP, Weiss NS, Band PR, Gallagher RP, White E, Daling JR, et al. History of lactation and breast cancer risk. Am J Epidemiol 1993;138:1050-6. |
| 42. | Anyanwu SN. Temporal trends in breast cancer presentation in the third world. J Exp Clin Cancer Res 2008;27:17. |
| 43. | Assi HA, Khoury KE, Dbouk H, Khalil LE, Mouhieddine TH, El Saghir NS. Epidemiology and prognosis of breast cancer in young women. J Thorac Dis 2013;5 Suppl 1:S2-8. |
| 44. | Adebamowo CA, Ogundiran TO, Adenipekun AA, Oyesegun RA, Campbell OB, Akang EU, et al. Obesity and height in urban Nigerian women with breast cancer. Ann Epidemiol 2003;13:455-61. |
| 45. | Satariano WA, Ragland DR. The effect of comorbidity on 3-year survival of women with primary breast cancer. Ann Intern Med 1994;120:104-10. |
| 46. | Vanderpuye V, Grover S, Hammad N, Prabhakar P, Simonds H, Olopade F, et al. An update on the management of breast cancer in Africa. Infect Agent Cancer 2017;12:13. |
| 47. | Kantelhardt EJ, Muluken G, Sefonias G, Wondimu A, Gebert HC, Unverzagt S, et al. A review on breast cancer care in Africa. Breast Care (Basel) 2015;10:364-70. |
| 48. | Vanderpuye VD, Olopade OI, Huo D. Pilot survey of breast cancer management in Sub-Saharan Africa. J Glob Oncol 2017;3:194-200. |
| 49. | Du Plessis M, Apffelstaedt JP. Treatment outcomes of breast carcinoma in a resource-limited environment. S Afr J Surg 2015;53:43-7. |
[Figure 1], [Figure 2], [Figure 3]
[Table 1], [Table 2], [Table 3], [Table 4]
|
Search Pubmed for