Cancer Research in sub-Saharan Africa: Progress in closing the gap
Main Article Content
Abstract
Cancer presents an escalating challenge in Sub-Saharan Africa (SSA), necessitating strategic interventions grounded in regionally relevant evidence-based medicine. Informed decision-making is critical to formulate effective strategies for cancer prevention, diagnosis, funding, and treatment within the SSA population. The aim of this study is to highlight ongoing clinical trials in SSA, emphasizing the continuous initiatives aimed at filling existing knowledge gaps. Further, the study seeks to assess whether SSA is progressing or stagnating in the global landscape of cancer research. A comprehensive review of research papers and online registries on clinical trials was executed, focusing on English-language journal articles retrieved from the PubMed database. Additionally, a quantitative, web-based, retrospective review was conducted on registered cancer studies in SSA over the past decade (2000-2023) from ClinicalTrials.gov and the Pan African Clinical Trials Registry (PACTR) databases. The review resulted in the inclusion of 71 articles from PubMed, alongside 104 and 140 clinical trials from ClinicalTrials.gov and PACTR databases, respectively. Aggregate findings from PubMed and clinical trial databases revealed that East Africa is the predominant contributor (37%) to cancer clinical trials, whereas Central Africa exhibited the lowest contribution (4%). Notably, PubMed indicated a predominant focus on cervical cancer in clinical trials. Between 2000 and 2015, less than 4% of global cancer clinical trials listed on ClinicalTrials.gov were performed in SSA; in subsequent years, there was an observable increase in the percentage of total trials performed in SSA. Analyses of funding sources revealed that 45% and 32% of clinical trials in SSA were supported by the United States and the United Kingdom, respectively. In the last two decades, the formation of entities like the African Consortium for Cancer Clinical Trials, spearheaded by BIO Ventures for Global Health in partnership with African ministries of health, cancer hospitals, private industry, research institutions, and global oncology experts, contributed to increasing the effective implementation of multicenter clinical trials in Africa. Noteworthy instances, such as the Burkitt's lymphoma and HypoAfrica studies, serve as examples of the results arising from these collaborative initiatives, reflecting substantial progress within SSA’s cancer research landscape.
Keywords:
Clinical trials, sub-Saharan Africa, Cancer research
Article Details
How to Cite
MALLUM, A et al.
Cancer Research in sub-Saharan Africa: Progress in closing the gap.
Medical Research Archives, [S.l.], v. 12, n. 4, apr. 2024.
ISSN 2375-1924.
Available at: <https://esmed.org/MRA/mra/article/view/5080>. Date accessed: 21 dec. 2024.
doi: https://doi.org/10.18103/mra.v12i4.5080.
Section
Research Articles
The Medical Research Archives grants authors the right to publish and reproduce the unrevised contribution in whole or in part at any time and in any form for any scholarly non-commercial purpose with the condition that all publications of the contribution include a full citation to the journal as published by the Medical Research Archives.
References
1. Ibraheem A, Pillai C, Okoye I, Smith JJ, Reidy-Lagunes D, Macaulay G, Alatise O. Cancer clinical trials in Africa—an untapped opportunity: recommendations from AORTIC 2019 conference special interest group in clinical trials. JCO Global Oncology. 2021;7:1 358-1363. https://doi.org/10.1200/go.21.00096
2. Hamdi Y, Abdeljaoued-Tej I, Zatchi AA, Abdelhak S, Boubaker S, Brown JS, Benkahla A. Cancer in Africa: the untold story. Frontiers in oncology. 2021;11:650117. https://doi.org/10.3389/fonc.2021.650117
3. Kizub D, Manner CK, Graef K, et al. Action for Increasing Diversity, Market Access, and Capacity in Oncology Registration Trials—Is Africa the Answer? Report From a Satellite Session of the Accelerating Anti-Cancer Agent Development and Validation Workshop. JCO Global Oncology. 2022;8:e2200117. https://doi.org/10.1200/GO.22.00117
4. Solarin O, Mohammed SI, Ndlovu N, Vanderpuye V, Olaiya V. Partnerships and collaborations: the right alliances for clinical trials in Africa. JCO Global Oncology. 2020;6: 954-958. https://doi.org/10.1200/jgo.19.00194
5. Ntekim A, Olopade OI. Innovative Strategies for Developing Biomarker-Informed Cancer Clinical Trials to Accelerate Progress in Precision Oncology in Sub-Saharan Africa. American Society of Clinical Oncology Educational Book. 2022;42:438-446. https://doi.org/10.1200/edbk_349955
6. Ngoma T, Adde M, Durosinmi M, et al. Treatment of Burkitt lymphoma in equatorial Africa using a simple three‐drug combination followed by a salvage regimen for patients with persistent or recurrent disease. British journal of haematology. 2012;158(6):749-762. https://doi.org/10.1111/j.1365-2141.2012.09236.x
7. Olatunji E, Swanson W, Patel S, et al. Challenges and opportunities for implementing hypofractionated radiotherapy in Africa: lessons from the HypoAfrica clinical trial. ecancermedicalscience. 2023;17. https://doi.org/10.3332%2Fecancer.2023.1508
8. Özdemir BC, Dotto G-P. Racial differences in cancer susceptibility and survival: more than the color of the skin? Trends in cancer. 2017;3(3):181-197. https://doi.org/10.1016/j.trecan.2017.02.002
9. Bentley AR, Callier SL, Rotimi CN. Evaluating the promise of inclusion of African ancestry populations in genomics. NPJ genomic medicine. 2020;5(1):5. https://doi.org/10.1038/s41525-019-0111-x
10. Alemayehu C, Mitchell G, Nikles J. Barriers for conducting clinical trials in developing countries-a systematic review. International journal for equity in health. 2018;17:1-11. https://doi.org/10.1186/s12939-018-0748-6
11. Koffi KG, Silué D, Laurent C, et al. AMAFRICA, a patient-navigator program for accompanying lymphoma patients during chemotherapy in Ivory Coast: a prospective randomized study. BMC cancer. 2019;19(1):1-8. https://doi.org/10.1186/s12885-019-6478-3
12. Firnhaber C, Swarts A, Jezile V, et al. Human papillomavirus vaccination prior to loop electroexcision procedure does not prevent recurrent cervical high-grade squamous intraepithelial lesions in women living with human immunodeficiency virus: a randomized, double-blind, placebo-controlled trial. Clinical Infectious Diseases. 2021;73(7):e 2211-e2216. https://doi.org/10.1093/cid/ciaa1456
13. Skiles JL, Chiang C, Li CH, et al. CYP3A5 genotype and its impact on vincristine pharmacokinetics and development of neuropathy in Kenyan children with cancer. Pediatric blood & cancer. 2018;65(3):e26854. https://doi.org/10.1002%2Fpbc.26854
14. Greene SA, De Vuyst H, John-Stewart GC, et al. Effect of cryotherapy vs loop electrosurgical excision procedure on cervical disease recurrence among women with HIV and high-grade cervical lesions in Kenya: a randomized clinical trial. Jama. 2019;322(16): 1570-1579. https://doi.org/10.1001/jama.2019.14969
15. Wagner GJ, Matovu JK, Juncker M, et al. Effects of a peer advocacy intervention on cervical cancer screening among social network members: results of a randomized controlled trial in Uganda. Journal of Behavioral Medicine. 2023;46(6):930-939. https://doi.org/10.1007%2Fs10865-023-00418-6
16. Nyirenda M, Ngongondo M, Kang M, et al. Early progression and immune reconstitution inflammatory syndrome during treatment of mild-to-moderate Kaposi sarcoma in sub-Saharan Africa and South America: Incidence, long-term outcomes and effects of early chemotherapy. Journal of acquired immune deficiency syndromes (1999). 2020;84(4):422. https://doi.org/10.1097%2FQAI.0000000000002361
17. Lin LL, Ndlovu N, Lowenstein J, et al. Quality Assurance in Clinical Trials Requiring Radiation Therapy in Sub-Saharan Africa. International Journal of Radiation Oncology* Biology* Physics. 2023;116(2):439-447. https://doi.org/10.1016/j.ijrobp.2022.11.042
18. Larkin J, Del Vecchio M, Ascierto P, et al. Vemurafenib in patients with BRAFv⁶⁰⁰ mutated metastatic melanoma: an open-label, multicentre, safety study. 2014. https://doi.org/10.1016/s1470-2045(14)70051-8
19. Unger JM, Cook E, Tai E, Bleyer A. The role of clinical trial participation in cancer research: barriers, evidence, and strategies. American Society of Clinical Oncology Educational Book. 2016;36:185-198. https://doi.org/10.1200/edbk_156686
20. Mboineki JF, Wang P, Dhakal K, Getu MA, Chen C. The effect of peer-led navigation approach as a form of task shifting in promoting cervical cancer screening knowledge, intention, and practices among urban women in Tanzania: a randomized controlled trial. Cancer Control. 2022;29:1073 2748221089480. https://doi.org/10.1177/10732748221089480
21. Deressa BT, Tigeneh W, Bogale N, Buwenge M, Morganti AG, Farina E. Short-course 2-dimensional radiation therapy in the palliative treatment of esophageal cancer in a developing country: a phase II study (Sharon Project). International Journal of Radiation Oncology* Biology* Physics. 2020;106(1):67-72. https://doi.org/10.1016/j.ijrobp.2019.10.004
22. Getu MA, Wang P, Addissie A, Seife E, Chen C, Kantelhardt EJ. The effect of cognitive behavioural therapy integrated with activity pacing on cancer‐related fatigue, depression and quality of life among patients with breast cancer undergoing chemotherapy in Ethiopia: A randomised clinical trial. International Journal of Cancer. 2023. https://doi.org/10.1002/ijc.34452
23. Udeh E, Amu O, Nnabugwu I, Ozoemena O. Transperineal versus transrectal prostate biopsy: our findings in a tertiary health institution. Nigerian journal of clinical practice. 2015;18(1):110-114. https://doi.org/10.4103/1119-3077.146991
24. Malan T, Moodley K. Phase 3 oncology clinical trials in South Africa: experimentation or therapeutic misconception? Journal of Empirical Research on Human Research Ethics. 2016;11(1):47-56. http://dx.doi.org/10.1177/1556264616637736
25. Gizaw M, Teka B, Ruddies F, et al. Uptake of cervical cancer screening in Ethiopia by self-sampling HPV DNA compared to visual inspection with acetic acid: a cluster randomized trial. Cancer Prevention Research . 2019;12(9):609-616. ttps://doi.org/10.1158/1940-6207.capr-19-0156
26. Gichuhi S, Macharia E, Kabiru J, et al. Topical fluorouracil after surgery for ocular surface squamous neoplasia in Kenya: a randomised, double-blind, placebo-controlled trial. The Lancet Global Health. 2016;4(6):e 378-e385. https://doi.org/10.1016%2FS2214-109X(16)30052-3
27. Linde DS, Andersen MS, Mwaiselage J, Manongi R, Kjaer SK, Rasch V. Effectiveness of one-way text messaging on attendance to follow-up cervical cancer screening among human papillomavirus–positive Tanzanian women (Connected2Care): parallel-group randomized controlled trial. Journal of Medical Internet Research. 2020;22(4):e15863 . https://doi.org/10.2196/15863
28. Sossauer G, Zbinden M, Tebeu P-M, Fosso GK, Untiet S, Vassilakos P, Petignat P. Impact of an educational intervention on women's knowledge and acceptability of human papillomavirus self-sampling: a randomized controlled trial in Cameroon. PloS one. 2014;9(10):e109788. https://doi.org/10.1371/journal.pone.0109788
29. Chagaluka G, Paintsil V, Renner L, et al. Improvement of overall survival in the collaborative Wilms tumour Africa project. Pediatric Blood & Cancer. 2020;67(9):e28383. https://doi.org/10.1002/pbc.28383
30. Stocks J, Ibrahim S, Park L, Huchko M. Mobile phone ownership and use among women screening for cervical cancer in a community-based setting in Western Kenya: Observational study. JMIR Public Health and Surveillance. 2022;8(6):e28885. https://doi.org/10.2196%2F28885
31. Graef KM, Okoye I, Ohene Oti NO, Dent J, Odedina FT. Operational strategies for clinical trials in Africa. JCO Global Oncology. 2020;6:973-982. https://doi.org/10.1200/jgo.19.00204
32. Pace LE, Dusengimana JMV, Shulman LN, et al. Cluster randomized trial to facilitate breast cancer early diagnosis in a rural district of Rwanda. Journal of Global Oncology. 2019; 5:1-13. https://doi.org/10.1200/jgo.19.00209
33. Huchko MJ, Ibrahim S, Blat C, Cohen CR, Smith JS, Hiatt RA, Bukusi E. Cervical cancer screening through human papillomavirus testing in community health campaigns versus health facilities in rural western Kenya. International Journal of Gynecology & Obstetrics. 2018;141(1):63-69. https://doi.org/10.1002/ijgo.12415
34. Erlandson KM, Gudza I, Fiorillo S, et al. Relationship of vitamin D insufficiency to AIDS-associated Kaposi's sarcoma outcomes: retrospective analysis of a prospective clinical trial in Zimbabwe. International Journal of Infectious Diseases. 2014;24:6-10. https://doi.org/10.1016%2Fj.ijid.2014.02.006
35. Odedina FT, Shamley D, Okoye I, et al. Landscape of oncology clinical trials in Africa. JCO Global Oncology. 2020;6:932-941. https://doi.org/10.1200/jgo.19.00189
36. Okunade KS, Soibi-Harry A, John-Olabode S, et al. Impact of mobile technologies on cervical cancer screening practices in Lagos, Nigeria (mHealth-Cervix): a randomized controlled trial. JCO Global Oncology. 2021;7:1418-1425. https://doi.org/10.1200/go.21.00258
37. Chigbu CO, Onyebuchi AK. See-and-treat management of high-grade squamous intraepithelial lesions in a resource-constrained African setting. International Journal of Gynecology & Obstetrics. 2014;124(3):204-206. https://doi.org/10.1016/j.ijgo.2013.07.040
38. Toto N, Douglas E, Gmeiner M, et al. Conducting clinical trials in sub-Saharan Africa: challenges and lessons learned from the Malawi Cryptosporidium study. Trials. 2020;21:1-8. https://doi.org/10.1186/s13063-020-04620-8
39. Esterhuizen TM, Li G, Young T, Zeng J, Machekano R, Thabane L. Advancing collaborations in health research and clinical trials in Sub-Saharan Africa: development and implementation of a biostatistical collaboration module in the Masters in Biostatistics Program at Stellenbosch University. Trials. 2021;22(1):1-9. https://doi.org/10.1186/s13063-021-05427-x
40. Page MJ, McKenzie JE, Bossuyt PM, et al. The PRISMA 2020 statement: an updated guideline for reporting systematic reviews. International journal of surgery. 2021;88:1059 06.https://doi.org/10.1016/j.ijsu.2021.105906
41. Bond MC, Pritchard S. Understanding clinical trials in childhood cancer. Paediatrics & child health. 2006;11(3):148-150. http://dx.doi.org/10.1093/pch/11.3.148
42. Amoako E, Jumbam DT, Bediako Y. Unseen and unheard: African children with cancer are consistently excluded from clinical trials. BMJ Global Health. 2021;6(1). https://doi.org/10.1136/bmjgh-2020-004750
43. Hough R, Sandhu S, Khan M, et al. Are survival and mortality rates associated with recruitment to clinical trials in teenage and young adult patients with acute lymphoblastic leukaemia? A retrospective observational analysis in England. BMJ open. 2017;7(10). https://doi.org/10.1136/bmjopen-2017-017052
44. NCCN. NCCN Oncology Research Program (ORP). https://www.nccn.org/education-research/nccn-oncology-research-program/
45. Yaris N, Mandiracioglu A, Büyükpamukcu M. Childhood cancer in developing countries. Pediatric hematology and oncology. 2004;21(3):237-253. https://doi.org/10.1080/08880010490276971
46. Opinion: D. childhood cancers in Ghana— we must do more to protect the vulnerable among US. 2020. https://www.devex.com/news/sponsored/opinion-childhood-cancers-in-ghana-we-must-do-more-to-protect-the-vulnerable-among-us-97841
47. Magrath I, Adde M, Shad A, et al. Adults and children with small non-cleaved-cell lymphoma have a similar excellent outcome when treated with the same chemotherapy regimen. Journal of Clinical Oncology. 1996;14(3):925-934. https://doi.org/10.1200/jco.1996.14.3.925
48. Adde M, Shad A, Venzon D, et al. Additional chemotherapy agents improve treatment outcome for children and adults with advanced B-cell lymphomas. Paper presented at: Seminars in oncology, 1998. https://europepmc.org/article/med/9578060
49. Gad-El-Mawla N, Hussein MH, Abdel-Hadi S, El-Taneer O, Adde M, Magrath I. Childhood non-Hodgkin's lymphoma in Egypt: preliminary results of treatment with a new ifosfamide-containing regimen. Cancer Chemotherapy and Pharmacology. 1989;24:S 20-S23. https://doi.org/10.1007/bf00253233
50. Advani S, Pai S, Adde M, et al. Preliminary report of an intensified, short duration chemotherapy protocol for the treatment of pediatric non-Hodgkin's lymphoma in India. Annals of oncology. 1997;8(9):893-897. https://doi.org/10.1023/a:1008228529397
51. Ngwa W, Addai BW, Adewole I, et al. Cancer in sub-Saharan Africa: a lancet oncology commission. The Lancet Oncology. 2022;23(6):e251-e312. https://doi.org/10.1016/s1470-2045(21)00720-8
52. Aluwini S, Pos F, Schimmel E, et al. Hypofractionated versus conventionally fractionated radiotherapy for patients with prostate cancer (HYPRO): acute toxicity results from a randomised non-inferiority phase 3 trial. The Lancet Oncology. 2015;16(3):274-283. https://doi.org/10.1016/S1470-2045(15)00567-7
53. Aluwini S, Pos F, Schimmel E, et al. Hypofractionated versus conventionally fractionated radiotherapy for patients with prostate cancer (HYPRO): late toxicity results from a randomised, non-inferiority, phase 3 trial. The Lancet Oncology. 2016;17(4):464-474. https://doi.org/10.1016/S1470-2045(14)70482-6
54. Dearnaley D, Syndikus I, Mossop H, et al. Conventional versus hypofractionated high-dose intensity-modulated radiotherapy for prostate cancer: 5-year outcomes of the randomised, non-inferiority, phase 3 CHHiP trial. The Lancet Oncology. 2016;17(8):1047-1060. https://doi.org/10.1016/S1470-2045(16)30102-4
2. Hamdi Y, Abdeljaoued-Tej I, Zatchi AA, Abdelhak S, Boubaker S, Brown JS, Benkahla A. Cancer in Africa: the untold story. Frontiers in oncology. 2021;11:650117. https://doi.org/10.3389/fonc.2021.650117
3. Kizub D, Manner CK, Graef K, et al. Action for Increasing Diversity, Market Access, and Capacity in Oncology Registration Trials—Is Africa the Answer? Report From a Satellite Session of the Accelerating Anti-Cancer Agent Development and Validation Workshop. JCO Global Oncology. 2022;8:e2200117. https://doi.org/10.1200/GO.22.00117
4. Solarin O, Mohammed SI, Ndlovu N, Vanderpuye V, Olaiya V. Partnerships and collaborations: the right alliances for clinical trials in Africa. JCO Global Oncology. 2020;6: 954-958. https://doi.org/10.1200/jgo.19.00194
5. Ntekim A, Olopade OI. Innovative Strategies for Developing Biomarker-Informed Cancer Clinical Trials to Accelerate Progress in Precision Oncology in Sub-Saharan Africa. American Society of Clinical Oncology Educational Book. 2022;42:438-446. https://doi.org/10.1200/edbk_349955
6. Ngoma T, Adde M, Durosinmi M, et al. Treatment of Burkitt lymphoma in equatorial Africa using a simple three‐drug combination followed by a salvage regimen for patients with persistent or recurrent disease. British journal of haematology. 2012;158(6):749-762. https://doi.org/10.1111/j.1365-2141.2012.09236.x
7. Olatunji E, Swanson W, Patel S, et al. Challenges and opportunities for implementing hypofractionated radiotherapy in Africa: lessons from the HypoAfrica clinical trial. ecancermedicalscience. 2023;17. https://doi.org/10.3332%2Fecancer.2023.1508
8. Özdemir BC, Dotto G-P. Racial differences in cancer susceptibility and survival: more than the color of the skin? Trends in cancer. 2017;3(3):181-197. https://doi.org/10.1016/j.trecan.2017.02.002
9. Bentley AR, Callier SL, Rotimi CN. Evaluating the promise of inclusion of African ancestry populations in genomics. NPJ genomic medicine. 2020;5(1):5. https://doi.org/10.1038/s41525-019-0111-x
10. Alemayehu C, Mitchell G, Nikles J. Barriers for conducting clinical trials in developing countries-a systematic review. International journal for equity in health. 2018;17:1-11. https://doi.org/10.1186/s12939-018-0748-6
11. Koffi KG, Silué D, Laurent C, et al. AMAFRICA, a patient-navigator program for accompanying lymphoma patients during chemotherapy in Ivory Coast: a prospective randomized study. BMC cancer. 2019;19(1):1-8. https://doi.org/10.1186/s12885-019-6478-3
12. Firnhaber C, Swarts A, Jezile V, et al. Human papillomavirus vaccination prior to loop electroexcision procedure does not prevent recurrent cervical high-grade squamous intraepithelial lesions in women living with human immunodeficiency virus: a randomized, double-blind, placebo-controlled trial. Clinical Infectious Diseases. 2021;73(7):e 2211-e2216. https://doi.org/10.1093/cid/ciaa1456
13. Skiles JL, Chiang C, Li CH, et al. CYP3A5 genotype and its impact on vincristine pharmacokinetics and development of neuropathy in Kenyan children with cancer. Pediatric blood & cancer. 2018;65(3):e26854. https://doi.org/10.1002%2Fpbc.26854
14. Greene SA, De Vuyst H, John-Stewart GC, et al. Effect of cryotherapy vs loop electrosurgical excision procedure on cervical disease recurrence among women with HIV and high-grade cervical lesions in Kenya: a randomized clinical trial. Jama. 2019;322(16): 1570-1579. https://doi.org/10.1001/jama.2019.14969
15. Wagner GJ, Matovu JK, Juncker M, et al. Effects of a peer advocacy intervention on cervical cancer screening among social network members: results of a randomized controlled trial in Uganda. Journal of Behavioral Medicine. 2023;46(6):930-939. https://doi.org/10.1007%2Fs10865-023-00418-6
16. Nyirenda M, Ngongondo M, Kang M, et al. Early progression and immune reconstitution inflammatory syndrome during treatment of mild-to-moderate Kaposi sarcoma in sub-Saharan Africa and South America: Incidence, long-term outcomes and effects of early chemotherapy. Journal of acquired immune deficiency syndromes (1999). 2020;84(4):422. https://doi.org/10.1097%2FQAI.0000000000002361
17. Lin LL, Ndlovu N, Lowenstein J, et al. Quality Assurance in Clinical Trials Requiring Radiation Therapy in Sub-Saharan Africa. International Journal of Radiation Oncology* Biology* Physics. 2023;116(2):439-447. https://doi.org/10.1016/j.ijrobp.2022.11.042
18. Larkin J, Del Vecchio M, Ascierto P, et al. Vemurafenib in patients with BRAFv⁶⁰⁰ mutated metastatic melanoma: an open-label, multicentre, safety study. 2014. https://doi.org/10.1016/s1470-2045(14)70051-8
19. Unger JM, Cook E, Tai E, Bleyer A. The role of clinical trial participation in cancer research: barriers, evidence, and strategies. American Society of Clinical Oncology Educational Book. 2016;36:185-198. https://doi.org/10.1200/edbk_156686
20. Mboineki JF, Wang P, Dhakal K, Getu MA, Chen C. The effect of peer-led navigation approach as a form of task shifting in promoting cervical cancer screening knowledge, intention, and practices among urban women in Tanzania: a randomized controlled trial. Cancer Control. 2022;29:1073 2748221089480. https://doi.org/10.1177/10732748221089480
21. Deressa BT, Tigeneh W, Bogale N, Buwenge M, Morganti AG, Farina E. Short-course 2-dimensional radiation therapy in the palliative treatment of esophageal cancer in a developing country: a phase II study (Sharon Project). International Journal of Radiation Oncology* Biology* Physics. 2020;106(1):67-72. https://doi.org/10.1016/j.ijrobp.2019.10.004
22. Getu MA, Wang P, Addissie A, Seife E, Chen C, Kantelhardt EJ. The effect of cognitive behavioural therapy integrated with activity pacing on cancer‐related fatigue, depression and quality of life among patients with breast cancer undergoing chemotherapy in Ethiopia: A randomised clinical trial. International Journal of Cancer. 2023. https://doi.org/10.1002/ijc.34452
23. Udeh E, Amu O, Nnabugwu I, Ozoemena O. Transperineal versus transrectal prostate biopsy: our findings in a tertiary health institution. Nigerian journal of clinical practice. 2015;18(1):110-114. https://doi.org/10.4103/1119-3077.146991
24. Malan T, Moodley K. Phase 3 oncology clinical trials in South Africa: experimentation or therapeutic misconception? Journal of Empirical Research on Human Research Ethics. 2016;11(1):47-56. http://dx.doi.org/10.1177/1556264616637736
25. Gizaw M, Teka B, Ruddies F, et al. Uptake of cervical cancer screening in Ethiopia by self-sampling HPV DNA compared to visual inspection with acetic acid: a cluster randomized trial. Cancer Prevention Research . 2019;12(9):609-616. ttps://doi.org/10.1158/1940-6207.capr-19-0156
26. Gichuhi S, Macharia E, Kabiru J, et al. Topical fluorouracil after surgery for ocular surface squamous neoplasia in Kenya: a randomised, double-blind, placebo-controlled trial. The Lancet Global Health. 2016;4(6):e 378-e385. https://doi.org/10.1016%2FS2214-109X(16)30052-3
27. Linde DS, Andersen MS, Mwaiselage J, Manongi R, Kjaer SK, Rasch V. Effectiveness of one-way text messaging on attendance to follow-up cervical cancer screening among human papillomavirus–positive Tanzanian women (Connected2Care): parallel-group randomized controlled trial. Journal of Medical Internet Research. 2020;22(4):e15863 . https://doi.org/10.2196/15863
28. Sossauer G, Zbinden M, Tebeu P-M, Fosso GK, Untiet S, Vassilakos P, Petignat P. Impact of an educational intervention on women's knowledge and acceptability of human papillomavirus self-sampling: a randomized controlled trial in Cameroon. PloS one. 2014;9(10):e109788. https://doi.org/10.1371/journal.pone.0109788
29. Chagaluka G, Paintsil V, Renner L, et al. Improvement of overall survival in the collaborative Wilms tumour Africa project. Pediatric Blood & Cancer. 2020;67(9):e28383. https://doi.org/10.1002/pbc.28383
30. Stocks J, Ibrahim S, Park L, Huchko M. Mobile phone ownership and use among women screening for cervical cancer in a community-based setting in Western Kenya: Observational study. JMIR Public Health and Surveillance. 2022;8(6):e28885. https://doi.org/10.2196%2F28885
31. Graef KM, Okoye I, Ohene Oti NO, Dent J, Odedina FT. Operational strategies for clinical trials in Africa. JCO Global Oncology. 2020;6:973-982. https://doi.org/10.1200/jgo.19.00204
32. Pace LE, Dusengimana JMV, Shulman LN, et al. Cluster randomized trial to facilitate breast cancer early diagnosis in a rural district of Rwanda. Journal of Global Oncology. 2019; 5:1-13. https://doi.org/10.1200/jgo.19.00209
33. Huchko MJ, Ibrahim S, Blat C, Cohen CR, Smith JS, Hiatt RA, Bukusi E. Cervical cancer screening through human papillomavirus testing in community health campaigns versus health facilities in rural western Kenya. International Journal of Gynecology & Obstetrics. 2018;141(1):63-69. https://doi.org/10.1002/ijgo.12415
34. Erlandson KM, Gudza I, Fiorillo S, et al. Relationship of vitamin D insufficiency to AIDS-associated Kaposi's sarcoma outcomes: retrospective analysis of a prospective clinical trial in Zimbabwe. International Journal of Infectious Diseases. 2014;24:6-10. https://doi.org/10.1016%2Fj.ijid.2014.02.006
35. Odedina FT, Shamley D, Okoye I, et al. Landscape of oncology clinical trials in Africa. JCO Global Oncology. 2020;6:932-941. https://doi.org/10.1200/jgo.19.00189
36. Okunade KS, Soibi-Harry A, John-Olabode S, et al. Impact of mobile technologies on cervical cancer screening practices in Lagos, Nigeria (mHealth-Cervix): a randomized controlled trial. JCO Global Oncology. 2021;7:1418-1425. https://doi.org/10.1200/go.21.00258
37. Chigbu CO, Onyebuchi AK. See-and-treat management of high-grade squamous intraepithelial lesions in a resource-constrained African setting. International Journal of Gynecology & Obstetrics. 2014;124(3):204-206. https://doi.org/10.1016/j.ijgo.2013.07.040
38. Toto N, Douglas E, Gmeiner M, et al. Conducting clinical trials in sub-Saharan Africa: challenges and lessons learned from the Malawi Cryptosporidium study. Trials. 2020;21:1-8. https://doi.org/10.1186/s13063-020-04620-8
39. Esterhuizen TM, Li G, Young T, Zeng J, Machekano R, Thabane L. Advancing collaborations in health research and clinical trials in Sub-Saharan Africa: development and implementation of a biostatistical collaboration module in the Masters in Biostatistics Program at Stellenbosch University. Trials. 2021;22(1):1-9. https://doi.org/10.1186/s13063-021-05427-x
40. Page MJ, McKenzie JE, Bossuyt PM, et al. The PRISMA 2020 statement: an updated guideline for reporting systematic reviews. International journal of surgery. 2021;88:1059 06.https://doi.org/10.1016/j.ijsu.2021.105906
41. Bond MC, Pritchard S. Understanding clinical trials in childhood cancer. Paediatrics & child health. 2006;11(3):148-150. http://dx.doi.org/10.1093/pch/11.3.148
42. Amoako E, Jumbam DT, Bediako Y. Unseen and unheard: African children with cancer are consistently excluded from clinical trials. BMJ Global Health. 2021;6(1). https://doi.org/10.1136/bmjgh-2020-004750
43. Hough R, Sandhu S, Khan M, et al. Are survival and mortality rates associated with recruitment to clinical trials in teenage and young adult patients with acute lymphoblastic leukaemia? A retrospective observational analysis in England. BMJ open. 2017;7(10). https://doi.org/10.1136/bmjopen-2017-017052
44. NCCN. NCCN Oncology Research Program (ORP). https://www.nccn.org/education-research/nccn-oncology-research-program/
45. Yaris N, Mandiracioglu A, Büyükpamukcu M. Childhood cancer in developing countries. Pediatric hematology and oncology. 2004;21(3):237-253. https://doi.org/10.1080/08880010490276971
46. Opinion: D. childhood cancers in Ghana— we must do more to protect the vulnerable among US. 2020. https://www.devex.com/news/sponsored/opinion-childhood-cancers-in-ghana-we-must-do-more-to-protect-the-vulnerable-among-us-97841
47. Magrath I, Adde M, Shad A, et al. Adults and children with small non-cleaved-cell lymphoma have a similar excellent outcome when treated with the same chemotherapy regimen. Journal of Clinical Oncology. 1996;14(3):925-934. https://doi.org/10.1200/jco.1996.14.3.925
48. Adde M, Shad A, Venzon D, et al. Additional chemotherapy agents improve treatment outcome for children and adults with advanced B-cell lymphomas. Paper presented at: Seminars in oncology, 1998. https://europepmc.org/article/med/9578060
49. Gad-El-Mawla N, Hussein MH, Abdel-Hadi S, El-Taneer O, Adde M, Magrath I. Childhood non-Hodgkin's lymphoma in Egypt: preliminary results of treatment with a new ifosfamide-containing regimen. Cancer Chemotherapy and Pharmacology. 1989;24:S 20-S23. https://doi.org/10.1007/bf00253233
50. Advani S, Pai S, Adde M, et al. Preliminary report of an intensified, short duration chemotherapy protocol for the treatment of pediatric non-Hodgkin's lymphoma in India. Annals of oncology. 1997;8(9):893-897. https://doi.org/10.1023/a:1008228529397
51. Ngwa W, Addai BW, Adewole I, et al. Cancer in sub-Saharan Africa: a lancet oncology commission. The Lancet Oncology. 2022;23(6):e251-e312. https://doi.org/10.1016/s1470-2045(21)00720-8
52. Aluwini S, Pos F, Schimmel E, et al. Hypofractionated versus conventionally fractionated radiotherapy for patients with prostate cancer (HYPRO): acute toxicity results from a randomised non-inferiority phase 3 trial. The Lancet Oncology. 2015;16(3):274-283. https://doi.org/10.1016/S1470-2045(15)00567-7
53. Aluwini S, Pos F, Schimmel E, et al. Hypofractionated versus conventionally fractionated radiotherapy for patients with prostate cancer (HYPRO): late toxicity results from a randomised, non-inferiority, phase 3 trial. The Lancet Oncology. 2016;17(4):464-474. https://doi.org/10.1016/S1470-2045(14)70482-6
54. Dearnaley D, Syndikus I, Mossop H, et al. Conventional versus hypofractionated high-dose intensity-modulated radiotherapy for prostate cancer: 5-year outcomes of the randomised, non-inferiority, phase 3 CHHiP trial. The Lancet Oncology. 2016;17(8):1047-1060. https://doi.org/10.1016/S1470-2045(16)30102-4