Oncology training and education initiatives in low and middle income countries: a scoping review
Safiya Karim1, Zahra Sunderji2, Matthew Jalink3, Sahar Mohamed4, Indranil Mallick5, Susan Citonje Msadabwe-Chikuni6, Nancy J Delgarno7, Nazik Hammad3 and Scott Berry3
1Department of Medical Oncology, University of Calgary, Tom Baker Cancer Centre, 1331 29 St NW, Calgary, AB T2N 4N2, Canada
2Department of Family Medicine, University of British Columbia, Vancouver, BC V6T 2A1, Canada
3Department of Oncology, Queen’s University, Kingston, ON K7L 5P9, Canada
4Department of Public Health Sciences, Queen’s University, Kingston, ON K7L 3N6, Canada
5Department of Radiation Oncology, Tata Medical Center, Kolkata 700 160, India
6Cancer Diseases Hospital, Lusaka 10101, Zambia
7Office of Professional Development and Educational Scholarship, Faculty of Health Sciences, Queen’s University, Kingston, ON K7L 0E9, Canada
Background: The global cancer burden falls disproportionately on low and middle-income countries (LMICs). One significant barrier to adequate cancer control in these countries is the lack of an adequately trained oncology workforce. Oncology education and training initiatives are a critical component of building the workforce. We performed a scoping review of published training and education initiatives for health professionals in LMICs to understand the strategies used to train the global oncology workforce.
Methods: We searched Ovid MEDLINE and Embase from database inception (1947) to 4 March 2020. Articles were eligible if they described an oncology medical education initiative (with a clear intervention and outcome) within an LMIC. Articles were classified based on the target population, the level of medical education, degree of collaboration with another institution and if there was an e-learning component to the intervention.
Findings: Of the 806 articles screened, 25 met criteria and were eligible for analysis. The majority of initiatives were targeted towards physicians and focused on continuing medical education. Almost all the initiatives were done in partnership with a collaborating organisation from a high-income country. Only one article described the impact of the initiative on patient outcomes. Less than half of the initiatives involved e-learning.
Conclusions: There is a paucity of oncology training and education initiatives in LMICs published in English. Initiatives for non-physicians, efforts to foster collaboration within and between LMICs, knowledge sharing initiatives and studies that measure the impact of these initiatives on developing an effective workforce are highly recommended.
Keywords: medical education, low and middle-income countries, e-health, oncology, scoping review
Correspondence to: Safiya Karim
Publication costs for this article were supported by ecancer (UK Charity number 1176307).
Copyright: © the authors; licensee ecancermedicalscience. This is an Open Access article distributed under the terms of the Creative Commons Attribution License (http://creativecommons.org/licenses/by/4.0), which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.
In 2018, it was estimated that 18.1 million new cancer cases and 9.6 million cancer deaths occurred worldwide . By 2040, the World Health Organization (WHO) estimates that global cancer cases will reach 29.5 million and there will be 16.5 million cancer related deaths . Although high income countries (HICs) have higher cancer incidence rates, cancer mortality rates are significantly higher in low and middle-income countries (LMICs) (defined by the World Bank as countries with a gross national income of $12,535 or less in 2019 ) and continue to rise . The proportion of cancer deaths in LMICs is expected to increase to 75% by 2030 [2, 5].
One of the major barriers to cancer control in LMICs is training an adequate oncology workforce . On average, LMICs have 1.3 physicians and 2.5 nurses per 1,000 people compared with 3.1 physicians and 10.9 nurses per 1,000 people in HICs [7, 8]. As a result, case volumes and clinical workload are significantly higher for oncology providers in LMICs compared with HICs . There are significant shortages in the oncology workforce, including specialists with skills in pathology, radiation and medical oncology . Furthermore, the absence of sufficient oncology training programmes and lack of focus on cancer care during medical school provide significant challenges towards training and retaining cancer care professionals . Given the rising cancer burden and limited workforce, it is essential to develop, promote and support local oncology education and training initiatives in LMICs.
Some traditional approaches to building the oncology workforce in LMICs such as travelling to HICs to acquire necessary skills may have unintended harmful consequences to LMIC health care systems . The ‘brain drain’, when trainees do not return to their native country to practice medicine, has been recognised by the WHO as a major problem that propagates imbalances in the global health workforce . To combat this, several global oncology initiatives have focused on building local capacity to provide high-quality cancer care . One such mechanism involves building partnerships between institutions facilitating bi-directional learning and knowledge transfer, and enabling local retention and capacity building . Furthermore, e-learning is increasingly being used to supplement learning in LMICs. Given the absence of a systematic examination of oncology education and training initiatives in LMICs, this scoping review was performed.
Scoping reviews facilitate the examination of a broad topic of interest with the purpose of identifying gaps in the evidence, clarifying concepts and synthesising what is known about a topic . We selected a scoping review methodology due to the paucity of empirical literature on this subject as well as to provide an overview of available information regarding oncology education and training in LMICs. This review aims to provide a description of the depth and breadth of the educational initiatives within this field . We applied a rigorous approach to this scoping review through a five-step approach to ensure reliability: (1) identify the research question, (2) identify relevant studies, (3) select studies, (4) chart the data and (5) collate, summarise and report the results [13, 14].
Identify the research question
Our scoping review was centred on the following research question: What has been published on oncology education and training to healthcare professionals in LMICs between the years 1947 and 2020?
Identify relevant studies
A qualified medical librarian assisted in the development and execution of the search strategy in two major electronic databases: Ovid MEDLINE and Embase up to 4 March 2020 (date of the search). We felt that these two databases would capture the majority of the published literature in this field and that including additional databases would not yield a significant increase in the number of results. The search string is shown in Supplementary Appendix A. The reference lists of relevant review papers and articles found during the search of the databases were also scanned for additional eligible articles.
A two-stage standardised screening process was used to evaluate the eligibility of the articles identified in the search using Covidence systematic review software (Covidence Systematic Review Software 2019). Two independent reviewers (MJ and SM) screened the title and abstracts of the captured articles using the pre-defined eligibility criteria. The same reviewers screened the full-text articles that passed stage 1 review. If there was uncertainty as to whether an article should be included, a third author was asked to provide input (SK).
We applied pre-determined eligibility criteria to the selection process. Eligible articles described a specific oncology medical education initiative targeted towards individuals residing in a LMIC. The initiative must have described one or more specific interventions as well as an outcome of that intervention. Oncology education was broadly defined to include any teaching within the following disciplines: surgical oncology, medical oncology, radiation oncology, haematologic oncology, gynaecological oncology and/or topics: research skills, pathology, diagnosis, treatment, supportive care or palliative care. We excluded any article that did not meet the above criteria as well as review articles, letters, commentaries, book chapters, abstracts and unpublished manuscripts.
Chart the data
Data were extracted using a pre-developed data extraction tool which included the terms: author, year, geographical area, host county(ies), host site/institution, collaborations, partner country, partner institution, location of training, project title, target population, level of education, use of e-learning, oncology discipline, programme duration (i.e. short (up to 1 month), medium (>1 month to 1 year), long-term (>1 year)), educational outcome(s) and funding. For the purposes of this study, e-learning was defined as learning facilitated by electronic technologies and involving access to a curricula outside of a traditional classroom, often in the form of interactive multimedia, audiovisual clips and virtual models .
Collate, summarise and report the results
A descriptive numerical summary of the characteristics of the studies was performed. Tables were created to show the overall number of studies included, the target study population, level of medical education, publication year, use of e-learning, oncology discipline, programme duration, educational outcome(s) and funding. As per scoping review methodology, an assessment of the quality of the included studies was not performed .
We also classified the impact of the studies’ based on the 4-level model by Kirkpatrick that measures the outcomes of a particular education study or training programme . These levels include: (1) reaction, (2) learning, (3) behaviour and (4) results.
After removal of duplicates, the initial search yielded 806 articles. Of these, 544 did not describe a specific medical education intervention. The remaining 261 full text articles were assessed for eligibility, and 201 did not meet the eligibility criteria. Sixty articles met our inclusion criteria, of which 33 were only in abstract form. Two articles were not available in full-text format. Twenty-five full-text articles were included in this scoping review (Figure 1). Of the 25 articles included, nine were quantitative studies [17–25], eleven were qualitative studies [27–36] and five were mixed method studies [37–41]. An overview of the selected articles is available in Table 1. Full details are available in Supplementary Tables 1 and 2.
Target population and location
Fifteen of the twenty-five articles described an education initiative for physicians [17, 20, 23–25, 27, 29, 30, 33, 35–40]. Four articles described an initiative for nurses [19, 21, 28, 31], and one article was aimed at pharmacists . Five articles described initiatives for more than one member of the health care team: three initiatives were for physicians and nurses [18, 22, 32], one was for physicians, nurses and pharmacists  and one was for physicians, nurses and other non-health professionals .
Thirteen initiatives were conducted in the Middle East/Africa [17, 19, 20, 25, 26, 29, 32, 34, 35, 38–41], six in the Americas [18, 23, 24, 27, 28, 31] and five in Asia/Pacific [21, 30, 33, 36, 37]. Project ECHO, a tele-mentoring programme for cervical cancer prevention was conducted in all three of these regions (Figure 2) .
Figure 1. PRISMA (Preferred Reporting Items for Systematic Reviews and Meta-Analyses) chart.
Level, topic and duration of education initiative
Continuing medical education (CME) initiatives (8 of 15) were the most common level of medical education for physicians, followed by graduate medical education (GME) initiatives (3 of 15), and a combination of CME/GME initiatives (2 of 15). There were only two initiatives for medical students (undergraduate medical education (UME)) [23, 33]. All four initiatives targeting nurses [19, 21, 28, 31] and the one initiative for pharmacists  were CME.
The initiatives focused on a range of oncology disciplines and topics. There were four initiatives in gynaecologic oncology (all in cervical cancer) [19, 22, 34, 39], four in medical/haematologic oncology [21, 29, 30, 41], four in paediatric oncology [18, 28, 31, 35], two in radiation oncology [17, 37], one in pathology  and one in surgical oncology . There was one initiative that focused on both surgical oncology and pathology . In addition, there was one intervention related to supportive care  and one on conducting population health research . There were six initiatives that focused on multiple topics within oncology [23, 25, 32, 33, 38, 40]. There were nine short-term [20, 23, 25, 26, 31–34, 39], six medium-term [19, 24, 27, 28, 36, 40] and eight long-term initiatives [18, 21, 22, 29, 30, 35, 37, 41]. Two articles did not specify the length of their initiative [17, 38].
Table 1. Overview of the 25 manuscripts included in the scoping review.
Figure 2. Low-and-middle income countries with educational initiatives highlighted in the 25 studies.
Use of e-learning
Eleven articles described a component of e-learning in their educational intervention. Six studies included the use of telehealth technology [18, 22, 24, 26, 35, 37], one used smartphone-based training , two used online teaching modules [17, 39] and one used simulations .
Almost all (24 of 25) educational initiatives were implemented with a collaborating organisation. The collaborating organisations were most often located in HICs, including fourteen from the United States [17, 19–22, 24–27, 29–32, 40], three from Canada [18, 35, 39], one from both the United States and Canada , two from the United Kingdom [38, 41] and one from Hong Kong . Two articles described collaborations with a variety of international agencies, including the WHO [33, 34], and the International Agency for Research on Cancer (IARC) . The article by Agrawal et al  was the only study to describe an in-country collaboration between two different institutions in India. Twelve articles noted that the collaboration between institutions was highly rewarding and beneficial in fostering bi-directional learning [18, 20, 21, 24, 30, 32, 34–36, 38, 40, 41].
The majority of the educational initiatives took place solely within the host LMIC (i.e. in-country training). Five initiatives had both in-country and out-of-country components to their training programmes, which involved travel to the collaborating organisation [24, 27, 29, 36, 41]. Only one initiative described an intervention that was solely located out-of-country, where participants spent the entire 3–6 weeks training at the collaborating organisation .
Seven studies focused on building local capacity through their medical education initiative. Five initiatives implemented a ‘train the trainer’ model where learners who had completed the educational intervention previously would then serve as the instructor (‘trainer’) for the next cohort of learners [27, 28, 34, 36, 38]. This was done to build capacity and self-sustainability within the LMIC. Barron et al  described the future of their educational programme to include a focus on preceptorship development so that nurses would become skilled teachers thereby helping to ensure that the training programme becomes self-sustaining. Fish et al  describe the potential to build local capacity as a result of their educational intervention by laying the foundation for continued international research collaborations and connections.
Impact of educational initiative
Based on the Kirkpatrick programme evaluation training model’s 4-levels of impact, 10 articles exclusively measured reaction outcomes [18, 22, 23, 26, 27, 29, 32, 33, 36, 37]. These were assessed primarily though surveys using Likert-scale, multiple choice and/or open-ended questions. Seven articles exclusively measured learning outcomes [17, 19, 20, 25, 30, 31, 34], most commonly through pre/post written tests. Two articles exclusively measured behaviour outcomes [35, 41]. For example, Lewis and Tibenderana  showed that after a series of training sessions in the safe handling, preparation and administration of chemotherapy, there was an increase in the rate of documented chemotherapy prescriptions which were correctly administered to patients compared to the pre-training levels. Three articles reported both reaction and learning outcomes [28, 38, 40], two articles learning and behaviour outcomes [24, 39] and one article reported learning and results outcomes . The result outcome in this article pertained to the success of a bone marrow transplant programme in Bangladesh in the months following training of nurses.
Several challenges were identified in implementing the educational initiative. Language barriers [17, 27, 34] and the lack of protected time for the learners to participate in the initiative were often identified [27, 28, 31]. Four articles also noted encountering technical problems [19, 22, 26, 37] (i.e. Internet connectivity, videoconferencing equipment dysfunction) and four articles described infrastructure limitations (i.e. limited medical supplies, lack of accurate medical records) within the LMIC [19, 20, 22, 38]. The logistics and expenses of international travel was identified as a challenge in three articles [27, 29, 40]. Cultural differences and political/workforce changes were also highlighted in one article . Eleven articles did not disclose their challenges in the implementation of the initiative [20–24, 28, 29, 31, 38, 40, 41].
The majority of the initiatives were partially or fully funded by external grants and/or by a charitable foundation located in the partner country [17, 18, 22, 24, 27, 31, 34, 36]. One initiative was partially funded by the collaborating country’s institution  and one initiative was partially funded by the collaborating country’s government  while another was funded by a grant through the host country’s government . Other sources of funding included research institutes [22, 23], a pharmaceutical company  (partial funding) and a fellowship award . Ten articles did not disclose the source of funding for their initiative [20, 21, 25, 26, 28, 30, 33, 35, 38, 39].
Medical education and training initiatives in oncology are a critical element in developing an effective workforce to manage rising cancer incidence and mortality rates in LMICs. In this scoping review, we identified 25 articles that described an oncology medical education initiative. The majority of these initiatives were aimed at physicians and CME. Almost all the initiatives were in partnership with a collaborating organisation from a HIC. In addition, based on Kirkpatrick’s 4-level model, the majority of initiatives evaluated only reaction outcomes. Finally, less than half of the initiatives involved a component of e-learning.
With only 25 articles identified, there is a clear paucity of published literature on educational initiatives in the field of oncology. This may be due to an absence of studies investigating this topic, or these initiatives are not being widely published in the peer-reviewed medical literature. For example, in LMICs, the emphasis may be on implementing an educational programme, and due to time, financial and/or language constraints, publication of such work, at least in full-text format, may not be possible. Over time, we found a gradual increase in the number of published manuscripts, with only six articles published before 2010 compared to 19 between 2010 and 2020 (Figure 3). This increase is encouraging as publication allows others to learn important lessons for design and implementation of medical education initiatives in oncology in LMICs. Where possible, efforts to assist educators in overcoming obstacles to conducting and publishing studies related to their initiatives could be considered. On the other hand, less onerous methods of disseminating important findings should also be encouraged.
The majority of the initiatives included in our scoping review were aimed towards physicians in LMICs. While the training of physicians is important, well-trained and skilled allied health professionals, including nurses and pharmacists, are also critical for the effective delivery of cancer care . Education and training of other non-physician providers is integral to the workforce crisis in LMICs, and is necessary in order to build a strong cancer-care delivery infrastructure. Furthermore, inter-professional education and collaboration has been proposed by the WHO as a promising solution to ensure the appropriate supply, mix and distribution of the global health workforce . Only five studies in our scoping review targeted multiple members of the healthcare team [18, 22, 32, 34, 41], showing that further focus on inter-professional education initiatives is warranted.
Our study also found that the majority of initiatives were focused on CME. This type of medical education is important for practicing health care providers to maintain competence and learn about new and developing areas within their field. However, if foundational education in oncology is not being provided in the earlier stages of health professions education, individuals may not have adequate exposure to the field in order to choose it as a speciality or profession. The lack of focus on oncology in medical school curricula in LMICs may have been due to an increased focus on infectious diseases, which historically has been the major concern in these countries . However, with the growing burden of cancer in LMICs, it is also important to include cancer as a core discipline in undergraduate health professions education.
Over the past few decades, there has been increased interest from institutions from HICs to form partnerships with those from LMICs . However, there is cause for concern that in many cases these partnerships may be driven by the funding and interests of the HIC partner, and that the needs of the LMIC institution are not fully considered . Other concerns with these ‘North-South’ partnerships have also been raised, including the low degree of sustainability and a focus on short-term goals instead in long-term capacity building . While several of the initiatives identified in our review had long-term partnerships and there was a focus on capacity building, almost all of these partnerships were with organisations from HICs. In recent years, ‘South-South’ collaborations (i.e. from within the same LMIC or between different LMICs) have gained popularity in the delivery of health professionals education due to several advantages, including better alignment with local needs, ability to engage senior leaders within the institutions and ensuring long-term sustainability .
Figure 3. Number of published oncology medical education initiatives per year.
The vast majority of the studies in our scoping review used either reaction or learning outcomes as their method of evaluation. These represent the two lowest levels of impact in Kirkpatrick’s framework . These evaluation methods are the most easily measured and implemented, but also are the least effective over time. Conversely, behaviour and result outcomes are more difficult to implement, take longer to measure and are often more costly. However, the goal of any medical educational initiative should be to improve patient outcomes, which are evaluated in level four of the Kirkpatrick model. As oncology medical education initiatives become more prevalent, and as collaborations develop into longer-term relationships, it will be important that all four levels of Kirkpatrick’s model are evaluated to improve the impact of these initiatives.
LMICs require effective and affordable medical education strategies to address the limited and poorly trained workforce. In a recent systematic review of e-learning for medical education in LMICs from 2007 to 2017, Barteit et al  included 52 articles and concluded that e-learning in LMICs has not met its expected potential. They proposed that some reasons for the limited success of e-learning implementation may be due to financial resources and that educational organisations may not be giving e-learning a strong mandate as an educational method. Our findings, where only 11 of the 25 studies used a component of e-learning as part of their educational initiative, support the conclusion that e-learning may still be underutilised as an educational method in LMICs. Similarly, in a scoping review of e-learning for primary healthcare, Reeves et al  found that of 23 studies published on this topic, only two were from LMICs. E-learning initiatives have the potential to offer highly effective, low-cost and high-quality education, especially in resource limited settings but will likely require a combined effort and commitment from a variety of national and international stakeholders in order to meet its full potential .
Our study should be interpreted in the context of certain limitations. First, we employed a scoping review methodology that does not assess the rigour or quality of the included studies. Second, we chose to include only two databases (Ovid MEDLINE and Embase) and excluded programmes in the gray literature (i.e. abstracts), where many educational initiatives may have been highlighted. Finally, despite efforts to optimise the search terms in this scoping review, we may have missed certain medical education initiatives that were indexed under different terms.
In conclusion, oncology training and education initiatives for health care professionals in LMICs are an essential component in building the workforce to address the growing cancer burden and to ensure that the workforce is well-trained to provide excellent care to cancer patients. This scoping review identifies a broad range of initiatives that have been published and the strategies used to implement them. In the coming years, we recommend that educators share valuable lessons learned related to the creation and execution of their programmes, including, where possible, performing and publishing studies of their work in order to optimise educational strategies. This may be achieved by establishing an online registry of oncology educational initiatives occurring across various LMICs and/or organising regional/national focused meetings that aim to share knowledge on best practices for delivering educational programmes. Furthermore, the design and delivery of oncology education for non-physician health professionals and between various health professionals should be prioritised to ensure optimal collaboration and teamwork within the global oncology workforce. Finally, in addition to long-term partnerships with HIC organisations, we encourage organisations within LMICs to foster collaborative relationships within their country or from other LMICs to better address local needs, contexts and ensure long-term sustainability of their educational initiatives.
This manuscript was supported by the University of Calgary Global Oncology Programme.
Conflicts of interest statement
The authors have no conflicts of interest.
1. Bray F, Ferlay J, and Soerjomataram I, et al (2018) Global cancer statistics 2018: GLOBOCAN estimates of incidence and mortality worldwide for 36 cancers in 185 countries CA Cancer J Clin 68(6) 394–424 https://doi.org/10.3322/caac.21492 PMID: 30207593
2. International Agency for Research on Cancer Cancer tomorrow [https://gco.iarc.fr/tomorrow/home] Date accessed: 1/02/2021
3. The World Bank World bank country and lending groups (Washington: World Bank)
4. Torre L, Siegel R, and Ward E, et al (2016) Global cancer incidence and mortality rates and trends-an update Cancer Epidemiol Biomarkers Prev 25 16–27 https://doi.org/10.1158/1055-9965.EPI-15-0578
5. The Lancet (2018) GLOBOCAN 2018: counting the toll of cancer Lancet 392 985 https://doi.org/10.1016/S0140-6736(18)32252-9 PMID: 30264708
6. Patel J, Galsky M, and Chagpar A, et al (2011) Role of american society of clinical oncology in low-and middle-income countries J Clin Oncol 29(22) 3097–3102 PMID: 21709190
7. The World Bank (2021) Physicians (per 1,000 people) [https://data.worldbank.org/indicator/SH.MED.PHYS.ZS] Date accessed 5/01/2021
8. The World Bank (2021) Nurses and midwives (per 1,000 people) [https://data.worldbank.org/indicator/SH.MED.NUMW.P3] Date accessed 5/01/2021
9. Fundytus A, Sullivan R, and Vanderpuye V, et al (2018) Delivery of global cancer care: an international study of medical oncology workload J Glob Oncol 4 1–11
10. Asirwa FC, Greist A, and Busakhala N, et al (2016) Medical education and training: building in-country capacity at all levels J Clin Oncol 34(1) 36–42
11. Mejia A, Pizurki H, and Royston E (1979) Physician and Nurse Migration: Analysis and Policy Implications (Geneva: WHO)
12. Peters M, Godfrey C, and McInerney P, et al (2020) Chapter 11: Scoping reviews (2020 version) JBI Manual for Evidence Synthesis eds E Aromataris and Z Munn https://doi.org/10.46658/JBIMES-20-12
13. Levac D, Colquhoun H, and O’Brien K (2010) Scoping studies: advancing the methodology Implement Sci 5 69 https://doi.org/10.1186/1748-5908-5-69 PMID: 20854677 PMCID: 2954944
14. Arksey H, and O’Malley L (2005) Scoping studies: towards a methodological framework Int J Soc Res Methodol 8(1) 19–32 https://doi.org/10.1080/1364557032000119616
15. Ruiz J, Mintzer M, and Leipzig R (2006) The impact of e-learning in medical education Acad Med 81(3) 207–212 https://doi.org/10.1097/00001888-200603000-00002 PMID: 16501260
16. Kirkpatrick D (1996) Great ideas revisited. Techniques for evaluating training programs. Revisiting Kirkpatrick’s fourlevel model Train Dev 50 54–59
17. Abigideiri M, Schreibmann E, and Switchenko J, et al (2019) Prospective international pilor study evaluating the efficancy of a self-guided contouring teaching module with integrated feedback for transitioning from 2D to 3D treatment planning J Glob Oncol 5 1–16
18. Adler E, Alexis C, and Ali Z, et al (2015) Bridging the distance in the Carribean: telemedicine as a means to build capacity for care in paediatric cancer and blood disorders Stud Heal Technol Inf 209 1–8
19. Asgary R, Adongo PB, and Nwameme A, et al (2016) mHealth to train community health nurses in Visual Inspection with Acetic Acid for cervical cancer screening in Ghana J Low Genit Track Dis 20(3) 239–242 https://doi.org/10.1097/LGT.0000000000000207
20. Awuah B, Martin I, and Takyi V, et al (2011) Implementation of a percutaneous core needle biopsy training program: results from the University of Michigan-Komfo Anokye Teaching Hopsital breast cancer research partnership Ann Surg Oncol 18(4) 957–960 https://doi.org/10.1245/s10434-010-1422-4 PMCID: 3073403
21. Barron A, Moran J, and Nina S, et al (2018) Building specialized nursing practice capacity in Bangladesh: an educational program to prepare nurses to care for oncology and bone marrow transplant patients in Dhaka, Bangladesh J Glob Oncol 4 1–6
22. Lopez M, Baker E, and Mibourne A, et al (2017) Project echo: a telementoring program for cervical cancer prevention and treatment in low-resource settings J Glob Oncol 3(5) 658–665 https://doi.org/10.1200/JGO.2016.005504 PMID: 29094102 PMCID: 5646881
23. de Camargo C, Schoueri J, and Neto F, et al (2018) Medical student oncology congress: designed and implemented by Brazilian medical students J Cancer Educ 33 1151–1158 https://doi.org/10.1007/s13187-017-1215-6
24. Santiago T, Jenkins J, and Pedrosa F, et al (2012) Improving the histopathologic diagnosis of pediatric malignancies in a low-resource setting by combining focused training and telepathology strategies Pediatr Blood Cancer 59 221–225 https://doi.org/10.1002/pbc.24071 PMID: 22315236
25. Shah N, Soliman A, and Banerjee M, et al (2006) Knowledge gained after a brief CME module on breast cancer diagnosis J Cancer Educ 21 169–174 https://doi.org/10.1207/s15430154jce2103_17
26. Alfaar AS, Kamal S, and AbouElnaga S, et al (2012) International telepharmacy education: another venue to improve cancer care in the developing world Telemed J E-Health 8(6) 470–474 https://doi.org/10.1089/tmj.2011.0182
27. Arnold LD, Barnoya J, and Gharzouzi EN, et al (2014) A training programme to build cancer research capacity in low- and middle-income countries: findings from Guatemala Bull World Health Organ 92 297–302 [doi:http://dx.doi.org/10.2471/BLT.13.126516] https://doi.org/10.2471/BLT.13.126516 PMID: 24700998 PMCID: 3967575
28. Wilimas J, Donahue N, and Chammas G, et al (2003) Training subspecialty nurses in developing countries: methods, outcomes and cost Med Pediatr Oncol 41 136–140 https://doi.org/10.1002/mpo.10242 PMID: 12825219
29. Butonzi J, Forbes V, and Kigonya C, et al (2019) Global oncology fellowship electives: the impact on cancer care and international collaborations Rwanda Med J 76(4) 1–5
30. Carbone P (1991) Developing a postgraduate medical oncology training program in Taipei, Taiwan, Republic of China J Clin Oncol 9(2) 335–338 https://doi.org/10.1200/JCO.19220.127.116.115 PMID: 1988580
31. Day S, Garcia J, and Antillon F, et al (2012) A sustainable model for pediatric oncology nursing education in low-income countries Pediatr Blood Cancer 58(2) 163–166 https://doi.org/10.1002/pbc.24007
32. Nwogu C, Mahoney M, and George S, et al (2014) Promoting cancer control training in resource limited environments: Lagos, Nigeria J Cancer Educ 29 14–18 https://doi.org/10.1007/s13187-013-0581-y
33. Kapoor N, Haagedoorn E, and de Vries J (2006) The UICC/WHO-CCCE cancer education project: an Indian experience J Cancer Educ 21(3) 182–185 https://doi.org/10.1207/s15430154jce2103_19
34. Miller D, Okolo C, and Mirabal Y, et al (2007) Knowledge dissemination and evaluation in a cervical cancer screening implementation program in Nigeria Gynecol Oncol 107 S196–207 https://doi.org/10.1016/j.ygyno.2007.07.014 PMID: 17889285
35. Qaddoumi I, Mansour A, and Musharbash A, et al (2007) Impact of telemedicine on pediatric neuro-oncology in a developing country: the Jordanian-Canadian experience Pediatr Blood Cancer 48 39–43 https://doi.org/10.1002/pbc.21085
36. Tam P, Wong K, and Li L, et al (2013) Internationalization: the Hong-Kong-China experience as a model for collaborative education in Asia Pediatr Surg Int 29 1053–1059 https://doi.org/10.1007/s00383-013-3407-4 PMID: 23975023
37. Agrawal S, Maurya A, and Shrivastava K, et al (2011) Training the trainees in radiation oncology with telemedicine as a tool in a developing country: a two-year audit Int J Telemed Appl 2011 230670 PMID: 21603023 PMCID: 3095242
38. Eastin J (2019) Adressing the burden of cancer in East Africa through cascaded training Cancer Control 2019 64–68
39. Elit LM, Rosen B, and Jimenez W, et al (2010) Teaching cervical cancer surgery in low- or middle-resource countries Int J Gynecol Cancer 20 1604–1608 [http://ovidsp.ovid.com/ovidweb.cgi?T=JS&CSC=Y&NEWS=N&PAGE=fulltext&D=med5&AN=21370604] [http://sfx.scholarsportal.info/uhn?sid=OVID:medline&id=pmid:21370604&id=doi:&issn=1048-891X&isbn=&volume=20&issue=9&spage=1604&pages=1604-8&date=2010&title=International]
40. Fish M, Parkes J, and Dharsee N, et al (2019) POETIC (program for enhanced training in cancer): an initial experience of supporting capacity building for oncology training in Sub-Saharan Africa Oncologist 24(23) 1557–1561 https://doi.org/10.1634/theoncologist.2019-0207 PMID: 31182656 PMCID: 6975941
41. Lewis P (2019) Improving the safety of chemotherapy treatment for cancer patients in Uganda Cancer Control 2019 59–62
42. Fadelu T, and Shulman L (2018) Health policy: towards greater equity in the global oncology workforce Nat Rev Clin Oncol 15(5) 270–272 https://doi.org/10.1038/nrclinonc.2018.31 PMID: 29485133
43. World Health Organization (2010) Health Professions Networks Nursing & Midwifery Human Resources for Health: Framework for Action on Interprofessional Education & Collaborative Practice (Geneva: WHO)
44. Costello A, and Zumla A (2000) Moving to research partnerships in developing countries Br Med J 321 827–829 https://doi.org/10.1136/bmj.321.7264.827
45. Kolars J, Cahill K, and Donkor P, et al (2012) Perspective: partering for medical education in sub-Saharan Africa: seeking the evidence for effective collabroations Acad Med 87(2) 216–220 https://doi.org/10.1097/ACM.0b013e31823ede39
46. Eichbaum Q, Nyarango P, and Bowa K, et al (2012) Global networks, alliances and consortia in global health education: the case for south-to-south partnerships J Acquir Immune Defic Syndr JAIDS 61(3) 263–264 https://doi.org/10.1097/QAI.0b013e31826bf957 PMID: 22878420
47. Barteit S, Guzek D, and Jahn A, et al (2020) Evaluation of e-learning for medical education in low-and middle-income countries: a systematic review Comput Educ 145 103726 https://doi.org/10.1016/j.compedu.2019.103726
48. Reeves S, Fletcher S, and McLoughlin C, et al (2017) Interprofessional online learning for primary healthcare: findings from a scoping review BMJ Open 7(8) e016872 https://doi.org/10.1136/bmjopen-2017-016872 PMID: 28780560 PMCID: 5623444
Supplementary Appendix A. Search Strategy for Embase and Ovid
Database: Embase Classic+Embase <1947 to 04 March 2020> Search strategy:
1 developing country/ (95112)
2 (developing adj2 countr*).mp. (137447)
3 (low income adj2 countr*).mp. (12243)
4 (middle income adj2 countr*).mp. (22509)
5 (lmic or lmics or lami countr*).mp. (5522)
6 exp China/ (221918)
7 exp India/ (150498)
8 exp Indonesia/ (17899)
9 exp Brazil/ (113496)
10 exp Pakistan/ (27316)
11 Nigeria/ (38503)
12 Bangladesh/ (16005)
13 exp Mexico/ (48224)
14 Philippines/ (11907)
15 Ethiopia/ (16430)
16 Sri Lanka/ (8639)
17 Kenya/ (21526)
18 Tanzania/ (15257)
19 Ghana/ (11602)
20 Thailand/ (33928)
21 Viet Nam/ (16730)
22 Nepal/ (11528)
23 Senegal/ (7000)
24 Uganda/ (18201)
25 Rwanda/ (3575)
26 or/1-25 (879016)
27 exp socioeconomics/ (384867)
28 low income.mp. (44302)
29 middle income.mp. (25281)
30 28 or 29 (63027)
31 27 and 30 (41592)
32 gross national product/ (4289)
33 30 and 32 (384)
34 31 or 33 (41675)
35 26 or 34 (899172)
36 medical student/ (69251)
37 exp physician/ (770756)
38 exp medicine/ (3516532)
39 resident/ (41748)
40 fellow*.mp. (41637)
41 clinical clerkship.mp. (658)
42 or/36-41 (4170864)
43 education/ (432964)
44 ((staff? or profession*) adj2 develop*).mp. (25018)
45 preceptorship.mp. (1174)
46 exp teaching/ (98612)
47 curriculum/ (90598)
48 exp medical education/ (331141)
49 videoconferencing/ (3653)
50 webcast/ (341)
51 e-learn*.mp. (4368)
52 exp telemedicine/ (38155)
53 or/43-52 (823448)
54 35 and 42 and 53 (19929)
55 exp oncology/ or oncology.mp. (301657)
56 54 and 55 (777)
Database: Ovid MEDLINE(R), Ovid MEDLINE(R) Daily and Epub Ahead of Print, In-Process & Other Non-Indexed Citations <1946 to Present> Search Strategy:
1 developing countries/ (73860)
2 (developing adj2 countr*).mp. (124238)
3 (low income adj2 countr*).mp. (6581)
4 (middle income adj2 countr*).mp. (17390)
5 (lmic or lmics or lami countr*).mp. (4439)
6 exp China/ (183472)
7 exp India/ (100850)
8 Indonesia/ (10128)
9 Brazil/ (90177)
10 Pakistan/ (17021)
11 Nigeria/ (27823)
12 Bangladesh/ (10604)
13 Mexico/ (37549)
14 Philippines/ (8182)
15 Ethiopia/ (12083)
16 Sri Lanka/ (5858)
17 Kenya/ (15502)
18 tanzania/ (11010)
19 ghana/ (7867)
20 thailand/ (25929)
21 vietnam/ (11941)
22 nepal/ (7872)
23 senegal/ (5630)
24 uganda/ (11691)
25 rwanda/ (2330)
26 or/1-25 (687275)
27 exp Socioeconomic Factors/ (441733)
28 low income.mp. (34224)
29 middle income.mp. (19404)
30 28 or 29 (50443)
31 27 and 30 (20396)
32 gross domestic product/ (800)
33 30 and 32 (73)
34 31 or 33 (20427)
35 26 or 34 (700368)
36 Students, Medical/ (32911)
37 exp Physicians/ (137284)
38 exp Medicine/ (1104890)
39 “Internship and Residency”/ (48445)
40 fellow*.mp. (29263)
41 Clinical Clerkship/ (4981)
42 or/36-41 (1260910)
43 Education/ (20633)
44 ((staff? or profession*) adj2 develop*).mp. (22740)
45 preceptorship/ (5016)
46 exp Teaching/ (84291)
47 exp Curriculum/ (83607)
48 exp Education, Medical/ (162473)
49 exp Videoconferencing/ (1756)
50 webcast/ (865)
51 e-learn*.mp. (2568)
52 exp Telemedicine/ (27252)
53 or/43-52 (324612)
54 35 and 42 and 53 (7390)
55 exp Medical Oncology/ or oncology.mp. (114202)
56 54 and 55 (80)
Supplementary Table 1. Detailed summary of the 25 articles included in the scoping review.
Supplementary Table 2. Detailed description of the 25 manuscripts included in the scoping review (Part 2).