Skip to main content
ecancermedicalscience logoLink to ecancermedicalscience
. 2021 Sep 30;15:1296. doi: 10.3332/ecancer.2021.1296

Oncology training and education initiatives in low and middle income countries: a scoping review

Safiya Karim 1, Zahra Sunderji 2, Matthew Jalink 3, Sahar Mohamed 4, Indranil Mallick 5, Susan Citonje Msadabwe-Chikuni 6, Nancy J Delgarno 7, Nazik Hammad 3, Scott Berry 3
PMCID: PMC8580602  PMID: 34824619

Abstract

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


In 2018, it was estimated that 18.1 million new cancer cases and 9.6 million cancer deaths occurred worldwide [1]. 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 [2]. 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 [3]) and continue to rise [4]. 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 [6]. 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 [9]. There are significant shortages in the oncology workforce, including specialists with skills in pathology, radiation and medical oncology [6]. 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 [10]. 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 [10]. 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 [11]. To combat this, several global oncology initiatives have focused on building local capacity to provide high-quality cancer care [10]. One such mechanism involves building partnerships between institutions facilitating bi-directional learning and knowledge transfer, and enabling local retention and capacity building [10]. 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.

Methods

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 [12]. 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 [13]. 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.

Select studies

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 [15].

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 [15].

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 [16]. These levels include: (1) reaction, (2) learning, (3) behaviour and (4) results.

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 [1725], eleven were qualitative studies [2736] and five were mixed method studies [3741]. An overview of the selected articles is available in Table 1. Full details are available in Supplementary Tables 1 and 2.

Figure 1. PRISMA (Preferred Reporting Items for Systematic Reviews and Meta-Analyses) chart.

Figure 1.

Table 1. Overview of the 25 manuscripts included in the scoping review.

First author Year published Low/middle income country Collaborating country/organisation Target population Level of medical education Duration E-learning (Y/N)
Abugideiri [17] 2019 Ethiopia USA Physicians GME Not specified Y – on-line teaching module
Adler [18] 2015 Barbados/Jamaica/St. Lucia Canada Physicians and nurses CME 18 months Y – telehealth
Agrawal [37] 2011 India India Physicians GME 2 years Y – telehealth
Alfaar [26] 2012 Egypt USA Pharmacists CME 3 days Y – telehealth
Arnold [27] 2014 Guatemala USA Physicians CME 1 year N
Asgary [19] 2016 Ghana USA Nurses CME 3.5 months Y – smartphone application
Awuah [20] 2011 Ghana USA Physicians CME 1 week N
Barron [21] 2018 Bangladesh USA Nurses CME 3 years N
Butonzi [29] 2019 Rwanda USA Physicians CME 2 years N
Carbone [30] 1991 Taiwan USA Physicians GME 2 years N
Day [31] 2012 Guatemala USA Nurses CME 10 days N
De Camargo [23] 2018 Brazil N/A Physicians UME 1 day N
Eastin [38] 2018 Kenya/Tanzania/Uganda United Kingdom Physicians GME/CME Not specified N
Elit [39] 2010 Kenya Canada Physicians CME 2 weeks Y – on-line teaching module
Fish [40] 2019 South Africa/Tanzania/Rwanda USA Physicians GME/CME 3–6 weeks N
Kapoor [33] 2006 India WHO Physicians UME 1 week N
Lewis [41] 2019 Uganda United Kingdom Physicians, nurses, pharmacists CME 18 months N
Lopez [22] 2017 Multiple countriesa USA Physicians and nurses CME 2 years Y – telehealth
Miller [34] 2007 Nigeria Multiple organisationsb Physicians, nurses, non-health professionals CME 10 days N
Nwogu [32] 2014 Nigeria USA Physicians and nurses CME 3 days N
Qaddoumi [35] 2007 Jordan Canada Physicians CME 17 months Y – telehealth
Santiago [24] 2012 Brazil USA Physicians CME 6 months Y – telehealth
Shah [25] 2006 Egypt/Tunisia USA Physicians CME 30 minutes N
Tam [36] 2013 China Hong Kong Physicians CME 1 year N
Wilimas [28] 2003 Morocco/El Salvador/Guatemala USA/Canada Nurses CME 3 months Y – simulations
a

Includes Brazil, Uruguay, Chile, Paraguay, Bolivia, Peru, Ecuador, Colombia, Nicaragua Honduras, India, South Africa, Mozambique, Nigeria, Ghana, and Zambia

b

Includes American College of Clinical Pharmacy, WHO, IARC, Program for Appropriate Technology in Health, Engender Health, John Hopkins Program for International Education in Gynecology and Obstetrics (JHPIEGO) and Pan American Health Organization

Supplementary Table 1. Detailed summary of the 25 articles included in the scoping review.

Abugideiri [17] 2019 A Prospective International Pilot Study Evaluating the Efficacy of a Self-Guided Contouring Teaching Module with Integrated Feedback for Transitioning from 2D to 3D Treatment Planning Middle East/Africa
Ethiopia Black Lion Hospital/Addis Ababa University
USA Winship Cancer Institute of Emory University In LMIC
Adler [18] 2019 Bridging the Distance in the Caribbean: Telemedicine as a means to build capacity for care in paediatric cancer and blood disorders Americas Barbados, Jamaica, St. Lucia University of the West Indies, Bustamante Hospital for Children Canada The Hospital for Sick Children In LMIC
Agrawal [37] 2011 Training the trainees in radiation oncology with telemedicine as a tool in a developing country: A two-year audit Asia Pacific India Chhatrapati Shahuji Maharaj Medical University India Sanjay Ghandi Post Graduate Institute of Medical Sciences In LMIC
Alfaar [26] 2012 International telepharmacy education: another venue to improve cancer care in the developing world Middle East/Africa
Egypt Children’s Cancer Hospital, Cairo
USA St. Jude Children’s Research Hospital
In LMIC
Arnold [27] 2014 A training programme to build cancer research capacity in low- and middle-income countries: findings from Guatemala Americas Guatemala Instituto de Cancerologia (INCAN)
USA School of Medicine of Washington University in St. Louis In LMIC and HIC
Asgary [19] 2016 mHealth to train community health nurses in visual inspection with acetic acid for cervical cancer screening in Ghana Middle East/Africa
Ghana Korle Bu Teaching Hospital USA New York University In LMIC
Awuah [20] 2011 Implementation of a percutaneous core needle biopsy training program: Results from the University of Michigan-Komfo Anokye Teaching Hospital breast cancer research partnership Middle East/Africa
Ghana Komfo Anokye Teaching Hospital (KATH), Kumasi USA University of Michigan
In LMIC
Barron [21] 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 Asia Pacific Bangladesh Dhaka Medical College Hospital and Massachusetts General Hospital USA Massachusetts General Hospital In LMIC
Butonzi [29] 2019 Global Oncology Fellowship Electives: The Impact on Cancer Care and International Collaborations Middle East/Africa
Rwanda
Butaro Hospital Cancer Center of Excellence USA University of Pennsylvania Center for Global Cancer Medicine, Geisel School of Medicine In LMIC
Carbone [30] 1991 Developing a Postgraduate Medical Oncology Training Program in Taipei, Taiwan, Republic of China Asia Pacific Taiwan
Taipei
USA University of Wisconsin In LMIC
Day [31] 2012 A sustainable model for pediatric oncology nursing education in low-income countries Americas
Guatemala
Unidad Nacional de Oncologia Pediatrica USA St. Jude Children’s Research Hospital In LMIC
De Camargo [23] 2018 A sustainable model for pediatric oncology nursing education in low-income countries Americas
Brazil
Multiple Medical Schools in Brazil No partner country N/A In LMIC
Eastin [38] 2018 Addressing the burden of cancer in East Africa through cascaded training Middle East/Africa
Kenya, Tanzania, Uganda N/A (individual physicians) UK Royal College of Physicians, London, UK In LMIC
Elit [39] 2010 Teaching Cervical Cancer Surgery in Low-or Middle-Resource Countries Middle East/Africa
Kenya Moi University Canada Gynaecologic Oncologists of Canada
In LMIC
Fish [40] 2019 POETIC (Program for Enhanced Training in Cancer): An Initial Experience of Supporting Capacity Building for Oncology Training in Sub-Saharan Africa Middle East/Africa
South Africa, Tanzania, Rwanda
University of Cape Town, Ocean Road Cancer Centre USA Massachusetts General Hospital, Beth Israel Deaconess Medical Centre
In HIC
Kapoor [33] 2006 The UICC/WHO-CCCE Cancer Education Project: An Indian Experience Asia Pacific India
Gandhi Medical College, Bhopal
International WHO Collaborating Center for Cancer Education, University Medical Center, The Netherlands In LMIC
Lewis [41] 2019 Improving the safety of chemotherapy treatment for cancer patients in Uganda Middle East/Africa
Uganda
Mbarara University of Science and Technology UK University of Bristol In LMIC and HIC
Lopez [22] 2017 Project Echo: A Telementoring Program for Cervical Cancer Prevention and Treatment in Low-Resource Settings Americas, Middle East/Africa, Asia Pacific
Multiple countries including Brazil, Uruguay, Chile, Paraguay, Bolivia, Peru, Ecuador, Colombia, Nicaragua Honduras, India, South Africa, Mozambique, Nigeria, Ghana, Zambia Multiple organisations USA University of New Mexico, University of Texas MD Anderson Cancer Center In LMIC
Miller [34] 2007 Knowledge dissemination and evaluation in a cervical cancer screening implementation program in Nigeria
Middle East/Africa
Nigeria
University of Ibadan International Organisations Multiple organisations including ACCP, WHO, IARC, PATH, Engender Health, JHPIEGO, PAHO In LMIC
Nwogu [32] 2014 Promoting Cancer Control Training in Resource Limited Environments: Lagos, Nigeria Middle East/Africa
Nigeria
Lagos State University Teaching Hospital
USA Roswell Park Cancer Institute In LMIC
Qaddoumi [35] 2007 Impact of Telemedicine on Pediatric Neuro-Oncology in a Developing Country: The Jordanian-Canadian Experience Middle East/Africa
Jordan
King Hussein Cancer Center
Canada The Hospital for Sick Children In LMIC
Santiago [24] 2012 Improving the histopathologic diagnosis of pediatric malignancies in a low-resource setting by combining focused training and telepathology strategies Americas
Brazil
Instituto Materno Infantil de Pernambuco
USA The Mayo Clinic and St. Jude Children’s Research Hospital In LMIC and HIC
Shah [25] 2006 Knowledge gained after a brief CME module on breast cancer diagnosis Middle East/Africa
Egypt/Tunisia
Individual primary care physicians from Egypt and Tunisia USA University of Michigan School of Public Health and Cancer Center, and the University of Texas M.D Anderson Cancer Centre In LMIC
Tam [36] 2013 Internationalization: the Hong Kong-China experience as a model for collaborative education in Asia Asia Pacific
China University of Medical Sciences Beijing, Shanghai Second Medical University Hong Kong University of Hong Kong
In LMIC and HIC
Wilimas [28] 2003 Training subspecialty Nurses in Developing Countries: Methods, Outcome, and Cost
Americas
Morocco, El Salvador, Guatemala
Morocco – Not Reported (NR),
El Salvador – Benjamin Bloom Hospital
Guatemala – NR
USA and Canada St. Jude Children’s Research Institute, Children’s Hospital of Eastern Ontario, The Hospital for Sick Children In LMIC

ACCP, American College of Clinical Pharmacy; WHO, World Health Organization; IARC, International Agency for Research on Cancer; PATH, Program for Appropriate Technology in Health; PAHO, Pan American Health Organization

Supplementary Table 2. Detailed description of the 25 manuscripts included in the scoping review (Part 2).

Abugideiri [17] Physicians GME Y Radiation Oncology Not specified Learning Host country institution and National Cancer Institute Grant
Adler [18] Physicians and nurses CME Y Paediatric oncology 18 months Reaction Sick Kids Foundation
Agrawal [37] Physicians GME Y Radiation oncology 2 years Reaction Grant by Department of Science and Technology, India
Alfaar [26] Pharmacists CME Y Supportive care 3 days Reaction NR
Arnold [27] Physicians CME N Population Health Research 1 year Reaction National Institutes of Health and National Cancer Institute
Asgary [19] Nurses CME Y Gynaecologic oncology (cervical cancer) 3.5 months Learning New York University Institute of Global Health, Global Health Challenge Fund
Awuah [20] Physicians CME N Surgical oncology and pathology 1 week Learning NR
Barron [21] Nurses CME Y Medical and haematologic oncology 3 years Learning and results NR
Butonzi [29] Physicians CME N Hematologic oncology 2 years Reaction Personal time (i.e. vacation time)
Carbone [30] Physicians GME N Medical Oncology 2 years Learning NR
Day [31] Physicians and nurses CME N Paediatric oncology 10 days Learning National Cancer Institute, American Lebanese Syrian Associated Charities
De Camargo [23] Physicians UME N Multiple disciplines 1 day Reaction CEPHO (research centre affiliated with a medical school) and self-funded through registration cost
Eastin [38] Physicians GME/CME N Multiple disciplines Not specified Reaction and Learning NR
Elit [39] Physicians CME Y Gynaecologic oncology (cervical cancer) 2 weeks Learning and Behaviour NR
Fish [40] Physicians GME/CME N Multiple disciplines 3–6 weeks Reaction and Learning Eddie Reed Philanthropic Fund
Kapoor [33] Physicians UME N Multiple disciplines 1 week Reaction NR
Lewis [41]
Physicians, nurses, pharmacists CME N Medical oncology 18 months Behaviour UK Government Department for International Development
Lopez [22] Physicians and nurses CME Y Gynaecologic oncology (cervical cancer) 2 years Reaction National Institutes of Health, Cancer Prevention Research Institute of Texas, Cancer Prevention Pharmaceuticals
Miller [34] Physicians, nurses and non-health professionals CME N Gynaecologic oncology (cervical cancer) 10 days Learning National Cancer Institute, ExxonMobil Foundation, T. Boone Pickens Research Fund
Nwogu [32] Physicians and nurses CME N Multiple disciplines 3 days Reaction UICC International Cancer Technology Transfer Fellowship funded by ASCO
Qaddoumi [35] Physicians CME Y Paediatric oncology 17 months Behaviour NR
Santiago [24] Physicians CME Y Pathology 6 months Learning and behaviour National Cancer Institute, American Lebanese Syrian Associated Charities
Shah [25] Physicians CME N Multiple disciplines 30 minutes Learning NR
Tam [36] Physicians CME N Surgical oncology (paediatric) 1 year Reaction S.K Yee Medical Foundation
Wilimas [28] Nurses CME Y Paediatric oncology 3 months Reaction and learning NR

UME, Undergraduate medical education; GME, Graduate medical education; CME, Continuing medical education; NR, Not reported; CEPHO, Centro de Estudos e Pesquisa de Hematologia e Oncologia; UICC, Union for International Cancer Control; ASCO, American Society of Clinical Oncology

Target population and location

Fifteen of the twenty-five articles described an education initiative for physicians [17, 20, 2325, 27, 29, 30, 33, 3540]. Four articles described an initiative for nurses [19, 21, 28, 31], and one article was aimed at pharmacists [26]. 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 [41] and one was for physicians, nurses and other non-health professionals [34].

Thirteen initiatives were conducted in the Middle East/Africa [17, 19, 20, 25, 26, 29, 32, 34, 35, 3841], 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) [22].

Figure 2. Low-and-middle income countries with educational initiatives highlighted in the 25 studies.

Figure 2.

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 [26] 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 [24] and one in surgical oncology [36]. There was one initiative that focused on both surgical oncology and pathology [20]. In addition, there was one intervention related to supportive care [26] and one on conducting population health research [27]. 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, 3134, 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].

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 [19], two used online teaching modules [17, 39] and one used simulations [28].

Collaborations

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, 1922, 2427, 2932, 40], three from Canada [18, 35, 39], one from both the United States and Canada [28], two from the United Kingdom [38, 41] and one from Hong Kong [36]. Two articles described collaborations with a variety of international agencies, including the WHO [33, 34], and the International Agency for Research on Cancer (IARC) [34]. The article by Agrawal et al [37] 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, 3436, 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 [40].

Capacity building

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 [21] 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 [40] 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 [41] 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 [21]. 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.

Challenges

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 [38]. Eleven articles did not disclose their challenges in the implementation of the initiative [2024, 28, 29, 31, 38, 40, 41].

Funding

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 [19] and one initiative was partially funded by the collaborating country’s government [41] while another was funded by a grant through the host country’s government [37]. Other sources of funding included research institutes [22, 23], a pharmaceutical company [22] (partial funding) and a fellowship award [32]. Ten articles did not disclose the source of funding for their initiative [20, 21, 25, 26, 28, 30, 33, 35, 38, 39].

Discussion

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.

Figure 3. Number of published oncology medical education initiatives per year.

Figure 3.

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 [42]. 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 [43]. 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 [6]. 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 [46]. 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 [44]. 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 [45]. 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 [46].

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 [16]. 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 [47] 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 [48] 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 [47].

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.

Conclusion

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.

Funding

This manuscript was supported by the University of Calgary Global Oncology Programme.

Conflicts of interest statement

The authors have no conflicts of interest.

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)

References

  • 1.Bray F, Ferlay J, Soerjomataram I, et al. Global cancer statistics 2018: GLOBOCAN estimates of incidence and mortality worldwide for 36 cancers in 185 countries. CA Cancer J Clin. 2018;68(6):394–424. doi: 10.3322/caac.21492. [DOI] [PubMed] [Google Scholar]
  • 2.International Agency for Research on Cancer. Cancer tomorrow. [1/02/2021]. [ https://gco.iarc.fr/tomorrow/home]
  • 3.The World Bank. Washington: World Bank; World bank country and lending groups. [Google Scholar]
  • 4.Torre L, Siegel R, Ward E, et al. Global cancer incidence and mortality rates and trends-an update. Cancer Epidemiol Biomarkers Prev. 2016;25:16–27. doi: 10.1158/1055-9965.EPI-15-0578. [DOI] [PubMed] [Google Scholar]
  • 5.The Lancet. GLOBOCAN 2018: counting the toll of cancer. Lancet. 2018;392:985. doi: 10.1016/S0140-6736(18)32252-9. [DOI] [PubMed] [Google Scholar]
  • 6.Patel J, Galsky M, Chagpar A, et al. Role of american society of clinical oncology in low-and middle-income countries J Clin Oncol. 2011;29(22):3097–3102. doi: 10.1200/JCO.2011.35.6378. [DOI] [PubMed] [Google Scholar]
  • 7.The World Bank. Physicians (per 1,000 people) 2021. [5/01/2021]. [ https://data.worldbank.org/indicator/SH.MED.PHYS.ZS]
  • 8.The World Bank. Nurses and midwives (per 1,000 people) 2021. [5/01/2021]. [ https://data.worldbank.org/indicator/SH.MED.NUMW.P3.
  • 9.Fundytus A, Sullivan R, Vanderpuye V, et al. Delivery of global cancer care: an international study of medical oncology workload. J Glob Oncol. 2018;4:1–11. doi: 10.1200/JGO.17.00126. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 10.Asirwa FC, Greist A, Busakhala N, et al. Medical education and training: building in-country capacity at all levels J Clin Oncol. 2016;34(1):36–42. doi: 10.1200/JCO.2015.63.0152. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 11.Mejia A, Pizurki H, Royston E. Physician and Nurse Migration: Analysis and Policy Implications. Geneva: WHO; 1979. [Google Scholar]
  • 12.Peters M, Godfrey C, McInerney P, et al. Aromataris E, Munn Z, editors. Chapter 11: Scoping reviews (2020 version) JBI Manual for Evidence Synthesis. 2020. [DOI]
  • 13.Levac D, Colquhoun H, O’Brien K. Scoping studies: advancing the methodology. Implement Sci. 2010;5:69. doi: 10.1186/1748-5908-5-69. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 14.Arksey H, O’Malley L. Scoping studies: towards a methodological framework. Int J Soc Res Methodol. 2005;8(1):19–32. doi: 10.1080/1364557032000119616. [DOI] [Google Scholar]
  • 15.Ruiz J, Mintzer M, Leipzig R. The impact of e-learning in medical education. Acad Med. 2006;81(3):207–212. doi: 10.1097/00001888-200603000-00002. [DOI] [PubMed] [Google Scholar]
  • 16.Kirkpatrick D. Great ideas revisited. Techniques for evaluating training programs. Revisiting Kirkpatrick’s fourlevel model. Train Dev. 1996;50:54–59. [Google Scholar]
  • 17.Abigideiri M, Schreibmann E, Switchenko J, et al. 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. 2019;5:1–16. doi: 10.1200/JGO.18.00224. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 18.Adler E, Alexis C, Ali Z, et al. 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. 2015;209:1–8. [PubMed] [Google Scholar]
  • 19.Asgary R, Adongo PB, Nwameme A, et al. mHealth to train community health nurses in Visual Inspection with Acetic Acid for cervical cancer screening in Ghana. J Low Genit Track Dis. 2016;20(3):239–242. doi: 10.1097/LGT.0000000000000207. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 20.Awuah B, Martin I, Takyi V, et al. 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. 2011;18(4):957–960. doi: 10.1245/s10434-010-1422-4. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 21.Barron A, Moran J, Nina S, et al. 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. 2018;4:1–6. doi: 10.1200/JGO.2016.006486. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 22.Lopez M, Baker E, Mibourne A, et al. Project echo: a telementoring program for cervical cancer prevention and treatment in low-resource settings. J Glob Oncol. 2017;3(5):658–665. doi: 10.1200/JGO.2016.005504. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 23.de Camargo C, Schoueri J, Neto F, et al. Medical student oncology congress: designed and implemented by Brazilian medical students. J Cancer Educ. 2018;33:1151–1158. doi: 10.1007/s13187-017-1215-6. [DOI] [PubMed] [Google Scholar]
  • 24.Santiago T, Jenkins J, Pedrosa F, et al. Improving the histopathologic diagnosis of pediatric malignancies in a low-resource setting by combining focused training and telepathology strategies. Pediatr Blood Cancer. 2012;59:221–225. doi: 10.1002/pbc.24071. [DOI] [PubMed] [Google Scholar]
  • 25.Shah N, Soliman A, Banerjee M, et al. Knowledge gained after a brief CME module on breast cancer diagnosis. J Cancer Educ. 2006;21:169–174. doi: 10.1207/s15430154jce2103_17. [DOI] [PubMed] [Google Scholar]
  • 26.Alfaar AS, Kamal S, AbouElnaga S, et al. International telepharmacy education: another venue to improve cancer care in the developing world. Telemed J E-Health. 2012;8(6):470–474. doi: 10.1089/tmj.2011.0182. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 27.Arnold LD, Barnoya J, Gharzouzi EN, et al. A training programme to build cancer research capacity in low- and middle-income countries: findings from Guatemala. Bull World Health Organ. 2014;92:297–302. doi: 10.2471/BLT.13.126516. doi: 10.2471/BLT.13.126516. [doi: ] [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 28.Wilimas J, Donahue N, Chammas G, et al. Training subspecialty nurses in developing countries: methods, outcomes and cost. Med Pediatr Oncol. 2003;41:136–140. doi: 10.1002/mpo.10242. [DOI] [PubMed] [Google Scholar]
  • 29.Butonzi J, Forbes V, Kigonya C, et al. Global oncology fellowship electives: the impact on cancer care and international collaborations. Rwanda Med J. 2019;76(4):1–5. [Google Scholar]
  • 30.Carbone P. Developing a postgraduate medical oncology training program in Taipei, Taiwan, Republic of China. J Clin Oncol. 1991;9(2):335–338. doi: 10.1200/JCO.1991.9.2.335. [DOI] [PubMed] [Google Scholar]
  • 31.Day S, Garcia J, Antillon F, et al. A sustainable model for pediatric oncology nursing education in low-income countries. Pediatr Blood Cancer. 2012;58(2):163–166. doi: 10.1002/pbc.24007. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 32.Nwogu C, Mahoney M, George S, et al. Promoting cancer control training in resource limited environments: Lagos, Nigeria. J Cancer Educ. 2014;29:14–18. doi: 10.1007/s13187-013-0581-y. [DOI] [PubMed] [Google Scholar]
  • 33.Kapoor N, Haagedoorn E, de Vries J. The UICC/WHO-CCCE cancer education project: an Indian experience. J Cancer Educ. 2006;21(3):182–185. doi: 10.1207/s15430154jce2103_19. [DOI] [PubMed] [Google Scholar]
  • 34.Miller D, Okolo C, Mirabal Y, et al. Knowledge dissemination and evaluation in a cervical cancer screening implementation program in Nigeria. Gynecol Oncol. 2007;107:S196–207. doi: 10.1016/j.ygyno.2007.07.014. [DOI] [PubMed] [Google Scholar]
  • 35.Qaddoumi I, Mansour A, Musharbash A, et al. Impact of telemedicine on pediatric neuro-oncology in a developing country: the Jordanian-Canadian experience. Pediatr Blood Cancer. 2007;48:39–43. doi: 10.1002/pbc.21085. [DOI] [PubMed] [Google Scholar]
  • 36.Tam P, Wong K, Li L, et al. Internationalization: the Hong-Kong-China experience as a model for collaborative education in Asia. Pediatr Surg Int. 2013;29:1053–1059. doi: 10.1007/s00383-013-3407-4. [DOI] [PubMed] [Google Scholar]
  • 37.Agrawal S, Maurya A, Shrivastava K, et al. Training the trainees in radiation oncology with telemedicine as a tool in a developing country: a two-year audit. Int J Telemed Appl. 2011;2011:230670. doi: 10.1155/2011/230670. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 38.Eastin J. Adressing the burden of cancer in East Africa through cascaded training. Cancer Control. 2019;2019:64–68. [Google Scholar]
  • 39.Elit LM, Rosen B, Jimenez W, et al. Teaching cervical cancer surgery in low- or middle-resource countries. Int J Gynecol Cancer. 2010;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] [PubMed] [Google Scholar]
  • 40.Fish M, Parkes J, Dharsee N, et al. POETIC (program for enhanced training in cancer): an initial experience of supporting capacity building for oncology training in Sub-Saharan Africa. Oncologist. 2019;24(23):1557–1561. doi: 10.1634/theoncologist.2019-0207. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 41.Lewis P. Improving the safety of chemotherapy treatment for cancer patients in Uganda. Cancer Control. 2019;2019:59–62. [Google Scholar]
  • 42.Fadelu T, Shulman L. Health policy: towards greater equity in the global oncology workforce. Nat Rev Clin Oncol. 2018;15(5):270–272. doi: 10.1038/nrclinonc.2018.31. [DOI] [PubMed] [Google Scholar]
  • 43.World Health Organization. Health Professions Networks Nursing & Midwifery Human Resources for Health: Framework for Action on Interprofessional Education & Collaborative Practice. Geneva: WHO; 2010. [Google Scholar]
  • 44.Costello A, Zumla A. Moving to research partnerships in developing countries. Br Med J. 2000;321:827–829. doi: 10.1136/bmj.321.7264.827. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 45.Kolars J, Cahill K, Donkor P, et al. Perspective: partering for medical education in sub-Saharan Africa: seeking the evidence for effective collabroations. Acad Med. 2012;87(2):216–220. doi: 10.1097/ACM.0b013e31823ede39. [DOI] [PubMed] [Google Scholar]
  • 46.Eichbaum Q, Nyarango P, Bowa K, et al. Global networks, alliances and consortia in global health education: the case for south-to-south partnerships. J Acquir Immune Defic Syndr JAIDS. 2012;61(3):263–264. doi: 10.1097/QAI.0b013e31826bf957. [DOI] [PubMed] [Google Scholar]
  • 47.Barteit S, Guzek D, Jahn A, et al. Evaluation of e-learning for medical education in low-and middle-income countries: a systematic review. Comput Educ. 2020;145:103726. doi: 10.1016/j.compedu.2019.103726. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 48.Reeves S, Fletcher S, McLoughlin C, et al. Interprofessional online learning for primary healthcare: findings from a scoping review. BMJ Open. 2017;7(8):e016872. doi: 10.1136/bmjopen-2017-016872. [DOI] [PMC free article] [PubMed] [Google Scholar]

Articles from ecancermedicalscience are provided here courtesy of ecancer Global Foundation

RESOURCES