Supportive care interventions for cancer patients in low- and middle-income countries (LMICs): a scoping review

In high-income countries (HICs), supportive care is often used to assist cancer patients as they seek treatment and beyond. However, in low-and middle-income countries (LMICs), where more than 70% of all cancer-related deaths occur [1], the provision of supportive care has not been assessed. The purpose of this scoping review is to assess the type of supportive care interventions for cancer patients across the cancer care continuum in LMICs. We examined published articles reporting on supportive care interventions in LMICs. Following PRISMA guidelines, we performed a systematic search of PubMed, ERIC, CINAHL, and PsycINFO. We limited the scope to original research studies focused on LMICs, studies concerning any type of supportive care intervention for adult cancer patients, from diagnosis, treatment, and post-treatment. Thirty-five studies met the criteria for inclusion in the scoping review. The majority were randomized clinical trials (RCT) or used a quasi-experimental design. The highest number of studies (n = 23) was implemented in the WHO Eastern-Mediterranean region, followed by South-East Asia (n = 6), Africa (n = 4), and Western-Pacific Regions (n = 2). Most studies focused on women’s cancers and included interventions for psychosocial support, symptom management, health literacy/education, and patient navigation. Although we found only a small number of interventions being conducted in these settings, our results suggest that providing different types of supportive services in less-resourced settings, even when health systems are fragmented and fragile, can improve mental health, physical health, and the quality of life (QoL) of cancer patients.


Introduction
Effective cancer care requires the delivery of efficacious treatments as well as appropriate supportive resources to assist patients in making the complex decisions surrounding their diagnosis and treatment. A cancer diagnosis is often accompanied by feelings of fear, anger, frustration, denial, loneliness, stress, anxiety, and depression, which can stem from the lack of knowledge of the illness, poor communication with physicians, financial burdens, and challenges in the areas of transportation and housing. It is critical for a cancer patient to not only understand their diagnosis, treatment plan, and follow up, but to also feel physically, emotionally, and practically supported.
Supportive care has been widely and loosely defined by different organizations and groups over the years, encompassing a wide range in scope of service, patient population, and stage of the disease, and also an evolving nature of definitions to involve cancer survivors, caregivers, and include social determinants of health. Recently, the Multinational Association of Supportive Care in Cancer (MASCC) defined supportive care as the prevention and management of the adverse effects of cancer and its treatment, including the management of physical and psychological symptoms and side effects from diagnosis through treatment to post-treatment care [2].
Studies in high-income countries (HIC) have shown that providing appropriate supportive care to newly diagnosed cancer patients may help them and their caregivers manage emotional and psychological symptoms and address social/cultural or logistical barriers, which in turn may improve treatment compliance and patients' quality of life. Several systematic reviews have assessed and evaluated the supportive care needs that cancer patients experience due to their diagnosis and treatment [3,4]. Some have evaluated specific types of interventions, namely educational interventions, or psychotherapeutic interventions such as cognitive behavioral therapy (CBT). Others have evaluated all interventions that target a specific need, a particular outcome, or a specific population or patient group.
However, in low-and middle-income countries (LMICs), where more than 70% of all cancer-relateddeaths occur [1], there is a dearth of supportive care interventions and an overall lack of research studies evaluating their effectiveness in these low-resource settings. A recent scoping review of reviews presents the first broad overview of the published studies addressing the supportive care needs of cancer patients during treatment and survivorship during the decade 2009-2019 [4]. This review of 551 studies found that the number of systematic reviews published tripled in the later years for the period reviewed compared to early years, although none evaluated supportive care interventions in LMICs or in settings with fragmented or under-resourced healthcare systems.
For our study, we chose to review supportive care interventions in LMICs published during the decade 2011-2021 for two reasons: first, to expand on the evidence provided by Edney's review to assess supportive care interventions that are implemented in LMICs; second, to complement the evidence provided by other reviews up to 2010-11, pertaining both the unmet supportive care needs of cancer patients [3] and the implementation of supportive care interventions [5].
The purpose of this scoping review is to assess the type of supportive care interventions for cancer patients across the cancer care continuum in LMICs, summarize the reported outcomes, and to call attention to the gaps in meeting the supportive care needs of cancer patients in these less-resourced settings.

Search strategy
Keywords were developed by reviewing published works for terms involving cancer, supportive care interventions, and LMICs. To refine search terms for "supportive care," we used the MASCC definition of supportive care as "the prevention and management of the adverse effects of cancer and its treatment" which includes the management of both the physical and psychological symptoms and side effects from diagnosis, through treatment, survivorship, and end-of-life care [2]. The full list of the search terms and the search strategy can be found in Table S1 in the supplementary documents.
We searched the following databases: PubMed, ERIC, CINAHL, and PsycINFO. The search followed PRISMA guidelines [6] and was restricted to adult cancer patients, articles published on or after 2011, and articles published in English. The search was run June through August 2021.

Inclusion/exclusion criteria
Articles were included in this review if they were original research studies focused on adult cancer patients in LMICs, described a non-pharmacological supportive care intervention, and reported outcomes of the intervention (process, implementation, or clinical). The review included articles focusing on any cancer type and care setting. Table 1 illustrates the inclusion and exclusion criteria that was applied in the screening process of this review.
This review was limited to the diagnosis, treatment, and post-treatment phases of the cancer care continuum. We excluded prevention and screening since our focus was on cancer patients rather than in the population at risk.
Articles were excluded from this review if the supportive care intervention took place in upper middle-income to high-income countries, was not directly evaluating a supportive care intervention, was not available in English, or if it included children.

Data extraction and assessment of quality
The initial search retrieved a total of 3823 articles. After removing the duplicate articles, 3807 articles were selected to be screened for this review. Three members of the research team participated in a two-phase screening process for each selected article.
First, the research team screened the title and abstract of each article against the inclusion and exclusion criteria, which excluded 3759 articles. Next, the study team reviewed the full text of the remaining sixty-three articles.
Twenty-eight additional articles were excluded in phase two of the screening process because they did not specifically evaluate the interventions. The study team assessed each article included in the review for reporting rigor, sample size, and study design. No articles were excluded from the review based on these criteria.
A total of thirty-five articles were included in this review after the completion of the screening process. Figure 1 shows the PRISMA flow diagram illustrating the process. The following information was extracted from each included article by two members of the review team: the study author(s), study type, cancer type, supportive care intervention, phase of the cancer care continuum, location of study, and primary and secondary outcomes. We followed synthesis without meta-analysis (SWIM) reporting guidelines (https:// swim. sphsu. gla. ac. uk/) for reporting of the results.

Types of supportive care
The types of supportive care interventions reported in the studies often included multiple types of services per study. Psychosocial supportive care was offered in 18 (51%) of the articles that were analyzed and was the most common supportive service. Table 3 depicts the characteristics of the supportive care interventions included in this scoping review.
The majority of the psychosocial interventions reported positive effects on the primary outcomes. Two articles implemented in Indonesia and Iran reported that a 6-week psychosexual intervention for cervical and breast cancer survivors can effectively improve sexual function and quality of sexual life [9,42].
Only two articles reported peer support interventions [14,15]. Both articles were RCTs conducted in Iran. One study showed that a peer support program using telephone or social media to connect peer mentors with patients significantly improved the subjective well-being of colorectal cancer patients [15]. The second compared two support groups from two different hospitals, both exclusively for women with breast cancer. The intervention of regular meetings to discuss the effects of each individual's cancer as a group showed a significant improvement in the quality of life of the participants in each group [14].
Two interventions in Kenya and Iran tested the effect of dignity therapy on the QoL of advanced cancer patients [19,38]. Dignity therapy has been studied to improve distress in patients with incurable diseases. While Weru et al. did not see any effect after one session of dignity therapy implemented in Kenya [38], the study conducted in Iran by Zaki-Neja et al. reported improvement in the quality of life of the intervention group after receiving three sessions [19].
Six articles reported interventions to improve education for patients [11-13, 20, 22, 31], one for caregivers [31], and one for both groups [24]. The education topics varied from basic skills to self-care, cancer information, and psychoeducation. All studies reported an increase in the patient's QoL after the intervention.
Additionally, a significant number of studies included in our review focused on non-pharmacological interventions to address common side effects of treatment: cancer-related fatigue (CRF), chemotherapy-induced peripheral neuropathy, and nutrition (n = 8). Five groups reported the effect of physical activity -exercise therapy, aerobic exercise, daily walking, muscle strengthening, and yoga -in overall QoL and mobility, CRF, and chemotherapy induced peripheral neuropathy [16, 23-25, 32, 33, 35, 40]. All studies reported improvement in the physical function of cancer patients and their QoL.
Malnutrition, a frequent, debilitating, side effect of cancer, was addressed in two interventions. One study implemented nutritional counseling for gastrointestinal cancer patients which reported an increase in QoL, improved physical function, and reduced negative symptoms [40]. In a second study, the implementation of a patient-centered foodservice model increased nutritional intake in cancer patients in a hospital in India [35].
Two studies included in the review reported patient navigation interventions [36,39]. Koffi et al. adapted an ambulatory navigation program for malignant lymphoma patients from Toulouse, France, to Abidjan, Cote d'Ivoire. The study showed that navigation significantly reduced treatment refusal and abandonment, but the extent of the effects of navigation was limited by the cost of treatment, a major reason for delays in clinical management. Odigie's study reported that the use of mobile phones is feasible and acceptable to improve the follow-up care of cancer patients in a hospital in Zaria, Nigeria.

Types of outcomes measured
Each intervention included in the review measured multiple outcomes. Although the included articles were reviewed for process, implementation, and clinical outcomes, most articles reported only clinical outcomes, with only two studies evaluating process and implementation outcomes [36,39]. Table 4 describes the primary outcomes and the results. The most common outcome measured was quality of life (QoL), followed by anxiety, overall physical and psychological health, depression and stress, and coping capacity. Other less frequently assessed outcomes were sexual function and well-being, social relationships, spiritual wellbeing, increased appetite, increased nutritional intake and weight gain, family involvement, self-esteem, cancer-related fatigue, cancer-induced neuropathy, mobility, and treatment abandonment.

Discussion
Since the World Cancer Declaration, launched in 2006, called upon government leaders and policymakers around the world to significantly reduce the global cancer burden, promote greater equity in the access to cancer services, and integrate cancer control into the global health and development agenda, significant progress has been made in cancer control globally. Dedicated efforts to develop quality, comprehensive, cancer care currently exist in many LMICs, although they tend to focus on clinical services. Less attention is directed to the development of supportive care services and measuring the impact and value such services might provide for cancer patients and their families in these settings. This scoping review presents supportive care interventions for cancer patients across the cancer care continuum in LMICs and their reported outcomes.
Evidence-based guidelines for supportive care for cancer patients exist, although they are applicable mostly to HIC. Even in these settings, gaps and barriers still exist in the implementation of such programs, in particular in the integration of clinical and supportive care [4].
For LMICs, the Breast Health Global Initiative (BHGI) has published consensus statements focused on supportive and palliative care for patients with breast cancer that are resource-stratified [43]. The recommendations cover physical symptom management, pain control, and some psychosocial and spiritual aspects of care and education. However, their focus on clinically related topics does not take into Supportive care needs (SCNs) After the intervention, the mean score of dimensions and total SCNs in the intervention group were significantly less than the control group

Treatment refusal and abandonment
The study showed that patient navigation may reduce refusal and abandonment of treatment consideration other important health-related issues such as nutrition, safe living conditions, practical needs (childcare, financial constraints), employment or women's rights that take place outside of the healthcare system. Of the studies included in this review, a large number focused on women's cancers and psychosocial supportincluding peer support, symptom management, health literacy/education, and patient navigation. During the search process, we found a significant number of articles which described supportive care needs in LMICs. However, there were few actual interventions published.
Notably, peer support interventions, where support is offered to people with cancer by those who have themselves experienced cancer, were rare. Only two peer support programs from Iran were included in the scoping review, despite peer support programs being increasingly recognized as an important component of supportive care for cancer patients.
Additionally, we did not find any interventions aimed at improving social problems or practical needs directly derived from a cancer diagnosis, such as financial toxicity, employment, disability, or stigma of the disease, all of which are highly prevalent in less-resourced settings. This could be related to the fact that 80% of the interventions included in the review are being conducted at the tertiary care level, and only a few at the community level. This was also noted by Edney et al. who identified a research gap for practical needs [4].
The interventions were described with different degrees of detail about process and implementation in the majority of the thirty-five articles. However, only two studies reported process or implementation outcomes. As health systems become more patient-centered, it may be valuable to use hybrid designs that include a process evaluation and measure implementation outcomes, in addition to the clinical efficacy of the intervention. Implementation science frameworks applied to the design of the interventions would lead to a better understanding of the factors that influence implementation which in turn could define the adaptations that are needed to effectively deliver the intervention in a specific context. The lessons learned from the implementation of these interventions could provide valuable guidance to adapt these established programs into new contexts.
To our knowledge, this is the first scoping review focused on a wide range of cancer supportive care interventions in LMICs. We found similar reviews in the literature that focused specifically on one type of supportive care: support groups [44], and navigation [45], which were extensively reviewed by Edney et al. [4]. However, most included a mix of studies conducted both in high-, middle-, and low-income countries; included community awareness and education, and screening interventions; and did not require studies to report outcomes.
The study findings should be interpreted considering several limitations. First, most articles reported positive effects on the primary outcome measured, which could be the result of a publication bias since interventions that fail are less likely to be reported in the literature. Almost all the interventions were randomized trials or quasi-experimental studies implemented in a hospital setting, which could potentially be an additional source of bias since community programs are more difficult to publish in peer reviewed journals or are not able to report (clinical) outcomes data. Additionally, there are undoubtedly more supportive care interventions being employed in LMIC settings; however, due to resource challenges in the areas of manpower and funding, these interventions may not have any research attached to them or their results have not been published.
We only included articles in English published in peer reviewed journals and as such, we likely omitted publications about interventions reported in different languages. There was an over representation of articles from Iran, with 20 of the included interventions coming from different hospitals in this country. After a thorough review of the full articles, we did not find a reason to exclude the articles and they are therefore included in the review.

Conclusion
This scoping review identified gaps in supportive care research and evaluation. First, our results point out the need to include cancer patients and advocacy/support groups in research ensuring that interventions are designed in a way that address the practical needs of patients and caregivers directly derived from a cancer diagnosis, which are currently understudied in LMICs.
The second is the need for increased research funding for and engagement of supportive care researchers in LMICs. This would hopefully result in an increased number of articles from these settings published in peer-reviewed journals. Finally, the promotion and the dissemination of best-practices in supportive care and implementation "toolkits" that share the core components and methodologies for developing and adapting evidence-based supportive care interventions.
Ensuring that patients and caregivers receive the assistance they need as they navigate the cancer care pathway and feel supported throughout is crucial to improve cancer outcomes in LMICs. Although only a small number of supportive interventions are being studied in these settings, the results from this scoping review suggest that providing different types of supportive services in less-resourced settings, even when health systems are fragmented and fragile, is possible and can improve mental, physical health, and QoL of cancer patients.