Abstract
Low- and middle-income countries (LMICs) report disproportionally worse cancer mortality. Current global cancer control efforts focus predominantly on expanding access to multimodality treatment for patients, whereas less attention has been spent on implementing strategies to ensure sustained quality assessment and improvement across the cancer care continuum. The goal of this focused review was to examine specific resource barriers to the development and implementation of quality improvement programs in LMICs. In this article, we use a nonsystematic review process to discuss the existing literature on four resource barriers within the context of cancer care delivery in LMICs, focusing on staff, time allocated for quality improvement work, research infrastructure, and funding. We provide possible solutions to address these barriers and share examples of specific quality improvement initiatives implemented across different world regions. Possible solutions to address these resource barriers include investment in human resources by increasing recruitment and training of the workforce, engagement of medical trainees and patients in quality improvement work, establishment of cancer registries and electronic medical records, and prioritization by large international funding agencies to invest in quality improvement research in LMICs. This review highlights four prevalent resources barriers to quality improvement in LMICs. Using examples from Botswana, Colombia, India, and Rwanda, we demonstrate solutions that may help overcome these barriers.
Pain et al highlight barriers to implementing QI cancer control in low- and middle-income countries
INTRODUCTION
In 2022, 19.98 million individuals were diagnosed with cancer and 9.74 million cancer-related deaths occurred globally.1 Low- and middle-income countries (LMICs) are disproportionally affected with 70% of newly diagnosed cancer cases occurring in LMICs and survival rates being 30%-50% lower than those of high-income countries (HICs).2,3 Current efforts focus predominantly on expansion of access to cancer services with less attention given to quality.4 The Lancet Global Health Commission on High Quality Health Systems demonstrated that poor quality care contributes to as much preventable mortality as no health care access at all.5
Given the increasing burden of cancer in LMICs predicted over the next several decades, research evaluating context-specific quality of care and programs in quality improvement are essential. Examples of quality improvement initiatives include decreasing cancer diagnostic delays, implementing evidence-based therapies, and addressing medication-administration errors.6 These initiatives can be implemented by establishing clear standards for these metrics, addressing barriers to meeting these standards, and designing interventions to help meet minimum performance standards.
Multiple barriers exist in the development of quality improvement programs, including adequate resources, organizational culture dynamics, political challenges, and cultural differences. This nonsystematic review will address resource barriers—namely, the lack of trained staff, adequate time for quality improvement work, research infrastructure, and funding. We present findings from 60 articles investigating these barriers within the context of cancer care delivery in LMICs and share quality improvement initiatives implemented across the globe.
DEFINING A SHARED VISION OF HIGH-QUALITY CANCER CARE
In 1999, the Institute of Medicine and the US National Cancer Policy Board advocated for formal monitoring of quality of cancer care and provided recommendations on how to measure and extend quality care to all people with cancer.7 The definition of high-quality cancer care has since expanded to include the delivery of patient-centered, evidence-based, and equitable cancer care; a workforce composed of skilled health professionals; and attention to ongoing quality measurement.8,9
Resources such as the WHO's Global Initiative on National Quality Policy and Strategy can help guide national cancer programs as they seek to develop priorities for quality improvement.10 The WHO has also defined specific targets for cancer control initiatives, which have been incorporated into National Cancer Control Plans (NCCPs). Moreover, the International Cancer Control Partnership has been pivotal in supporting countries in developing context-specific NCCPs and in coordinating engagement between national implementers and international organizations.11 Finally, ASCO developed the Quality Oncology Practice Initiative to provide a framework for improving quality through evidence-based practices. In 2020, this program expanded to include an LMIC track, making quality improvement development more accessible to providers in these settings.12
RESOURCE BARRIERS
Staffing Shortages
The shortage of providers and investigators trained in quality improvement poses a significant barrier to effective quality improvement initiatives in LMICs. WHO estimates a shortage of 10 million health care workers by 2030, with the largest shortages concentrated in LMICs.13 LMICs have 1.3 physicians and 2.5 nurses for every 1,000 people, compared with 3.1 physicians and 10.9 nurses per 1,000 people in HICs.14 As a result, the clinical volume per provider is significantly greater in LMICs than in HICs.15,16 Notably, there are severe staffing shortages of workers across all oncology subspecialties (pathology, surgery, medical oncology, and radiation oncology).17,18 This shortage of human capital pertains to both availability of trained staff and recruitment and retention of providers.15 Providers working in understaffed hematology/oncology units in LMICs are more likely to suffer from work-related stress and burnout,16,19 often leading to high staff turnover.20 Furthermore, global brain drain of educated providers migrating from LMICs to HICs contributes to the decline in availability of trained professionals in LMIC settings.21
Time Constraints
Time devoted to quality improvement initiatives is another essential resource. Lack of dedicated time for quality improvement efforts and competing clinical and administrative priorities are major barriers.22 A survey distributed to 1,115 oncology physicians in 65 countries revealed that 71% of LMIC physicians worked 6-7 days per week (compared with 21% of physicians in HICs).15 LMIC oncologists saw significantly more consults than HIC oncologists (425 v 175 consults per year). This contributes to less time spent per patient in clinic. The lack of adequate time could lead to delays along the cancer care continuum and diminished quality of care. Furthermore, these clinical demands leave little time for quality improvement training and engagement. Staff involved in quality improvement projects require not just time for implementation and evaluation of interventions but also time to set improvement goals and action plans.23 Efforts to carry out these projects without adequate time can lead to decreased motivation among staff.24-26
Lack of Available Research and Data System Infrastructure
An additional barrier to improving quality of cancer care in LMICs is the inadequacy of existing real-world data systems and infrastructure.27 Notably, cancer research is heavily concentrated in HICs, and there is a paucity of LMIC-generated evidence regarding best practices of cancer care delivery. Quality improvement programs require a systematic and iterative approach to identifying specific care improvement goals, developing and implementing interventions to meet these goals, and measuring whether these care delivery goals are accomplished. Subsequently, gaps in quality and patient outcomes can only be identified through ongoing data collection and analyses. Many LMICs rely on manual data extraction from paper charts rather than electronic medical records (EMRs), making it particularly challenging to access and analyze data needed to accurately measure quality in real time.8
Inadequate Funding for Quality Improvement
Finally, a quality improvement program requires dedicated funding. Strikingly, only an estimated 0.5%-5% of global cancer funding is directed to LMICs.28,29 An analysis of global funding for cancer research between 2016 and 2020 found that of the $23 billion in US dollars invested in cancer care, 41% was dedicated to research and 20% to drug development, whereas global health garnered only 0.5%.29 Although quality improvement initiatives may ultimately be cost effective, the upfront costs can be a significant barrier for countries where limited health care budgets must be prioritized for care delivery.30 Many of these countries are not able to budget for quality improvement in their cancer control efforts.31
POTENTIAL SOLUTIONS TO BARRIERS
Investing in the Cancer Care Workforce
The United Nations Sustainable Development Goals and the WHO Resolution stress the importance of investment in human resources by increasing health financing, recruitment, training, and retention of the workforce in LMICs.13,32 An understanding of the needs of the workforce can serve as a first step to address the growing shortages in staffing. One potential solution involves the establishment of cancer workforce registries to understand workforce gaps and capacities and health care worker migration patterns (Table 1).33
TABLE 1.
Resource Barriers to Quality Improvement Implementation in LMICs and Potential Solutions
| Resource Barrier | Potential Solutions |
|---|---|
| Staffing shortages | Establish cancer workforce registries to capture the needs of workers and identify patterns in migration Invest in education and recruitment of providers in LMICs Train staff in necessary skills to carry out quality improvement work |
| Time constraints | Emphasize the benefits of quality improvement work in improving workflow and patient outcomes Engage medical trainees and patients in the development and implementation of quality improvement programs Use task-sharing to nonphysician health workers to free up time for quality improvement |
| Lack of available research and data system infrastructure | Invest in cancer registries and hospital-based clinical databases Invest in electronic medical records (when feasible) and link these with national cancer registries Share quality improvement strategies through regional quality improvement group meetings |
| Inadequate funding | Use funding mechanisms from NIH/NCI to execute quality improvement research in LMICs and advocate for continued expansion of funding from these agencies Set priorities for quality improvement implementation at every level of oncology care delivery Specify costs devoted to quality improvement work into the budget |
Abbreviations: LMICs, low- and middle-income countries; NCI, National Cancer Institute; NIH, National Institutes of Health.
In addition, the Makuku and Mosadeghrad’s34 Root Stem Model offers a holistic approach to achieve health worker retention by targeting six workforce process stages: academic education, recruitment, job training, remuneration, workforce environment, and investment in staff. In adapting these to oncology staffing in LMICs, medical education strategies should include the establishment and improvement of medical education in LMICs and incorporation of quality improvement curricula into medical training.35,36 Efforts aimed at recruitment of workers can include full government scholarships with a commitment to work in areas of highest need.37 Third, investment in job training is needed to ensure that the workforce is well versed in necessary skills and knowledge to carry out daily work.38 Continuing medical education programs are essential in LMICs, as they are in HICs, and they can be a prerequisite for renewing employment at the workplace. Additionally, staff—including both clinical providers and researchers—need to be formally trained in quality improvement work, including didactic training of evidence-based medicine as well as methods of identifying and implementing interventions.22 Adequate remuneration that is linked to attaining specific quality improvement targets, as executed in countries like Tanzania, Rwanda, and Burundi, may motivate health workers to improve the quality of care delivered.39 Additionally, efforts to recruit and retain health workers must address workplace environment and living concerns.40 Finally, a long-term investment in the workforce is paramount; this involves adequate compensation, job promotions, and leadership opportunities.34
Addressing Time Constraints
Hospital leadership must provide time and resources devoted to quality improvement efforts (eg, mentor availability, coursework, access to collaborators from different disciplines).41 Given the high clinical demands of staff in LMICs, oncology department leadership must emphasize the importance of quality improvement work and the impact of implementing specific interventions to improve workflow, transitions in care delivery, and patient outcomes. Hospital leadership should assure adequate physician staffing to allow for these dedicated activities and not compromise daily patient care. An early investment in this work may reap future benefits.
One potential solution to the limited time resource is the engagement of medical trainees and patients in the implementation of quality improvement programs. First, trainees often have relatively more time to dedicate to educational efforts, and quality improvement education can have a significant impact on their long-term professional development. Trainees can develop projects under the guidance of staff which are based on their own clinical experiences or motivated by the needs of the cancer center. Recognizing the power dynamics at play between trainees and their superiors, there must be a culture where areas of improvement can be safely identified. Studies have demonstrated that the majority of trainees who are exposed to quality improvement education continue to incorporate work in quality improvement into their future careers.41 Additionally, the role of patients in quality improvement work is often underused. Providing opportunities for patient advocacy groups to serve as equal partners in promoting quality care can elevate this topic not only in the health care sphere but also in the public eye of civil society at large.42
Finally, task-sharing to nonphysician health workers can free up more time for quality improvement work.43 Undeniably, the scale-up of HIV care in sub-Saharan Africa would not have been possible without task-sharing, as evidenced by the incorporation of nurses and community health workers in the administration of care.44,45 Task-sharing will be essential across cancer care delivery as the burden of cancer increases in LMIC settings.
Investing in Quality Improvement Research and Data System Infrastructure
Increased oncology research in LMICs is needed to describe cancer epidemiology, treatment patterns, and outcomes to inform quality improvement metrics that are relevant to the LMIC context. These results can then be used to influence local policies made by high-level decision-making bodies, such as Ministries of Health, regarding in-country resource modifications and investments to support successful implementation of their NCCPs.
The implementation of cancer registries can help provide necessary cancer epidemiologic data. A Global Initiative for Cancer Registry Development was developed in 2011 primarily by the International Agency for Research on Cancer in collaboration with other stakeholders.46 Through this program, regional hubs have been developed that partner with countries in registry development and research capacity building. In addition to cancer registries, database development—particularly prospective databases—can build research capacity and lead to the development of quality improvement questions and projects informed by available health system data. In both HIC and LMIC settings, quality assessment and improvement efforts are frequently based at the hospital or program level. Hospital- or program-based clinical databases can be more feasible than national registries, given the smaller population size and need for coordination, and can lead to identification of critical local needs that may not be readily identified from a larger national registry.
A potential solution in building data system infrastructure is transitioning from paper records to EMRs. This transition, however, requires specific resource requirements and will require prerequisite training, adequate network, and high upfront procurement costs.47 Benefits include eliminating issues of misplaced patient data, linkage of EMRs with national cancer registries, and increased access to data for research activities.
Another potential solution for increasing capacity includes the development of regional quality improvement group meetings, much like regional tumor boards developed to facilitate discussion of clinical cases and management strategies. This shared knowledge process can enable clinical groups at different health systems to share strategies that have worked to address issues in care delivery.
Finally, in HIC settings, it has been proposed that implementation of clinical trials results in an infrastructure effect: an improvement in the quality of clinical care and outcomes for patients treated at institutions that participate in clinical trials, even for patient populations that are not study participants.48-50 A systematic review of the impact of institution and practitioner involvement on patient outcomes suggested that trial involvement at both hospital and physician levels trended with greater use of evidence-based treatment.51 Clinical trials can contribute to similar benefits in LMICs.
Expanding Funding for Quality Improvement and Research in LMICs
Across the spectrum of broad international public and private initiatives, several potential funding sources have the capability to directly or indirectly provide financial support for the incorporation of this essential work into oncology care in LMICs.
The US-based National Institutes of Health (NIH) provides 45% of the total funding for cancer research globally, far outpacing the next largest funder, the European Commission, which supplies 6.5%.29 The oncology-focused branch of the NIH, the National Cancer Institute (NCI), has increased support of cancer control programs in LMICs over the last decade and has developed a Strategic Plan for 2021-2025 to be carried out by the Center for Global Health.52 Programs include the International Cancer Control Partnership, which aims to support the development, implementation, and evaluation of data-driven NCCPs in participating countries. Priorities at the funder level often dictate the downstream focus of investigators; thus, an emphasis from NCI and Ministries of Health leadership on quality improvement efforts in global health research could prove to be an important mechanism for ensuring that funded research aims not only to advance clinical care but also to implement paradigms of high-quality care.
Funding mechanisms for global oncology research range from direct funding of investigators based in LMICs, funding of investigators from HICs working in LMICs, and joint partner funding of investigators from each setting. Collaboration between LMICs and HICs can provide a conduit for public funding from entities such as the NCI. The 2021 Global Oncology Survey of NCI-Designated Cancer Centers found that 13% of awards had an international collaborator.53 Several current awards have primary aims to evaluate and improve guideline-concordant care in LMICs. The NCI also partnered with the African Organization for Research and Training in Cancer to support the Beginning Investigator Grant for Catalytic Research initiative to fund research conducted by early-career African investigators.54
Ideally, governments and institutions in LMICs should set priorities for quality improvement implementation at every level of oncology care delivery and include the costs of such initiatives as a necessary component of care provision. In HICs, several factors pressure entities to incorporate such costs into operating budgets, including advocacy by patients and families for improved quality of care, review and regulation by private and public bodies, incentive payment structures, and medicolegal considerations.55 These expenditures drive the implementation of policies, procedures, and processes that optimize the quality of care delivered. Increasing the presence of these factors in LMICs may garner the political will and institutional motivation to make implementation a financial priority.56,57
EXAMPLES OF QUALITY IMPROVEMENT INITIATIVES
Below, we describe quality improvement efforts from four different LMIC settings, highlighting the implementation of the solutions discussed above.
Botswana
Timely initiation of cancer treatment requires accurate and timely pathology reporting. In Gaborone, Botswana, Martei et al58 measured the pathology turnaround time for breast cancer biopsy and surgical specimens analyzed at the National Health Laboratory (the major pathology service in the public sector) and the Diagnofirm Medical Laboratories (an independent laboratory that serves as a major referral for specialized pathology services) between 2011 and 2015. Within this period, several significant changes were implemented to improve the quality of pathology services. In 2012, the Botswana Ministry of Health expanded its pathology capacity by doubling the number of pathologists. Additionally, the University of Botswana implemented a pathology residency training program. Through a collaboration between the Ministry of Health, the National Cervical Cancer Screening Program, and the American Society of Clinical Pathology, automated tissue processing equipment and whole slide imaging system were obtained in 2013.59 The investigators aimed to determine whether these pathology scale-up efforts by the Ministry of Health decreased the pathology turnaround time for breast cancer specimens over this period. The turnaround time intervals were calculated by using the dates within the cascade of specimen processing and analysis, and intervals between 2011 and 2012 were compared with postimplementation intervals in 2013-2015.
Overall, there was a significant positive effect of scale-up efforts in Botswana. Notably, there was a 62% decline in median turnaround time for biopsy reports and an 82% decline in turnaround time for immunohistochemistry reporting from the period 2011-2012 to 2013-2015.58 However, there was no significant change in turnaround time for surgical specimens. The authors hypothesized that the delay in surgical pathology turnaround time could be the result of preanalytical processes (grossing, slicing, and slide preparation), and following that study, a strict 24-hour preanalytical processing turnaround time for surgical specimens was implemented. Overall, this study helped to identify pathology turnaround times that had improved after locally led interventions and areas where additional interventions were necessary. This retrospective analysis was feasible because of the availability of a multidisciplinary team, including trained research staff with quality improvement expertise, dedicated time for research, and a well-established EMR system for pathology reports that included detailed time stamp documentation of pathology processes.
Colombia
Cervical cancer is the second most frequent cancer in women in Colombia, with over 4,700 new cases and 2,400 deaths annually.60 Curative treatment for locally advanced cervical cancer requires external beam radiation with chemotherapy in addition to brachytherapy.61,62 Access to brachytherapy has been one of the greatest challenges in Colombia, which housed only 31 high dose rate (HDR) brachytherapy machines in 2022 for a population of 52 million people. Given this machine shortage, patients from the western Antioquia region were often referred to other states for brachytherapy completion, often leading to significant delays.
To improve the quality of care delivered, an HDR brachytherapy unit was purchased in 2015 in Clinica Somer, a hospital serving a population of over 700,000 people. Safe implementation of HDR brachytherapy required multiple resources. First, dedicated staff was needed, including a radiation oncologist, medical physicist, radiation therapist, and radiation nurse. This staff required specialized training in the delivery of brachytherapy and dedicated time to carry out brachytherapy procedures. In addition, anesthesiology support was needed for most cases. Implementation also necessitated infrastructure, such as a dedicated room for brachytherapy applicator placement, an operating room, and a shielded room for treatment delivery. A new treatment planning system was needed given the unique planning needs of brachytherapy compared with external beam radiotherapy. Finally, funding was needed for the costs of the HDR brachytherapy unit and periodic replacement of the radioactive sources.
To meet these needs and ensure delivery of safe, high-quality brachytherapy, a committee was formed to create an action plan and identified solutions for implementation of HDR brachytherapy. The local staff was trained in collaboration with the radiotherapy company Elekta, who supplied the brachytherapy equipment; this included travel to Germany for physicians to learn directly from the manufacturer and site visits within Colombia where Elekta representatives held training sessions to review machine functionality and planning software. A new treatment room was built to accommodate the brachytherapy treatments. This initiative was funded by the partnering hospital. Funding was secured after extensive discussion with key stakeholders, emphasizing the need to invest in this technology to improve the outcomes of women with cervical cancer in Colombia.
Since 2017, over 180 patients have been treated with brachytherapy at Clinica Somer. Notably, Clinica Somer accepts payment from the national health scheme that covers patients regardless of their ability to pay, ensuring that all women have access to this critical therapy. Future improvement efforts will focus on enhanced data sharing between institutions, ensuring that patients who receive external beam radiotherapy anywhere in the region can have their radiation plans electronically transferred to Clinica Somer.
India
Timely delivery of chemotherapy in daycare units across urban cities in India is an essential component of high-quality care.63 Delays from admission to the start of chemotherapy create several adverse impacts. First, there is suboptimal utilization of daycare beds and loss of daycare allotted time. Second, additional staff is required during such delays, which is challenging given staffing shortages at baseline across these settings. Finally, there is widespread patient dissatisfaction with these delays.
The first step to address this problem entails quantifying the existing delays in care along the cancer continuum. From February 2019 to July 2019, the time from daycare admission to chemotherapy administration was measured across three oncology daycare units in an urban hospital in Pune, India. The median time from daycare admission to chemotherapy administration was 80 minutes (range, 60-120 minutes), which was a significant delay.
From July 2019, several initiatives were implemented across all three daycare units to better use existing resources. First, order sheets for the following day's chemotherapy were completed in advance by the junior doctors. Additionally, customized packages of chemotherapy drugs and accessories for each patient were made available in the pharmacy on the morning of chemotherapy administration. An additional step involved stocking basic premedication drugs, saline infusion bags, and bottles in the clean utility room. Finally, treatments were brought to the daycare unit as soon as the patient was admitted by a designated runner.
Six months later, repeated clinic measurements found a significant improvement in the median time from daycare admission to the time of chemotherapy administration. The median time reduced from 80 minutes to 35 minutes, a 56.3% reduction. Since 2020, the process has been further streamlined by using physical chutes to send drugs from pharmacy to daycare units and organizing monthly meetings between the daycare and pharmacy staff for better coordination. Ultimately, this initiative was made possible due to an understanding of the existing delays in care, trained clinical and research staff with dedicated time to carry out this work, and an EMR system that could capture key time points in care delivery. This work has important policy implications in other LMIC settings, as it showed that better care coordination across disciplines could improve efficiency in chemotherapy delivery.
Rwanda
The Butaro Cancer Center of Excellence (BCCOE) was established in 2012 and has cared for more than 17,000 patients with cancer over the following decade. From the start, databases were established through a combination of an EMR and paper charts. A research director and staff have been supported by funds from US cancer centers, the nonprofit organization Partners In Health, and Rwandan Ministry of Health.
Previous research at BCCOE demonstrated that patients with breast cancer experience long delays before presenting to a health center.64 Pace et al65 thus created a health facility–level intervention in Burera District to train community health workers and nurses in signs and symptoms of breast cancer and clinical breast examinations, as well as facilitated mechanisms for referrals to the cancer center. Nurses received mentorship from a trained hospital-based nurse midwife. From April 2015 to April 2017, a cluster randomized trial was conducted. The investigators found that health centers receiving the intervention had more hospital visits and breast biopsies and higher breast cancer incidence than control health centers. The incidence of early-stage breast cancer was 3.3/100,000 (intervention) versus 0.7/100,000 (control), P = .048, suggesting that training health workers can facilitate earlier stage breast cancer diagnosis.65 Following the intervention, there was an increased demand for staffing and breast diagnostic services, suggesting that policymakers in LMICs should anticipate these increased resource needs while developing early detection programs. This work was implemented through consistent training of health care personnel, research funding, and electronic district hospital and BCCOE medical records.
In conclusion, the resource barriers to building quality improvement programs in LMICs include the lack of trained staff, adequate time for quality improvement, data and research infrastructure, and funding. To see substantive changes to improve care delivery, there must be investment in quality improvement training, innovative approaches to allow the workforce to prioritize quality efforts, enhancement of data systems and cancer registries to capture data needed for improvement, and dedicated funding for quality improvement work.
AUTHOR CONTRIBUTIONS
Conception and design: Debanjan Pain, Emily MacDuffie, Lawrence N. Shulman, Shona Nag, Surbhi Grover
Provision of study materials or patients: Lawrence N. Shulman
Collection and assembly of data: Debanjan Pain, Megan Kassick, Lina Loaiza Salazar, Dayssy Diaz Pardo, Shona Nag, Surbhi Grover
Data analysis and interpretation: Debanjan Pain, Yehoda M. Martei, Daniel J. Ikeda, Lawrence N. Shulman, Surbhi Grover
Manuscript writing: All authors
Final approval of manuscript: All authors
Accountable for all aspects of the work: All authors
AUTHORS' DISCLOSURES OF POTENTIAL CONFLICTS OF INTEREST
The following represents disclosure information provided by authors of this manuscript. All relationships are considered compensated unless otherwise noted. Relationships are self-held unless noted. I = Immediate Family Member, Inst = My Institution. Relationships may not relate to the subject matter of this manuscript. For more information about ASCO's conflict of interest policy, please refer to www.asco.org/rwc or ascopubs.org/go/authors/author-center.
Open Payments is a public database containing information reported by companies about payments made to US-licensed physicians (Open Payments).
Lawrence N. Shulman
Consulting or Advisory Role: Genentech
Dayssy Diaz Pardo
Employment: The Ohio State University
Shona Nag
Speakers' Bureau: Roche/India, Novartis, Lilly, Zydus Pharmaceuticals, AstraZeneca
Research Funding: Roche India (Inst), AstraZeneca (Inst), Novartis (Inst)
Surbhi Grover
Consulting or Advisory Role: GenesisCare
No other potential conflicts of interest were reported.
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