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Published in final edited form as: Cancer. 2023 Jan 3;129(5):671–684. doi: 10.1002/cncr.34630

Global Cancer Surgery in Low-resource Settings: a Strengths, Weaknesses, Opportunities, and Threats analysis

Samantha J Sadler 1, Erickson F Torio 2, Alexandra J Golby 2
PMCID: PMC10069626  NIHMSID: NIHMS1874231  PMID: 36597652

Abstract

Global cancer surgery is an essential and complex component of oncologic care. This study aims to describe global cancer surgery literature since the 2015 Lancet Commission on Global Surgery and Cancer Surgery and perform a SWOT analysis. A systematic search was performed in PubMed of global cancer surgery articles. Themes were extracted from the included studies based on the following criteria: (1) performed in low- or low-middle-income countries, (2) published during or after 2015, (3) published in peer-reviewed journals, (4) written in the English language, and (5) accessible to the authors. Themes were further groups into strengths, weaknesses, opportunities, and threats (SWOT analysis). The search strategy identified 154 articles published from 1992 to 2022. Forty-six articles were included in the qualitative synthesis and SWOT analysis. Recurring themes included local epidemiologic studies, local innovations and feasibility studies, prioritizing quality of life outcomes, multidisciplinary team approaches, limited resources, health system gaps, lack of economic analyses, diverse cancer management strategies and priorities, inter-setting collaboration, research expansion, the COVID-19 pandemic, and unchecked technological advancements. These strengths, weaknesses, opportunities, and threats were described and related to the themes of research, surgical systems strengthening, economics and financing, and political framing of the 2015 Lancet Commission on Global Cancer Surgery. SWOT analyses of global cancer surgery may be helpful in suggesting future strategies for this expanding field.

Keywords: global cancer surgery, SWOT analysis, low- and low-middle-income countries, health policy, cancer

Precis:

Global cancer surgery is an essential and expanding field in low resource settings. Performing a SWOT analysis of global cancer surgery may aid its growth in multiple areas.

Lay Summary:

Cancer surgery is a resource-intensive yet essential component of cancer care. In the face of projected growth of cancer burden, the present gap in cancer surgery care in low-resource settings with stressed healthcare and surgical infrastructure risks further exacerbation. We present a Strengths, Weaknesses, Opportunities, and Threats (SWOT) analysis of recent global cancer surgery literature pertaining to low-resource settings.

Background

The burden of cancer continues to grow globally, but not evenly. The 2019 Global Burden of Disease (GBD) study demonstrated that the burden of cancer is growing at a disproportionately high rate in areas with a lower socio-demographic index (SDI), a composite indicator of income per capita, average years of education and total fertility rate of females under 25 years-of-age 1, 2. From 2010 to 2019, countries in the low and low-middle SDI quintiles demonstrated the largest increase in annualized rates of change of the absolute numbers of cancer cases and deaths, as well as the age-standardized rates of mortality from, and incidence of, cancer. Morbidity and mortality due to cancer translates into an economic burden, which likewise disproportionately falls on low-resource countries 3.

Cancer surgery is an essential yet complex component of oncologic care. Surgery is used to achieve various goals in cancer management depending on timeline, symptoms, complications, and the nature of the cancer itself. Surgery plays a critical role in diagnosis, treatment, prevention, monitoring, reconstruction and functional restoration, and management of complications of cancer. For example, individuals discovered to have certain genetic predispositions to breast, colon, thyroid and/or gastric cancers may benefit from prophylactic surgical management 46. Preventative surgery includes early intervention with the discovery of precancerous lesions deemed to have high risk of malignant transformation. This decision-making hinges on the diagnostic capacity of cancer surgery, such as through biopsy. Cancer surgery may be curative in certain cases, often possible with early detection and intervention. Surgical cancer resection can also be performed primarily for symptom alleviation, even in non-curable, palliative cases. For example, symptoms caused by the cancer itself (i.e. paraneoplastic syndromes, ascites production, pain due to tissue invasion) or by secondary manifestations of cancer size (i.e. mass effect, lumen obstruction) may be indications for removal. Finally, reconstructive surgery for functional and/or body form restoration is an important consideration when the surgical cancer resection results in a defect that impacts the patient’s quality of life.

Cancer surgery is a resource-intensive, technically-challenging practice performed for prophylactic, preventative, diagnostic, curative, palliative and reconstructive purposes. Determining the appropriate role of surgery involves informed consideration of timing, pathophysiology, and symptomatology of the specific cancer and patient’s presentation. A recent estimate suggests that over 80% of all cancers require some surgical management, resulting in an estimated global need for 32 million cancer-related operations annually in 2015 and 45 million by 2030 7. More recent modeling by Perera et al. (2021) predicts a 52% increase in global surgical cancer cases between 2018 and 2040--approximately 5 million more procedures needed for cancer-related indications in 2040 compared to in 2018 8. Once the decision is made to pursue cancer surgery, there are significant technological, human, monetary, and intellectual resource requirements to facilitate such care; this includes various extra-operative components such as imaging, pathology, and adjunct oncologic therapies, such as chemotherapy, radiotherapy, and immunotherapy 9.

Unfortunately, broad, inclusive access to cancer surgery is not a present reality. In 2015, the Lancet Commission on cancer surgery explored the global landscape of cancer surgery in terms of the global need, the economic and financial complexities surrounding its delivery (or lack thereof), mechanisms for systems strengthening, research in cancer surgery and global surgery more broadly, as well as the complex and important role of government and politics in the future of global cancer surgery 7. The authors estimated that only 5% of patients in low-income settings have access to adequate cancer surgery performed in a safe, timely and effective manner. The 2015 Lancet Commission on global surgery likewise asserted the importance of cancer surgery to achieve equitable health outcomes, vouching for its inclusion in certain universal health coverage packages for more holistic oncologic management 10. Ultimately, as cancer and cancer surgery caseloads are expected to increase disproportionately in low-resource settings 11, 12, capacity-building for cancer surgery is essential for promoting equitable cancer treatment and outcomes globally 13, 14.

Engagement by key stakeholders is important to foster effective, sustainable, and resilient improvements in cancer surgery performance and outcomes. From the perspective of a given operative setting, these stakeholders include but are not limited to: the patients, patient families, local cancer surgery care providers (i.e. surgeons, other staff) and their multidisciplinary care-providing partners (i.e. pathology, radiology), local academic and healthcare institutions, local health policy-makers and relevant political figures, international research and training partners, and industry. With these key stakeholders in mind, it is important to understand the current state of cancer surgery in low-resource settings and associated interventions.

The objectives of this report are to (1) describe the landscape of global cancer surgery literature since the 2015 Lancet Commission on Global Surgery and Global Cancer Surgery and (2) characterize the global cancer surgery field through a Strengths, Weaknesses, Opportunities, and Threats (SWOT) analysis to inform future research and interventions.

Methods

An electronic literature search was performed on April 5, 2022 in PubMed using the search terms (“cancer surgery” OR “oncological surgery” OR “oncologic surgery” OR “surgical oncology” OR “tumor surgery”) AND (“low resource” OR “LMIC” OR “low income” OR “developing country” OR “developing nation”). Medical Subject Headings (MeSH) and non-MeSH terms were applied with filters utilized to reject studies published before January 1, 2015. The compiled reference list was reviewed for relevance. The reference lists of published studies and reviews were also examined to identify additional studies. The primary themes of interest were strengths, weaknesses, opportunities, and threats that affect Global Cancer Surgery stakeholders in low-resource settings. Included studies of Global Cancer Surgery met the following criteria: (1) performed in low-resource settings, which this review defined as low- or low-middle-income countries as defined by the World Bank for the 2023 fiscal year, or published in collaboration with low- to low-middle income countries; (2) published during or after 2015, the year the Lancet Commission on Global Cancer Surgery report was published; (3) published in peer-reviewed journals; (4) written in the English language; and (5) accessible to the authors. Excluded from consideration were studies about global surgery that did not treat cancer and studies describing cancer treatment without a surgical cancer focus. The following data were extracted and reported: first author and year of study, country, World Bank income classification for the 2023 fiscal year, whether the article was open access, study type, cancer type(s) and intervention(s) included. Studies were summarized and evaluated for themes, which were further grouped into strengths, weaknesses, opportunities, and threats (SWOT analysis).

Results

Our search strategy identified 154 articles published from 1992 to 2022. Of these, 123 articles were published during or after 2015. The inclusion and exclusion criteria were then applied to the titles and abstracts yielding 71 articles. These articles underwent full-text analysis resulting in 46 articles included in quantitative analysis, qualitative synthesis, and SWOT analysis (Table 1). The majority of included studies were published in 2021 and 2022 (n=26) (Figure 1). Thirty-four articles were open access (Table 1).

Table 1.

Description of studies produced and included by electronic literature search. The 46 articles that met inclusion criteria for analysis are listed here. For each article, the following descriptive data is included where applicable: first author, year, open access (yes/no), study type, country/countries (i.e. low-resource settings in which these studies were performed or pertain to) and the corresponding World Bank income classification(s), and the included cancer(s) and/or intervention(s).

First Author Year Open Access
(Yes/No)
Study Type Country/ Countries World Bank
Income
Classification
Cancer(s) Intervention(s)

Amin AT 2015 Yes Case series Egypt LMIC Colorectal Laparoscopic colectomy
Khan MK 2015 Yes Retrospective
cohort
Pakistan LMIC Gastric Subtotal gastrectomy, total gastrectomy, splenectomy with/without distal pancreatectomy (“total plus gastrectomy”)
Rukewe A 2015 Yes Case Report Nigeria LMIC Breast Single-shot lamina technique of paravertebral block
Bhatt A 2017 Yes Case series India LMIC Peritoneal métastasés cytoreductive surgery, hyperthermic intraperitoneal chemotherapy (HIPEC)
Martin AN 2018 Yes Restrospective
cohort
Rwanda LIC Gastric palliative (Gastrojejunostomy, exploratory laparotomy/primary perforation repair); curative (distal gastrectomy, other gastrectomy, Billroth I or II reconstruction)
Youssef MMG 2018 Yes Prospective Cohort Egypt LMIC Breast Oncoplastic breast surgery, axillary staging procedure
Ayandipo OO 2019 No prospective cohort study Nigeria LMIC Breast (primary) with cerebral métastasés craniotomy (infra- and supratentorial)
Ekdahl Hjelm T 2019 Yes Retrospective
cohort
Uganda LIC Breast Tumor/breast excisions, debulking/debridement, quadrantectomies, lumpectomies, simple-, radical- and palliative/toilet mastectomies
Khalil MAI 2019 Yes Retrospective
Cohort
Pakistan LMIC Renal cell carcinoma, angiomyolipoma, pseudotumor Partial nephrectomy
Almas T 2020 Yes Retrospective
cohort
Pakistan LMIC Various (soft tissue) sarcomas Wide local excision, compartmental excision
Asfour HY 2020 Yes Retrospective
Cohort
Egypt LMIC Wilms’ tumor Nephrectomy, lymph node sampling
De Oliveira, AJM 2020 Yes Retrospective
Cohort
Angola LMIC Multiple Surgical training in Brasil for Angolan doctors through the Cooperation Program for Foreign Doctors (PCME)
Debas H 2020 No Clinical Practice Guidelines Multiple Includes LMICs Multiple Guiding principles for equitable, sustainable, and effective partnerships between low- and high-resource settings by the American Surgical Association Working Group for Global Surgery
Deepa KV 2020 Yes Survey India LMIC Breast Breast conservation surgery
Elghazawy H 2020 Yes Review Egypt, Morocco, Saudi Arabia, Jordan Includes LMIC Breast Multiple
Fiaz S 2020 Yes Retrospective
Cohort
Pakistan LMIC Bladder Radiotherapy and Radical Cystectomy
Jamal A 2020 No Retrospective
Cohort
Pakistan LMIC Pancreatic, periampullary, duodenal Pancreaticoduodenectomy
Kumar N 2020 Yes Retrospective
Cohort
India LMIC Vulvar Wide local excision, bilateral inguinofemoral dissection, primary repair; radical vulvectomy; modified radical vulvectomy with or without lymph node dissection; reconstruction with V-Y gracilis myocutaneous and local rotation advancement V-Y fasciocutaneous flaps; therapeutic groin nodal dissection
Naeem A 2020 Yes Retrospective
Cohort
Pakistan LMIC Colon laparoscopic right or extended right hemicolectomy
Rizvi FH 2020 Yes Cohort Pakistan LMIC Breast level II axillary lymph node dissection (all patients); breast-conserving surgery (BCS), modified radical masectomy (MRM)
Akhtar N 2021 Yes Retrospective
Cohort
India LMIC Multiple N/A
Deo S 2021 Yes Retrospective
Cohort
India LMIC Multiple HIPEC
Deo SVS 2021 Yes Retrospective
Cohort
India LMIC Gastro-oesophageal, colorectal, breast, gynaecological, musculoskeletal, head-and-neck, hepatobiliary Multiple
Deo SVS 2021 Yes Retrospective
Cohort
India LMIC Colorectal N/A
Fadlalla WM 2021 Yes Randomized controlled trial Egypt LMIC Bladder Laparoscopic radical cystectomy, open radical cystectomy
Kamarajah SK 2021 No Prospective Cohort Multiple Includes LMICs Esophageal Esophagectomy
Kaul P 2021 No Retrospective case series India LMIC Oral Reconstructions of Large and Complex Oral Cavity Defects Using Extended Bipaddle Pectoralis Major Myocutaneous Flaps
Knight SR 2021 Yes Prospective Cohort Multiple Includes LICs & LMICs Breast, Colorectal, Gastric Multiple
Majbar MA 2021 No Retrospective
cohort
Morocco; France as comparison Includes LMIC Colorectal colo-anal anastomoses (delayed, classical)
Malik AA 2021 No Clinical Practice Guidelines Pakistan LMIC Colorectal Multiple
Mishra V 2021 Yes Retrospective
Cohort
India LMIC Oral squamous cell carcinoma N/A
Naveed S 2021 Yes Retrospective
Cohort
India LMIC Gallbladder Radical cholecystectomy, lymph node ratio
Ndlovu N 2021 Yes Report Zimbabwe, Cameroon, Nigeria, Tanzania, Kenya LMICs Multiple N/A
Perera SK 2021 No Cross-sectional
study
Multiple Includes LICs & LMICs Multiple Multiple
Ranganathan K 2021 No Review Multiple Includes LICs & LMICs Breast N/A
Ranganathan P 2021 Yes Review India LMIC Multiple Multiple
Sohail S 2021 Yes Retrospective
Cohort
Pakistan LMIC Adrenocortical carcinoma Radical adrenalectomy
Arshad A 2022 Yes Cohort Pakistan LMIC breats, parotid, oesophagus, chondosarcoma cancers with metastatic spine disease Posterior surgical decompression and fixation of the spine.
Chargari C 2022 No Review Multiple LMICs Cervical Resection, lymph node dissection
DeBoer RJ 2022 Yes Retrospective
Cohort
Rwanda LIC Cervical Radical hysterectomy, chemoradiation, upfront chemotherapy
Hornstein P 2022 Yes Cross-sectional Multiple Includes LICs & LMICs Multiple N/A
Houssaini K 2022 No Retrospective
Cohort
Morocco LMIC Hepatocellular carcinoma Liver resections
Rashad N 2022 Yes Consensus
guidelines
Egypt LMIC Colorectal N/A
Selmouni F 2022 No Prospective Cohort Morocco LMIC Colorectal Fecal immunochemical test
Souadka A 2022 Yes Cross-sectional Morocco, Algeria, Tunisia, Mauritania, Libya Includes LMICs Ovarian, Gastric, Colorectal, Pseudomyxoma peritonei Cytoreductive surgery with hyperthermic intraperitoneal chemotherapy.
Vohra LM 2022 Yes Retrospective
Cohort
Pakistan LMIC Breast N/A

Figure 1.

Figure 1.

Included publications by year published. The online literature search yielded 123 articles, of which 46 articles met inclusion criteria for analysis. The majority of included studies were open access (n=34) and published between 2021 and 2022 (n=26).

A SWOT analysis was performed utilizing the themes gathered from the included studies to further illustrate current cancer surgery research in resource-limited areas; brief descriptive summaries of key identified themes were synthesized and tabulated (Figure 2). Below, we elaborate on aspects described in the SWOT table that are not otherwise described in the background.

Figure 2.

Figure 2.

SWOT analysis of the current global cancer surgery landscape. A literature review was performed of global cancer surgery studies involving low-resource settings published since the landmark 2015 Lancet Commission on Global Surgery and Global Cancer Surgery. Key findings and themes from the included papers were characterized through a Strengths, Weaknesses, Opportunities, and Threats (SWOT) analysis.

Strengths

Local epidemiologic studies

Studies describing the local landscape of cancer surgery burden, caseload, operative techniques, outcomes, and barriers are foundational to identifying key intervention targets and to evaluating change over time 15, 16. On a more “microscopic” level, recent studies highlighting differences in tumor pathology and epidemiology between settings have yielded important insights 1721. A study among Indian patients status-post radical cholecystectomy for gallbladder carcinoma supported the utility of evaluating lymph node involvement for determining prognosis 19. While some of the cancers investigated may be considered rare, these studies provide critical context for targeted design and informed assessment of effective local interventions.

Local innovations and feasibility studies

A number of studies in low-resource settings have investigated the feasibility of utilizing certain intraoperative techniques, equipment and other technological advancements which have been previously proven effective in higher-resource settings. It should be noted that many (but not all) of the feasibility studies discussed in this section used small sample sizes and/or were performed at a single, high-volume cancer center; this raises questions, for example, about the generalizability of study findings across variable patient populations or among smaller community hospitals, which may more accurately represent the average care received within a given country. It is important to appreciate that these study design limitations in many ways reflect the local resource limitations of low-resource settings and thus provide contextual value for future studies. A few key studies are highlighted below.

Since the 2015 Lancet Commission on Global Surgery, a number of studies on the feasibility and safety of surgical procedures for several cancers including orofacial, gastrointestinal, urological, gynecological, breast, brain, and spine tumors have been performed in countries including Egypt, India, Nigeria, Pakistan, and Taiwan 2236. It is notable that most of these studies were performed at a single institution, with multicenter collaborative studies being rare. Surgical interventions described mostly include resections which aim to maximize overall survival and progression-free survival such as pancreaticoduodenectomy, gastrectomy, hepatectomy, cytoreductive surgery, laparoscopic colorectal surgery, radical cystectomy, partial nephrectomy, and brain and spine tumor removal. A number of techniques were described with an alternative primary goal of improving quality of life, such as oncoplastic surgery, breast-conserving therapy, spine stabilization 23, 28, 31, 36; this concept is further explored in the following section.

Critical to the success of many complex surgical procedures in oncology is the integration of technological advancements into low-resource surgical settings. For example, a few studies investigated the feasibility of implementing laparoscopic surgery in lower-resource settings 22, 37. The ongoing costs involved with laparoscopic equipment is significant due to the need for single use components. Thus, one study determined that reusing certain components of laparoscopic equipment deemed “single-use” for colectomies by the manufacturer may be a feasible option to reduce costs and increase access to these operations 22.

Creating cost-effective alternatives for existing technologies is also a target of research interest. Application of hyperthermic intraperitoneal chemotherapy (HIPEC) was also described 25, 26, 38, with some institutions demonstrating a capacity to locally engineer their own HIPEC machines. A group in India created a “homemade” HIPEC machine that reduced the cost of consumables to less than a third of that of commercially available products while demonstrating similar patient outcomes 25. Thus, feasibility studies on local adaptation of technological advancements in surgery are important to reducing cost and securing more equitable access to standard-of-care surgical procedures 23, 39, 40.

Finally, cancer surgery facilities and system operations also offer a target for improvement. For example, surgical oncologists in a Moroccan tertiary cancer center implemented a series of quality improvement interventions targeting inter-staff communication, electronic patient data management, treatment protocol development, and morbidity and mortality reviews 41. In the following year, there was a significant decrease in severe postoperative complications from liver resections for primary tumors or metastases. This study suggests a positive relationship between improving administrative and interpersonal functions and patient safety, which may be achieved through applying organizational practices, technological advances or other quality improvement interventions.

Prioritizing quality of life outcomes

Feasibility studies in cancer surgery from LMICs have expanded to cover not only survival outcomes but also quality of life measures. A qualitative approach to evaluating surgical oncology effectiveness and to guiding interventions is the relative impact on patient quality of life. Cancer surgery can be performed for a wide range of urgent and nonurgent indications, the latter including surgical procedures performed for palliative or reconstructive purposes. Preserving or improving a patient’s quality of life is a critical function and consideration of cancer surgery 42 and therefore an important consideration in providing equitable surgical cancer care 28. Palliative cancer surgeries may be particularly important in low resource settings due to a higher burden of advanced, and therefore more symptomatic disease 43. A study in India demonstrated feasibility and effectiveness of palliative operations for a variety of cancer patients, with the vast majority of patients endorsing subsequent symptomatic relief 18. However, post-operative morbidity is an important consideration for any procedure, especially for patients with limited financial resources, health literacy, or access; weighing these risks and benefits necessitates a case-by-case determination and discussion with the patient and family.

Surgery for breast cancer carries a particularly sensitive physical burden, and thus a number of studies in LMICs have investigated the feasibility and effectiveness of various surgical approaches 31, 35, 36, 44. Two options for breast cancer surgery include (modified radical) mastectomy, which often involves removing the entire breast, and breast-conserving surgery, in which the cancerous tissue is removed selectively to minimize the loss of normal breast tissue; thus, the mastectomy approach causes a more drastic physical alteration than a more targeted, “breast-conserving” approach. The recommended type of surgery varies based on a combination of clinical findings and patient preferences.

While overall self-reported quality of life scores among women receiving either surgical treatment may be similar, breast-conserving approaches may be associated with improved body image 36, 44. Further, a study in Egypt found that implementing oncoplastic, breast-conserving techniques in the primary surgical treatment of breast surgery was a feasible way of improving patient satisfaction and achieving appropriate resection margins, which may reduce the need for future procedures 31. Rizvi et al. (2020) further demonstrated no difference in complication rates between patients receiving modified radical mastectomy and breast conserving surgery in Pakistan 35.

Multidisciplinary team approaches to cancer care

Cancer is a complex disease, and thus multidisciplinary management is the standard of care for most cancers 45. Patients frequently engage multiple specialties at different time points along the disease trajectory, including before and after surgery. Education and support for healthcare personnel who are involved in diagnosis and treatment before cancer surgery is an important aspect of multidisciplinary investment, as these may influence utilization of surgical interventions 46. It is also important to consider the downstream effects of engaging patients at that point of their care journeys. Just as cancer surgery is inherently an interdisciplinary field, so should efforts toward achieving equitable cancer surgery outcomes be multidisciplinary in nature. For example, recognizing that pathology and radiology are integral to cancer surgery, we must not neglect extrasurgical infrastructure as we push for innovative surgical cancer approaches. Moreover, pain management and anesthesia are critical to safe interventions and reducing patient suffering. A case study from a Nigerian hospital showed that utilizing a thoracic paravertebral block as an adjunct to general anesthesia produced long-lasting post-operative pain control following radical mastectomy 47. Importantly, usage of this block was associated with shorter lengths of stay in PACU and overall hospital stay and reduced opioid consumption. This example also highlights how inter-disciplinary collaboration to improve efficient and effective postoperative pain management can improve patient outcomes qualitatively and quantitatively.

Weaknesses

Limited resources and perioperative services

Resources are severely lacking in all aspects of cancer surgery in LMICs. Low-resource healthcare systems commonly lack adequate cancer management resources across all aspects of cancer surgery, including limited cancer workforce personnel 48 and few cancer specialty hospitals (Arshad, 2022). Further, patients who undergo surgical cancer treatment in low-resource areas tend to have higher rates of severe postoperative complications 49 and mortality 50. In LMICs, poor post-operative care infrastructure was associated with seven to ten more deaths per 100 major complications 49.

Limited essential extra-operative services, including pathology, imaging, and adjunct therapies (i.e. chemo/radio/immune/brachytherapy) pose a significant challenge to improving cancer surgery outcomes and accessibility 42. For example, breast-conserving surgery, an alternative to mastectomy whose importance is explored earlier in this piece, is usually followed by radiation therapy to the remaining breast tissue, if available. Mastectomy may be otherwise be recommended in the absence of available radiation therapy for appropriate margins. Unfortunately, radiation therapy is exceedingly difficult to access in low- versus high-resource settings. In Africa, for example, low-income countries have so few megavoltage machines (MVM) for radiation therapy that there are 39.8 million people per MVM, orders of magnitude higher than the Atomic Energy Agency’s recommendation of 250,000 people per MVM 51. While this is perhaps the most drastic example, this trend is consistent in lower-middle income countries in both Africa and Latin America, whose populations are served by 2.47 and 1.64 million people per MVM, respectively. Of note, data from lower-resource settings in the Middle East, South Asia, and Southeast Asia were limited in this study.

Other proposed barriers to improved cancer surgery access, facilitation, and outcomes in low-resource settings include, but are not limited to: delayed presentation due to geographic isolation and transportation challenges 52 and sociocultural and sociopolitical factors, which ultimately increases care cost and complexity 53; unaffordable out-of-pocket costs 54 which may disproportionately affect individuals in low-resource settings 55; poor national cancer and cancer surgery registries, which may hinder accurate estimations of cancer surgery gaps and needs 7, 16, 43.

Broader health system gaps

Indirect approaches, which emphasize external systems or policies that influence surgical cancer care, have also been a source of interest to researchers. For example, a study in Morocco sought to improve early cancer detection rates by providing point-of-care fecal immunochemical testing at primary health centers and offering colonoscopies for those who tested positive 56; however, only 62.6% of those who tested positive successfully underwent a subsequent colonoscopy, with many patients citing logistical and financial barriers to attending the follow-up procedure and appointments. Furthermore, the increased burden on the Moroccan surgical infrastructure due to more patients seeking colonoscopies secondary to the positive fecal screening intervention resulted in increased wait times and, as a result, decreased compliance. This is an important reminder that despite potential benefits of earlier cancer screening, non-surgical techniques that require diagnostic and/or surgical follow-up do not necessarily overcome barriers to surgical access, may overburden under-equipped systems, and, therefore, should be implemented thoughtfully in low-resource settings.

Lack of economic analyses

Although desperately important, detailed economic and cost-effectiveness studies of cancer surgery performed in low-resource settings are limited 13, 57. A select few of the aforementioned feasibility studies included detailed cost-effectiveness analyses in their evaluation of specific intervention effectiveness and sustainability 22, 25, and others have asserted the importance of considering cost when developing interventions 23, 37, 39, 40. Horton & Gauvreau (2015) produced the most detailed global summaries by surgical oncology subspecialty, even stratifying different interventions by relative cost-effectiveness 57. The net return on investing in cancer surgery in terms of patient outcomes is generally viewed as positive. For example, an essential cancer control intervention package for low- and middle-income countries outlined how a USD$20 billion-per-year increase in spending on relevant interventions should ultimately improve cancer outcomes in low- and middle-income countries, which included provision of cancer surgery 58. However, detailing the monetary investment return – and comparing this return to the relative cost-effectiveness of alternative interventions – will be important for garnering funding and influencing long-lasting policy change, thus elevating cost-effectiveness as an important area for further research. A holistic cost-effectiveness evaluation should compare cancer surgery to other major health interventions or programs competing for political or philanthropic support, such as infectious disease (i.e. malaria). A critical foundational component of economic and financial planning lies in evaluating the local feasibility of the proposed surgical intervention 23, 39, 40.

As highlighted in Sullivan et al. (2015), the effects of including cancer surgery in universal health care coverage plans in low-resource settings should be evaluated by further research 7. Given that cancer surgery is often not explicitly included in universal health care coverage plans, little data exist on the impact, limitations, and costs of increasing access to cancer surgery in settings experiencing significant resource restrictions in their medical systems. In the United States, a decidedly high-resource setting, states that expanded Medicaid coverage under the Affordable Care Act demonstrated a significant increase in cancer surgery utilization among low-income residents 59, though further research is needed to determine the ultimate impact on outcomes. It is uncertain whether LMICs will demonstrate a similar effect on service utilization due to differences in resources and settings.

Opportunities

Diverse cancer management strategies and priorities at the local level

An important theme among approaches to strengthening surgical systems is local context and adaptation. It is critical to understand, respect, and center local perspectives toward cancer management strategies and execution when developing interventions or quality improvement strategies 38, 60. A survey conducted among North African physicians across multiple institutions regarding peritoneal surface malignancy management illustrated great diversity in oncologic management strategies 38. This diversity illustrates not only local intervention targets but also opportunities that could potentially be applied to multiple settings, such as developing formal referral structures within local healthcare systems. In this way, “local adaptation” does not necessarily require developing novel interventions but rather requires selecting interventions that respect local context and needs. Another example of this lies in locally validating metrics used in other, perhaps higher-resource settings. For example, a study in Mexico City among patients who underwent surgery for colorectal cancer evaluated patient outcomes using modified Cancer Care Ontario quality-of-care indicators for colorectal cancer management, a framework of indicators designed to compare outcome metrics over time 61. This study found these indicators, which were produced for primary use in a high-income setting, useful for evaluating improvement over time in their low-resource healthcare setting. While there are certainly benefits to widely standardizing cancer surgery approaches, local adaptation is critical – and feasible 6264.

Inter-setting collaboration: research, education, and surgical training

Multiple cancer surgery studies have encouraged bidirectional, thoughtful collaboration between high- and low-income medical centers and surgical providers to mutually share and engage with cancer surgery research, education, and training 30, 42, 6567. A few studies facilitated explicit, guided opportunities for local stakeholders to produce and execute research proposals to maximize intervention appropriateness. For example, local workshops held by the International Collaboration for Research Methods Development in Oncology (CReDO), demonstrated a high rate of subsequent research project execution among individuals attending from low-resource settings 68. Training cancer surgeons in low-resource settings is another topic of international interest, as such operations require a complicated skillset to perform. One study investigating the significance of a training program for Angolan surgeons in Brazil (an upper-middle income country) by the Cooperation Program for Foreign Doctors saw increased surgical specialty diversity in Angola following training 69.

Importantly, an ethical partnership and positive relationship must be maintained between partners of lower and higher-resource countries that proactively address sustainability, cultural differences, and overall expectations; Debas et al. (2020) provides an example of guiding principles to ensure these concepts are addressed in partnerships written by the American Surgical Association Working Group for Global Surgery 65.

Thoughtful research expansion

Building capacity within low-resource settings to conduct high-quality primary research is of utmost importance in achieving equity in oncology research. This literature search demonstrated an increase in the volume of published global cancer research in low-resource settings since 2015 (Figure 1). In these efforts to expand research in surgical oncology and related topics, it is critical to empower groups who are historically underrepresented in such research, including women and authors from low resource settings 70.

Threats

The COVID-19 pandemic

The impact of the COVID-19 pandemic on healthcare systems globally illustrates how external stressors can overwhelm overburdened medical and surgical systems in both low and high resource settings. Few studies have yet to demonstrate the impact of the COVID-19 pandemic on surgical operations in low-resource settings, much less on cancer surgery specifically 14, 7173. A study conducted in Pakistan showed that breast cancer patients who underwent surgery further into the COVID-19 pandemic presented with more advanced disease that often necessitated more aggressive treatment, perhaps due to fear of contracting COVID-19 and reduced operational capacity during this time 73.

Unchecked technological advancements risk widening disparities

We must encourage explicit consideration of implementation nuances in low-resource settings when evaluating new technological advancements developed in (and for) higher-resource settings. Local context is important to intervention adoption, preparation, delivery, and scaling 74. Therefore, as resource-intensive research in high-resource contexts produces new resource-demanding technology, universal implementation of such products may be challenging and therefore could contribute to widening outcome and surgical procedural gaps 66.

For example, implementing robotic surgery platforms incurs both hefty up-front and maintenance costs. While locally manufacturing certain components of these expensive systems may eventually help decrease costs, limited data on long-term costs and feasibility call into question the sustainability of modern-day robotic surgery in low-resource areas 75. Image-guided surgery for tumor ablation is another increasingly common yet highly resource-intensive surgical approach to cancer 76. With advancements in this field developed in high-resource settings leading to increasing technology reliance, such as with the MRI-dependent Minimally INvasive IMage-guided Ablation (MINIMA) technique 77, the gap to implementing new standard-of-care approaches grows.

Aforementioned studies investigating local adaptability of technologies widely used in well-resourced areas demonstrate hopeful results. However, when research into surgical technology advancements is conducted, the process of equitable dissemination should be considered at the forefront of the design phase such that downstream project decision-making is rooted in inclusivity.

Discussion

Based on our literature search, there has been a significant increase in the number of published global cancer surgery studies in LMICs since 2015 (Figure 1). This result may indicate increased awareness and research capacity of LMIC stakeholders regarding cancer surgery. There is significant heterogeneity in the topics within cancer surgery in LMICs, perhaps attributable to variability in prioritization, stakeholders, and settings across and within countries. Further, this search only included published works, which may not reflect the direction or outcomes of ongoing, unpublished works at this time. While developing policies more broadly generalizable to LMIC settings may have utility in increasing awareness, collaboration, and perhaps outcomes, the authors surmise that given the diversity, ultimately local stakeholders in their respective LMICs are critical to developing effective local policies and interventions as the stewards of cancer surgery within their specific health ecosystem. Thus, stakeholders and settings may utilize the themes gathered in this review and SWOT analysis to inform local strategies for improving global cancer surgery.

In the 2015 Lancet Commission on Global Cancer Surgery, the authors analyze and describe cancer surgery data across various spheres essential to cancer surgery, including research, surgical systems strengthening, economics and financing, and political framing 7. This presents a useful framework for understanding the current landscape of global cancer surgery since this landmark publication, as understood from our literature review.

In terms of research, the current literature suggests a growing emphasis on local disease etiology and pathophysiology, as well as local feasibility studies trialing cancer surgery equipment, approaches, techniques, and technology in local low-resource settings. The definition of “patient outcomes” has itself been challenged to highlight patient quality of life, a qualitative shift that may better reflect local perception of and patient experiences with cancer surgery outcomes. Successful workshops held between participants from low- and high-resource settings to further research and training is encouraging and should remain a focus of research for further development of these collaborations. Engagement of local stakeholders across all levels of research and intervention implementation is critical to success.

To foster further progress in research and global cancer surgery outcomes, there are a few notable opportunities for investigation and expansion. For example, investigators should further characterize the gap in both cancer surgery access and outcomes. Given the heterogeneous nature of the “cancer surgery” field, it is no surprise that the associated risks, complexity, utility, and urgency of different operations vary. There is a need for a more detailed investigation into how these indicators of quality cancer surgery differ by the goal of the cancer surgery performed as this may better highlight targets for intervention.

Further, effective development and local adaptation of surgical techniques, technology, and other quality improvement interventions in low-resource settings relies on high quality feasibility studies. Importantly, feasibility study outcomes are in many ways dictated by local context and thus should be designed and analyzed accordingly; this offers important data about local context. However, larger and more inclusive studies may help identify more generalizable principles for cancer surgery interventions.

Limited cancer surgery infrastructure remains a significant barrier to progress. Postoperative infrastructure, outcomes and complications remain disproportionately poor among patients receiving care in low-resource settings. Moreover, the burden of cancer is growing at a disproportionately high rate in low-resource settings, further stressing limited cancer surgery infrastructure with increased cases and potentially more severe disease. Advancements in technology, while encouraging, also raise the threat of disproportionate distribution. Surgical training in collaboration with higher-resource settings is a promising approach to surgical access expansion when conducted in an ethical, attentive manner. Point-of-care interventions for screening, while effective, may further stress already limited cancer surgery infrastructure in low-resource settings. The COVID-19 pandemic highlighted how other burdens on healthcare may further exacerbate this burden and can contribute to delayed presentation for care. Future research should further investigate ways to optimize cancer surgery coverage and utilization in low-resource settings with less robust healthcare infrastructure such that available surgical systems are adequately prepared for an anticipated increase in utilization.

The economics and financing of surgical oncology in low-resource settings remains an underexplored yet essential component of global cancer surgery efforts. This gap presents a barrier to progress, as limited financial resources in LMICs present challenges to equitable and long-term care provision that must be factored into intervention selection and planning. The local emphasis on research in current literature, as previously described, lays a strong foundation for future financial modeling at a local level, which is critical for informing intervention selection and future funding targets to produce the most efficient, effective outcomes with a given budget. Future feasibility studies should include financial models, when possible, as cost-effectiveness is paramount when defining what interventions may be considered “feasible” in resource-restricted settings.

Finally, the present literature review revealed a paucity of themes pertaining to political framing of global cancer surgery in low resource settings 72. Perhaps the most salient point lies in the opportunity for including cancer surgery in universal healthcare coverage, which carries political weight. Further, understanding the relative cost effectiveness of cancer surgery versus other interventions for infectious or other diseases may help inform political or even philanthropic decision-making. This exemplifies how economics and financing of global surgery are intertwined with the political infrastructures governing surgical care delivery. Thus, engaging political figures is important for progress in global cancer surgery.

Conclusion

Global cancer surgery is a growing field. This SWOT analysis describes the landscape of global cancer surgery through a literature review of published studies since the 2015 Lancet Commission. Ultimately, the growing body of published literature in global cancer surgery appears to reflect increased attention to this important area. Of the literature reviewed in this analysis, Strengths include local studies investigating cancer epidemiology as well as surgical and technological innovation, studies that highlight quality-of-life as a key surgical outcome metric, and demonstration of successful interdisciplinary work to promote progress in cancer surgery. Weaknesses include systems-level limitations, such as resource, perioperative services, and broader health system gaps, and a paucity of detailed economic analyses related to cancer surgery. Opportunities include diverse cancer management strategies at the local level, successful inter-setting collaborations to progress research, education, and surgical skills training, and thoughtful research expansion for an inclusive future. Threats include future large-scale stresses on the local healthcare infrastructure like the COVID-19 pandemic and the risk posed by unchecked technological advancements to widening disparities.

This SWOT analysis may inform local intervention strategies and action plans to help stakeholders in LMICs achieve Global Cancer Surgery goals. Similar analyses are needed at the local level help elucidate best practices around the world that might be applied to other similar settings.

Acknowledgements:

We gratefully acknowledge the work of the researchers whose pieces have contributed to the fund of knowledge supporting the present piece, particularly the efforts of local researchers in low-resource settings. We support greater inclusion in academic journals of authors from low-resource settings.

Funding:

AJG receives support from the Jennifer Oppenheimer cancer initiative and NIH P41EB028741.

Footnotes

Conflict of Interest: There are no conflicts of interest.

References

  • 1.Kocarnik JM, Compton K, Dean FE, et al. Cancer Incidence, Mortality, Years of Life Lost, Years Lived With Disability, and Disability-Adjusted Life Years for 29 Cancer Groups From 2010 to 2019: A Systematic Analysis for the Global Burden of Disease Study 2019. JAMA Oncol. Dec 30 2021;doi: 10.1001/jamaoncol.2021.6987 [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 2.Wang H, Abbas KM, Abbasifard M, Abbasi-Kangevari M, Abbastabar H, Abd-Allah F, Abdelalim A, Abolhassani H, Abreu LG, Abrigo MR and Abushouk AI Global age-sex-specific fertility, mortality, healthy life expectancy (HALE), and population estimates in 204 countries and territories, 1950–2019: a comprehensive demographic analysis for the Global Burden of Disease Study 2019. Lancet. Oct 17 2020;396(10258):1160–1203. doi: 10.1016/S0140-6736(20)30977-6 [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 3.Ranganathan K, Singh P, Raghavendran K, et al. The Global Macroeconomic Burden of Breast Cancer: Implications for Oncologic Surgery. Ann Surg. Dec 1 2021;274(6):1067–1072. doi: 10.1097/sla.0000000000003662 [DOI] [PubMed] [Google Scholar]
  • 4.Garber JE, Offit K. Hereditary cancer predisposition syndromes. J Clin Oncol. Jan 10 2005;23(2):276–92. doi: 10.1200/JCO.2005.10.042 [DOI] [PubMed] [Google Scholar]
  • 5.Oseni T, Jatoi I. An overview of the role of prophylactic surgery in the management of individuals with a hereditary cancer predisposition. Surg Clin North Am. Aug 2008;88(4):739–58, vi. doi: 10.1016/j.suc.2008.04.010 [DOI] [PubMed] [Google Scholar]
  • 6.You YN, Lakhani VT, Wells SA Jr. The role of prophylactic surgery in cancer prevention. World J Surg. Mar 2007;31(3):450–64. doi: 10.1007/s00268-006-0616-1 [DOI] [PubMed] [Google Scholar]
  • 7.Sullivan R, Alatise OI, Anderson BO, et al. Global cancer surgery: delivering safe, affordable, and timely cancer surgery. The Lancet Oncology. September 1, 2015 2015;16(11):1193–1224. doi: 10.1016/S1470-2045(15)00223-5 [DOI] [PubMed] [Google Scholar]
  • 8.Perera SK, Jacob S, Wilson BE, et al. Global demand for cancer surgery and an estimate of the optimal surgical and anaesthesia workforce between 2018 and 2040: a population-based modelling study. Lancet Oncol. Feb 2021;22(2):182–189. doi: 10.1016/S1470-2045(20)30675-6 [DOI] [PubMed] [Google Scholar]
  • 9.Wyld L, Audisio RA, Poston GJ. The evolution of cancer surgery and future perspectives. Nature Reviews Clinical Oncology. 2015-02 2015;12(2):115–124. doi: 10.1038/nrclinonc.2014.191 [DOI] [PubMed] [Google Scholar]
  • 10.Meara JG, Leather AJM, Hagander L, et al. Global Surgery 2030: evidence and solutions for achieving health, welfare, and economic development. The Lancet. August 8, 2015 2015;386(9993):569–624. doi: 10.1016/S0140-6736(15)60160-X [DOI] [PubMed] [Google Scholar]
  • 11.Bray F, Jemal A, Grey N, Ferlay J, Forman D. Global cancer transitions according to the Human Development Index (2008–2030): a population-based study. Lancet Oncol. Aug 2012;13(8):790–801. doi: 10.1016/S1470-2045(12)70211-5 [DOI] [PubMed] [Google Scholar]
  • 12.Soerjomataram I, Bray F. Planning for tomorrow: global cancer incidence and the role of prevention 2020–2070. Nat Rev Clin Oncol. Oct 2021;18(10):663–672. doi: 10.1038/s41571-021-00514-z [DOI] [PubMed] [Google Scholar]
  • 13.Dare AJ, Anderson BO, Sullivan R, et al. Surgical Services for Cancer Care. In: Gelband H, Jha P, Sankaranarayanan R, Horton S, eds. Cancer: Disease Control Priorities, Third Edition (Volume 3). The International Bank for Reconstruction and Development / The World Bank; 2015. [PubMed] [Google Scholar]
  • 14.Ndlovu N, Ndarukwa S, Nyamhunga A, et al. Education and training of clinical oncologists-experience from a low-resource setting in Zimbabwe. Ecancermedicalscience. 2021;15:1208. doi: 10.3332/ecancer.2021.1208 [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 15.Kumar N, Ray MD, Sharma DN, et al. Vulvar cancer: surgical management and survival trends in a low resource setting. J Egypt Natl Canc Inst. Jan 14 2020;32(1):4. doi: 10.1186/s43046-019-0015-y [DOI] [PubMed] [Google Scholar]
  • 16.Ekdahl Hjelm T, Matovu A, Mugisha N, Lofgren J. Breast cancer care in Uganda: A multicenter study on the frequency of breast cancer surgery in relation to the incidence of breast cancer. PLoS One. 2019;14(7):e0219601. doi: 10.1371/journal.pone.0219601 [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 17.Asfour HY, Khalil SA, Zakaria AS, Ashraf ES, Zekri W. Localized Wilms’ tumor in low-middle-income countries (LMIC): how can we get better? J Egypt Natl Canc Inst. Aug 14 2020;32(1):32. doi: 10.1186/s43046-020-00043-3 [DOI] [PubMed] [Google Scholar]
  • 18.Deo SVS, Kumar N, Rajendra VKJ, et al. Palliative Surgery for Advanced Cancer: Clinical Profile, Spectrum of Surgery and Outcomes from a Tertiary Care Cancer Centre in Low-Middle-Income Country. Indian J Palliat Care. Apr-Jun 2021;27(2):281–285. doi: 10.25259/IJPC_399_20 [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 19.Naveed S, Qari H, Thau CM, Burasakarn P, Mir AW, Panday BB. Lymph Node Ratio is an Important Prognostic Factor in Curatively Resected Gallbladder Carcinoma, Especially in Node-positive Patients: An Experience from Endemic Region in a Developing Country. Euroasian J Hepatogastroenterol. Jan-Jun 2021;11(1):1–5. doi: 10.5005/jp-journals-10018-1336 [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 20.Sohail S, Azmat U, Khawaja S, et al. Clinical and Histopathological Variables and Prognostic Factors of Adrenocortical Carcinoma. Cureus. Jun 2021;13(6):e15721. doi: 10.7759/cureus.15721 [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 21.Zaghloul MS, Zaghloul TM, Bishr MK, Baumann BC. Urinary schistosomiasis and the associated bladder cancer: update. J Egypt Natl Canc Inst Nov 30 2020;32(1):44. doi: 10.1186/s43046-020-00055-z [DOI] [PubMed] [Google Scholar]
  • 22.Amin AT, Ahmed BM, Khallaf SM. Safety and feasibility of laparoscopic colo-rectal surgery for cancer at a tertiary center in a developing country: Egypt as an example. J Egypt Natl Canc Inst Jun 2015;27(2):91–5. doi: 10.1016/j.jnci.2015.03.005 [DOI] [PubMed] [Google Scholar]
  • 23.Arshad A, Yousaf I. Surgical fixation of metastatic spine fractures: 6-months experience at a cancer hospital from a developing country - an audit. J Pak Med Assoc Feb 2022;72(2):292–295. doi: 10.47391/JPMA.3459 [DOI] [PubMed] [Google Scholar]
  • 24.Ayandipo OO, Adeleye AO, Ulasi IB, Ogundiran TO. Outcome of Cerebral Metastasectomy in Select Cases of Brain Metastases from Breast Cancer in Ibadan, Nigeria. World Neurosurg. Jul 2019;127:186–193. doi: 10.1016/j.wneu.2019.03.279 [DOI] [PubMed] [Google Scholar]
  • 25.Bhatt A, Prabhu R, Sethna K, Tharayil S, Kumar M. The “homemade” HIPEC machine - a cost-effective alternative in low-resource countries. Pleura Peritoneum. Dec 1 2017;2(4):163–170. doi: 10.1515/pp-2017-0022 [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 26.Deo S, Ray M, Bansal B, et al. Feasibility and outcomes of cytoreductive surgery and HIPEC for peritoneal surface malignancies in low- and middle-income countries: a single-center experience of 232 cases. World J Surg Oncol. Jun 5 2021;19(1):164. doi: 10.1186/s12957-021-02276-5 [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 27.Jamal A, Shakeel O, Mohsin J, et al. Pancreaticoduodenectomy: Outcomes of a complex surgical procedure from a developing country. Pancreatology. Oct 2020;20(7):1534–1539. doi: 10.1016/j.pan.2020.08.013 [DOI] [PubMed] [Google Scholar]
  • 28.Kaul P, Poonia DR, Kottayasamy Seenivasagam R, et al. Technical Considerations and Outcome Analysis of Using Extended Bipaddle Pectoralis Major Myocutaneous Flaps for Reconstructions of Large and Complex Oral Cavity Defects: Expanding the Horizons. Indian J Surg Oncol. Sep 2021;12(3):484–490. doi: 10.1007/s13193-021-01345-1 [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 29.Khalil MAI, Khan N, Ali A, et al. Outcomes of Nephron Sparing in a Specialist Cancer Hospital of a Developing Country. Cureus. Feb 27 2019;11(2):e4150. doi: 10.7759/cureus.4150 [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 30.Khan DA, Farooq A, Jiwani U, Ahsan MA, Shahzad F, Rahman MF. Aboard the Smile Train: Outcomes of Primary Cleft Palate Repair at a Tertiary Care Center: A bord du Smile Train : les resultats cliniques de reparations de fentes palatines dans un centre de soins tertiaires. Plast Surg (Oakv). Feb 2021;29(1):10–15. doi: 10.1177/2292550320935969 [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 31.Youssef MMG, Namour A, Youssef OZ, Morsi A. Oncologic and Cosmetic Outcomes of Oncoplastic Breast Surgery in Locally Advanced Breast Cancer After Neoadjuvant Chemotherapy, Experience from a Developing Country. Indian J Surg Oncol. Sep 2018;9(3):300–306. doi: 10.1007/s13193-017-0689-3 [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 32.Almas T, Khan MK, Murad MF, et al. Clinical and Pathological Characteristics of Soft Tissue Sarcomas: A Retrospective Study From a Developing Country. Cureus. Aug 21 2020;12(8):e9913. doi: 10.7759/cureus.9913 [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 33.Fadlalla WM, Hanafy A, Abdelhakim M, Aboulkassem H, Ashraf ES, Abdelbary A. Randomized Controlled Trial of Laparoscopic versus Open Radical Cystectomy in a Laparoscopic Naive Center. Adv Urol. 2021;2021:4731013. doi: 10.1155/2021/4731013 [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 34.Fiaz S, Ali A, Adnan S, et al. Comparison of Outcomes Between Radical Radiotherapy and Radical Cystectomy in Muscle Invasive Bladder Cancer in a Cancer Specialized Unit of a Developing Country. Cureus. Aug 26 2020;12(8):e10057. doi: 10.7759/cureus.10057 [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 35.Rizvi FH, Khan MK, Almas T, et al. Early Postoperative Outcomes of Breast Cancer Surgery in a Developing Country. Cureus. Aug 22 2020;12(8):e9941. doi: 10.7759/cureus.9941 [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 36.Deepa KV, Gadgil A, Lofgren J, Mehare S, Bhandarkar P, Roy N. Is quality of life after mastectomy comparable to that after breast conservation surgery? A 5-year follow up study from Mumbai, India. Qual Life Res. Mar 2020;29(3):683–692. doi: 10.1007/s11136-019-02351-1 [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 37.Naeem A, Shakeel O, Ashraf I, et al. Laparoscopic Curative Resection for Right-Sided Colonic Tumors: Initial Experience From a Specialized Cancer Hospital of a Developing Country. Cureus. Jul 29 2020;12(7):e9465. doi: 10.7759/cureus.9465 [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 38.Souadka A, Essangri H, Makni A, et al. Current Opinion and Practice on Peritoneal Carcinomatosis Management: The North African Perspective. Front Surg. 2022;9:798523. doi: 10.3389/fsurg.2022.798523 [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 39.Mishra V, Giri R, Hota S, Senapati U, Sahu SK. Neutrophil-to-lymphocyte ratio as a prognostic factor in oral squamous cell carcinoma - A single-institutional experience from a developing country. J Oral Maxillofac Pathol. May-Aug 2021;25(2):322–326. doi: 10.4103/0973-029X.325235 [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 40.Singh BK, Ray S, Dhawan S, Nundy S. Spectrum of presentation in primary anorectal malignant melanoma and its management. BMJ Case Rep. Oct 1 2021;14(10)doi: 10.1136/bcr-2021-245449 [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 41.Houssaini K, Majbar MA, Souadka A, et al. Liver resection safety in a developing country: Analysis of a collective learning curve. J Visc Surg. Feb 2022;159(1):5–12. doi: 10.1016/j.jviscsurg.2021.02.006 [DOI] [PubMed] [Google Scholar]
  • 42.Chargari C, Arbyn M, Leary A, et al. Increasing global accessibility to high-level treatments for cervical cancers. Gynecol Oncol. Jan 2022;164(1):231–241. doi: 10.1016/j.ygyno.2021.10.073 [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 43.Martin AN, Silverstein A, Ssebuufu R, et al. Impact of delayed care on surgical management of patients with gastric cancer in a low-resource setting. J Surg Oncol. Dec 2018;118(8):1237–1242. doi: 10.1002/jso.25286 [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 44.Tsai HY, Kuo RN, Chung KP. Quality of life of breast cancer survivors following breast-conserving therapy versus mastectomy: a multicenter study in Taiwan. Jpn J Clin Oncol. Oct 1 2017;47(10):909–918. doi: 10.1093/jjco/hyx099 [DOI] [PubMed] [Google Scholar]
  • 45.Deressa BT, Cihoric N, Tefesse E, Assefa M, Zemenfes D. Multidisciplinary Cancer Management of Colorectal Cancer in Tikur Anbessa Specialized Hospital, Ethiopia. J Glob Oncol. Oct 2019;5:1–7. doi: 10.1200/JGO.19.00014 [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 46.Murillo R, Robles C. Research Needs for Implementing Cancer Prevention and Early Detection in Developing Countries: From Scientists’ to Implementers’ Perspectives. Biomed Res Int. 2019;2019:9607803. doi: 10.1155/2019/9607803 [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 47.Rukewe A, Fatiregun A, Ademola AF, Ugheoke A. Single-shot lamina technique of paravertebral block as an adjunct to general anesthesia for modified radical mastectomy. Niger J Clin Pract. May-Jun 2015;18(3):429–31. doi: 10.4103/1119-3077.151805 [DOI] [PubMed] [Google Scholar]
  • 48.Trapani D, Murthy SS, Boniol M, et al. Distribution of the workforce involved in cancer care: a systematic review of the literature. ESMO Open. Dec 2021;6(6):100292. doi: 10.1016/j.esmoop.2021.100292 [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 49.Knight SR, Shaw CA, Pius R, Drake TM, Norman L, Ademuyiwa AO, Adisa AO, Aguilera ML, Al-Saqqa SW, Al-Slaibi I, Bhangu A Global variation in postoperative mortality and complications after cancer surgery: a multicentre, prospective cohort study in 82 countries. Lancet. Jan 30 2021;397(10272):387–397. doi: 10.1016/s0140-6736(21)00001-5 [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 50.Kamarajah SK, Nepogodiev D, Bekele A, Cecconello I, Evans RPT, Guner A, Gossage JA, Harustiak T, Hodson J, Isik A and Kidane B Mortality from esophagectomy for esophageal cancer across low, middle, and high-income countries: An international cohort study. Eur J Surg Oncol. Jun 2021;47(6):1481–1488. doi: 10.1016/j.ejso.2020.12.006 [DOI] [PubMed] [Google Scholar]
  • 51.Bishr MK, Zaghloul MS. Radiation Therapy Availability in Africa and Latin America: Two Models of Low and Middle Income Countries. Int J Radiat Oncol Biol Phys. Nov 1 2018;102(3):490–498. doi: 10.1016/j.ijrobp.2018.06.046 [DOI] [PubMed] [Google Scholar]
  • 52.Stitzenberg KB, Sigurdson ER, Egleston BL, Starkey RB, Meropol NJ. Centralization of cancer surgery: implications for patient access to optimal care. J Clin Oncol. Oct 1 2009;27(28):4671–8. doi: 10.1200/JCO.2008.20.1715 [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 53.O’Neill KM, Mandigo M, Pyda J, et al. Out-of-pocket expenses incurred by patients obtaining free breast cancer care in Haiti. Lancet. Apr 27 2015;385 Suppl 2:S48. doi: 10.1016/S0140-6736(15)60843-1 [DOI] [PubMed] [Google Scholar]
  • 54.Foerster M, Anderson BO, McKenzie F, et al. Inequities in breast cancer treatment in sub-Saharan Africa: findings from a prospective multi-country observational study. Breast Cancer Res. Aug 13 2019;21(1):93. doi: 10.1186/s13058-019-1174-4 [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 55.Udayakumar S, Solomon E, Isaranuwatchai W, et al. Cancer treatment-related financial toxicity experienced by patients in low- and middle-income countries: a scoping review. Support Care Cancer. Mar 23 2022;doi: 10.1007/s00520-022-06952-4 [DOI] [PubMed] [Google Scholar]
  • 56.Selmouni F, Amrani L, Sauvaget C, et al. Delivering colorectal cancer screening integrated with primary health care services in Morocco: Lessons learned from a demonstration project. Cancer. Mar 15 2022;128(6):1219–1229. doi: 10.1002/cncr.34061 [DOI] [PubMed] [Google Scholar]
  • 57.Horton S, Gauvreau CL. Cancer in Low- and Middle-Income Countries: An Economic Overview. In: Gelband H, Jha P, Sankaranarayanan R, Horton S, eds. Cancer: Disease Control Priorities, Third Edition (Volume 3). 2015. [Google Scholar]
  • 58.Gelband H, Sankaranarayanan R, Gauvreau CL, et al. Costs, affordability, and feasibility of an essential package of cancer control interventions in low-income and middle-income countries: key messages from Disease Control Priorities, 3rd edition. Lancet. May 21 2016;387(10033):2133–2144. doi: 10.1016/S0140-6736(15)00755-2 [DOI] [PubMed] [Google Scholar]
  • 59.Crocker AB, Zeymo A, McDermott J, et al. Expansion coverage and preferential utilization of cancer surgery among racial and ethnic minorities and low-income groups. Surgery. Sep 2019;166(3):386–391. doi: 10.1016/j.surg.2019.04.018 [DOI] [PubMed] [Google Scholar]
  • 60.Ranganathan K, Ogunleye AA, Aliu O, Agbenorku P, Momoh AO. Breast Reconstruction Practices and Barriers in West Africa: A Survey of Surgeons. Plast Reconstr Surg Glob Open. Nov 2020;8(11):e3259. doi: 10.1097/GOX.0000000000003259 [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 61.Vergara-Fernandez O, Rangel-Rios H, Trejo-Avila M, Ramos ES, Velazquez-Fernandez D. Assessment of quality-of-care indicators for colorectal cancer surgery at a single centre in a developing country. Can J Surg. Sep-Oct 2020;63(5):E468–E474. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 62.Duggan C, Dvaladze A, Rositch AF, et al. The Breast Health Global Initiative 2018 Global Summit on Improving Breast Healthcare Through Resource-Stratified Phased Implementation: Methods and overview. Cancer. May 15 2020;126 Suppl 10:2339–2352. doi: 10.1002/cncr.32891 [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 63.Malik AA, Afzal MF, Majid HJ, et al. Clinical Practice Guidelines For The Management Of Colorectal Cancer, A Consensus Statement By The Society Of Surgeons(R) And Surgical Oncology Society Of Pakistan(R). J Pak Med Assoc. Sep 2021;71(Suppl 6)(10):S1–S7. [PubMed] [Google Scholar]
  • 64.Rashad N, Abdulla M, Farouk M, et al. Resource Oriented Decision Making for Treatment of Metastatic Colorectal Cancer (mCRC) in a Lower-Middle Income Country: Egyptian Foundation of Medical Sciences (EFMS) Consensus Recommendations 2020. Cancer Manag Res. 2022;14:821–842. doi: 10.2147/CMAR.S340030 [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 65.Debas H, Alatise OI, Balch CM, et al. Academic Partnerships in Global Surgery: An Overview American Surgical Association Working Group on Academic Global Surgery. Ann Surg. Mar 2020;271(3):460–469. doi: 10.1097/SLA.0000000000003640 [DOI] [PubMed] [Google Scholar]
  • 66.Ilbawi AM, Anderson BO. Global cancer consortiums: moving from consensus to practice. Ann Surg Oncol. Mar 2015;22(3):719–27. doi: 10.1245/s10434-014-4346-6 [DOI] [PubMed] [Google Scholar]
  • 67.Kauffmann RM, Neuzil K, Koch R, Terhune KP. Global Surgery Electives: A Strategy to Improve Care to Domestic Underserved Populations? J Surg Res. Nov 2020;255:247–254. doi: 10.1016/j.jss.2020.05.065 [DOI] [PubMed] [Google Scholar]
  • 68.Ranganathan P, Chinnaswamy G, Sengar M, et al. The International Collaboration for Research methods Development in Oncology (CReDO) workshops: shaping the future of global oncology research. Lancet Oncol. Aug 2021;22(8):e369–e376. doi: 10.1016/S1470-2045(21)00077-2 [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 69.De Oliveira A, Fresta M. Impact of International Training of Medical Specialists for underdeveloped Countries: Brazil-Angola experience. J Adv Med Educ Prof. Jan 2020;8(1):50–52. doi: 10.30476/jamp.2019.81744.1030 [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 70.Hornstein P, Tuyishime H, Mutebi M, Lasebikan N, Rubagumya F, Fadelu T. Authorship Equity and Gender Representation in Global Oncology Publications. JCO Glob Oncol. Jan 2022;8:e2100369. doi: 10.1200/GO.21.00369 [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 71.Akhtar N, Rajan S, Chakrabarti D, et al. Continuing cancer surgery through the first six months of the COVID-19 pandemic at an academic university hospital in India: A lower-middle-income country experience. J Surg Oncol. Apr 2021;123(5):1177–1187. doi: 10.1002/jso.26419 [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 72.Elghazawy H, Bakkach J, Zaghloul MS, et al. Implementation of breast cancer continuum of care in low- and middle-income countries during the COVID-19 pandemic. Future Oncol. Nov 2020;16(31):2551–2567. doi: 10.2217/fon-2020-0574 [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 73.Vohra LM, Jabeen D, Khan N, Nizar A, Jamil A, Siddiqui T. Analysing the trends in breast surgery practice during COVID-19 pandemic: A comparative study with the Pre-COVID era. Ann Med Surg (Lond). Feb 2022;74:103342. doi: 10.1016/j.amsu.2022.103342 [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 74.Erasmus E, Orgill M, Schneider H, Gilson L. Mapping the existing body of health policy implementation research in lower income settings: what is covered and what are the gaps? Health Policy Plan. Dec 2014;29 Suppl 3:iii35–50. doi: 10.1093/heapol/czu063 [DOI] [PubMed] [Google Scholar]
  • 75.Mehta A, Jyi CN, Wireko AA, et al. Embracing robotic surgery in low- and middle-income countries: Potential benefits, challenges, and scope in the future. Annals of Medicine and Surgery. 2022;84:104803. doi: 10.1016/j.amsu.2022.104803 [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 76.Ahmed M, Solbiati L, Brace CL, et al. Image-guided tumor ablation: standardization of terminology and reporting criteria--a 10-year update. Radiology. Oct 2014;273(1):241–60. doi: 10.1148/radiol.14132958 [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 77.Baker RR, Payne C, Yu Y, et al. Image-Guided Magnetic Thermoseed Navigation and Tumor Ablation Using a Magnetic Resonance Imaging System. Adv Sci (Weinh). Apr 2022;9(12):e2105333. doi: 10.1002/advs.202105333 [DOI] [PMC free article] [PubMed] [Google Scholar]

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