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Lung Cancer in Sudan

      Introduction

      Sudan, with an area of 1,886,068 km2, is the third-largest country in Africa. This African Arab country is surrounded by North Africa, Sub-Saharan Africa, and the Middle East. In 2020, the population of Sudan was about 43.8 million.
      United Nations
      World population prospects 2019.
      The population structure is young, with approximately 40% under 15 years of age, as illustrated in Figure 1. Sudan is a low-income country despite its abundant natural resources, with approximately half of the population living below the poverty line. In 2011, with the independence of South Sudan under the term of Comprehensive Peace Agreement,
      • Sudan C.R.
      The Failure and Division of an African State.
      Sudan lost almost half of its revenue, as South Sudan took with it approximately 75% of all oil production and reserves.
      • Pedersen A.
      • Bazilian M.
      Considering the impact of oil politics on nation building in the Republic of South Sudan.
      Consequently, the annual growth rate of gross domestic products decreased from 7.8% in 2008 to 4.0% in 2015 and is further declining, reaching –1.6% in 2020.
      The World Bank
      GDP Growth (annual %) - Sudan.
      Figure thumbnail gr1
      Figure 1Sudan population pyramid (2020). Adapted from the United Nations Department of Economic and Social Affairs, Population Division. World Population Prospects. 2019 revision.
      Health services in Sudan are provided by the government, nonprofit organizations, and the private sector. This system is managed by the federal ministry of health and the states ministries of health. The public health care services are organized at three levels: primary, secondary, and tertiary. The health care system is understaffed and there is a lack of resources. However, the public health system provides subsidized medical care. Moreover, there is a national policy to provide, free of charge, health care services at public health care facilities to the following: (1) patients presenting in emergency states; (2) children under 5 years of age; (3) pregnant women; (4) patients with cancer; and (5) patients with renal failure, including dialysis and renal transplant; and also medicines for malaria, tuberculosis, and human immunodeficiency virus. The National Insurance Fund, launched in 1995, has a good contribution; but the services it is covering are somewhat limited.
      • Wharton G.
      • Ali O.E.
      • Khalil S.
      • Yagoub H.
      • Mossialos E.
      Rebuilding Sudan’s health system: opportunities and challenges.
      In addition, charity organizations, such as the Sudanese Zakat Chamber (a form of Islamic charity) and other charitable nongovernmental organizations, assist patients with limited personal finances with other costs that may not be covered by the government. It is worthwhile to mention that these strained services are further starched by a huge number of refugees and jobseekers from neighboring countries.
      Similar to many low- and middle-income countries, Sudan faces an increasing burden of chronic noncommunicable diseases, including cancer.
      • Charani E.
      • Cunnington A.J.
      • Yousif A.H.
      • et al.
      In transition: current health challenges and priorities in Sudan.
      ,
      The International Agency for Research on Cancer
      Sudan fact sheets.
      In Sudan, as in most Sub-Saharan African countries, cancer is recognized as a serious health problem; however, the public health care system has other issues to deal with such as the excessive burden of communicable diseases, mother and child health, and malnutrition.
      • Charani E.
      • Cunnington A.J.
      • Yousif A.H.
      • et al.
      In transition: current health challenges and priorities in Sudan.
      Cancer treatment in Sudan is mainly provided by the Khartoum Oncology Hospital in Khartoum State and the National Cancer Institute (NCI) in the Gezira state. The Khartoum Oncology Hospital (formerly Radiation and Isotope Center in Khartoum), the first cancer center in the country, opened at the beginning of the 1960s, which, at the time, was only the second of its kind in Africa.
      • Christ S.M.
      • Siddig S.
      • Elbashir F.
      • et al.
      Radiation Oncology in the Land of the Pyramids: How Sudan Continues to Push the Frontiers of Cancer Care in Eastern Africa.
      In the 1990s, the NCI was established in Wad Madani city, the capital of the Gezira state.
      • Christ S.M.
      • Siddig S.
      • Elbashir F.
      • et al.
      Radiation Oncology in the Land of the Pyramids: How Sudan Continues to Push the Frontiers of Cancer Care in Eastern Africa.
      Lately, the government established eight chemotherapy units attached to eight state hospitals (Fig. 2). There are also private chemotherapy clinics, all of which are in the capital Khartoum, that cater to out-of-pocket payers and those with private insurance coverage.
      Figure thumbnail gr2
      Figure 2Geographic distribution of cancer treatment centers in Sudan. Blue dots represent cancer treatment centers (chemotherapy and radiotherapy). Gray dots represent chemotherapy unit services. The map of Sudan was reprinted from https://franck.com/sudan/geography/ (site accessed on November 20, 2021).
      Cancer is becoming a major health problem in the developing world and the number of cancer cases in Sub-Saharan Africa is rising. Being an African country, Sudan has its share of the cancer burden. Yet, the real data on cancer incidence, prevalence, and mortality in Sudan is unknown and hard to obtain because of the lack of a national population-based cancer registry. According to the Global Cancer Incidence, Mortality, and Prevalence 2020 estimates, breast and prostate are the most common type of cancer in Sudanese men and women, respectively.
      • Sung H.
      • Ferlay J.
      • Siegel R.L.
      • et al.
      Global cancer Statistics 2020: GLOBOCAN estimates of incidence and mortality worldwide for 36 cancers in 185 countries.
      The incidence rate of lung cancer (the second most prevalent cancer globally) in Africa is low.
      • Sung H.
      • Ferlay J.
      • Siegel R.L.
      • et al.
      Global cancer Statistics 2020: GLOBOCAN estimates of incidence and mortality worldwide for 36 cancers in 185 countries.
      Information about epidemiology, management, and survival of lung cancer are lacking in Sudan. In this article, we provide an up-to-date situational analysis of lung cancer in Sudan as an example of an African limited-resource setting.

      Epidemiology

      Globally, lung cancer is the leading cause of cancer death and the second most typically diagnosed cancer in 2020. The age-standardized incidence rates of lung cancer among men and women are 31.5 per 100,000 population and 14.6 per 100,000 population, respectively.
      • Sung H.
      • Ferlay J.
      • Siegel R.L.
      • et al.
      Global cancer Statistics 2020: GLOBOCAN estimates of incidence and mortality worldwide for 36 cancers in 185 countries.
      Most lung cancer cases occur in low- and middle-income countries. In Africa, the low incidence of lung cancer has been attributed to the low prevalence of smoking and the lower life expectancy of the population.
      • Barta J.A.
      • Powell C.A.
      • Wisnivesky J.P.
      Global epidemiology of lung cancer.
      The reported numbers for lung cancer also underestimate the true numbers.
      • Becher H.
      • Winkler V.
      Lung cancer mortality in Sub-Saharan Africa.
      In addition, there is a huge variation among different countries in Africa, as illustrated in Table 1. Lung cancer incidence rates are higher in Southern and Northern African regions than in other regions. In the Arab league countries, Sudan has the lowest age-standardized incidence rate of lung cancer for men.
      • Salim E.I.
      • Jazieh A.R.
      • Moore M.A.
      Lung cancer incidence in the Arab League countries: risk factors and control.
      These regional differences are mainly linked to cigarette smoking patterns. It is estimated that less than 10% of adult men in Sudan are smokers,
      American Cancer Society
      The tobacco atlas.
      which is lower when compared with South Africa (26.5%) and countries from North Africa such as Egypt (46.4%) and Tunisia (48.4%).
      • Jazieh A.R.
      • Algwaiz G.
      • Errihani H.
      • et al.
      Lung cancer in the Middle East and North Africa region.
      ,
      • Van Eeden R.
      • Tunmer M.
      • Geldenhuys A.
      • Nayler S.
      • Rapoport B.L.
      Lung cancer in South Africa.
      A previous survey conducted in Sudan found that cigarette smoking prevalence among men (12%) was significantly higher than women (0.9%).
      • Idris A.M.
      • Ibrahim Y.E.
      • Warnakulasuriya K.A.
      • Cooper D.J.
      • Johnson N.W.
      • Nilsen R.
      Toombak use and cigarette smoking in the Sudan: estimates of prevalence in the Nile State.
      Furthermore, the same study found that the prevalence of smokeless tobacco (dipped in the mouth and known as Toombak in Sudan) consumption is far higher than cigarette smoking, and is particularly common in rural areas.
      • Idris A.M.
      • Ibrahim Y.E.
      • Warnakulasuriya K.A.
      • Cooper D.J.
      • Johnson N.W.
      • Nilsen R.
      Toombak use and cigarette smoking in the Sudan: estimates of prevalence in the Nile State.
      It is worthwhile to mention that Toombak is very cheap compared with cigarettes. Despite the fact that control of tobacco smoking is the most important preventive measure for many types of malignant disorders including lung cancer, Sudan has neither a national tobacco control strategy nor national tobacco cessation clinical guidelines.
      World Health Organization
      WHO report on the global tobacco epidemic 2019: offer help to quit tobacco use.
      Table 1Age-Standardized Incidence Rate of Lung Cancer by African Region
      African RegionAge-Standardized Incidence Rate Per 100,000
      MenWomen
      Southern Africa27.59.3
      Northern Africa19.53.5
      Eastern Africa4.23.0
      Middle Africa3.41.8
      Western Africa2.81.8
      GOBOCAN, Global Cancer Incidence, Mortality and Prevalence.
      Data adapted from Global Cancer Statistics 2020: GLOBOCAN.
      • Sung H.
      • Ferlay J.
      • Siegel R.L.
      • et al.
      Global cancer Statistics 2020: GLOBOCAN estimates of incidence and mortality worldwide for 36 cancers in 185 countries.
      Sudan does not have a national population-based cancer registry. The relative frequency of lung cancer in the reported case series of adult Sudanese patients with cancer was approximately 1%.
      • Awadelkarim K.D.
      • Mariani-Costantini R.
      • Elwali N.E.
      Cancer in the Sudan: an overview of the current status of knowledge on tumor patterns and risk factors.
      Lung cancer was not even in the top 10 cancer sites for all registered cancer cases in Khartoum state between 2009 and 2010.
      • Saeed I.E.
      • Weng H.Y.
      • Mohamed K.H.
      • Mohammed S.I.
      Cancer incidence in Khartoum, Sudan: first results from the Cancer Registry, 2009-2010.
      The estimated age-standardized rate of lung cancer in Khartoum-Sudan in men and women were 3.6 per 100,000 population and 2.8 per 100,000 population, respectively.
      • Saeed I.E.
      • Weng H.Y.
      • Mohamed K.H.
      • Mohammed S.I.
      Cancer incidence in Khartoum, Sudan: first results from the Cancer Registry, 2009-2010.

      Clinicopathologic Features

      There is a paucity of information on clinical and pathologic features of lung cancer in Sudan. Data from Central Sudan found that the majority of patients with lung cancer treated at the NCI never smoked tobacco (Table 2) and more than two-thirds were men (Table 3), with a male-to-female ratio of 2.5. The male-to-female ratio varies widely across regions, ranging from 1.2 in Northern America to 5.6 in Northern Africa.
      • Sung H.
      • Ferlay J.
      • Siegel R.L.
      • et al.
      Global cancer Statistics 2020: GLOBOCAN estimates of incidence and mortality worldwide for 36 cancers in 185 countries.
      This sex difference in the incidence of lung cancer in Sudan can be attributed to differences in tobacco smoking rates. Intersetingly the smokig pattern among patients with lung cancer treated at NCI differ markedly by sex. Most Sudanese women (90%) with lung cancer have never smoked tobacco (Table 2). Overall, we found a prevalence of 63% never-smokers among patients newly diagnosed with Lung cancer at NCI (Table 2). This finding is higher than the reported rate that ranges from 10% to 30% in Europe or North America.
      • Dias M.
      • Linhas R.
      • Campainha S.
      • Conde S.
      • Barroso A.
      Lung cancer in never-smokers - what are the differences?.
      ,
      • Bryant A.
      • Cerfolio R.J.
      Differences in epidemiology, histology, and survival between cigarette smokers and never-smokers who develop non-small cell lung cancer.
      It is worth mentioning that the very high prevalence of nonsmoking women with lung cancer in our setting (Table 2) highlights the existence of distinctive biological aspects in women, such as reproductive hormones that may interact with other identified factors for lung cancer including genetic factors, cooking and heating fumes, or exposure to ionizing radiation.
      • Couraud S.
      • Zalcman G.
      • Milleron B.
      • Morin F.
      • Souquet P.J.
      Lung cancer in never smokers--a review.
      Table 2Smoking Prevalence Among Patients With Lung Cancer Treated at the NCI, Sudan Between 2015 and 2019
      SexNever smokerSmokerTotal
      No. (%)No. (%)No. (%)
      Male51 (52)47 (48)98 (100)
      Female36 (90)4 (10)40 (100)
      Total87 (63)51 (37)138 (100)
      NCI, National Cancer Institute.
      Table 3Characteristics of Patients With Lung Cancer (n = 138) Treated at the NCI, Sudan Between 2015 and 2019
      CategorySubcategoryNo. (%)
      Sex
      Male98 (71)
      Female40 (29)
      Median age (range), yAll population61 (31–86)
      Mean age (95% CI), y
      Men61 (58–63)
      Women64 (60–69)
      All population62 (59–64)
      Presenting symptoms
      Some patients may present with more than one symptoms (the total number of presenting symptoms was 212).
      Cough86 (41)
      Shortness of breath57 (27)
      Chest pain31 (15)
      Hemoptysis20 (9)
      Other18 (8)
      Mode of diagnosis
      Sputum sample12 (9)
      Thoracentesis38 (28)
      CT-guided biopsy52 (38)
      Bronchoscopy21 (15)
      Peripheral lymph node biopsy8 (6)
      Not documented7 (5)
      Histopathology
      NSCLC123 (89)
      SCLC15 (11)
      Stage
      I or II11 (8)
      III37 (27)
      IV90 (65)
      CI, confidence interval; CT, computed tomography; NCI, National Cancer Institute.
      Data adapted from NCI Cancer Registry.
      a Some patients may present with more than one symptoms (the total number of presenting symptoms was 212).
      In Central Sudan, the median age at diagnosis for lung cancer was 61 years old (Table 3), approximately a decade younger than the median age seen in high-income countries.
      • Torre L.A.
      • Siegel R.L.
      • Jemal A.
      Lung cancer statistics.
      This is may be partially related to the fact that Sudan, similar to other African countries, has a young population structure (Fig. 1), in addition to a short life expectancy, as the risk of lung cancer increases with age.
      The clinical stage is the most important factor for the outcome of patients with lung cancer. In Sudan, similar to other limited-resource countries, patients with lung cancer usually present in advanced stages.
      • Lubuzo B.
      • Ginindza T.
      • Hlongwana K.
      The barriers to initiating lung cancer care in low-and middle-income countries.
      Most (93%) patients with lung cancer treated at the NCI presented with stage III or IV disease (Table 3). Bone was the most common site of metastasis followed by pleura (Fig. 3). In Sudan, patients in remote rural areas have limited access to cancer care facilities, as cancer treatment centers are limited in number and resources (Fig. 2). Many patients have to travel long distances to seek cancer care, which is a great financial burden to patients and families. Furthermore, these patients suffer from poor referral systems with low levels of awareness leading to suboptimal lung cancer management. A delay in initiating lung cancer treatment is not always the responsibility of the patient; sometimes patients contact the health services early, but physicians do not suspect lung cancer on the basis of presenting symptoms. It is a common practice that patients with long-standing respiratory symptoms or pulmonary nodular mass on chest x-ray are referred to tuberculosis clinics for further assessment. In this regard, studies to assess the time required to diagnose lung cancer and factors that contribute to diagnostic delays in our limited-resource setting are needed.
      Figure thumbnail gr3
      Figure 3Distribution of patients with stage IV lung cancer (n = 90) treated at the NCI, Sudan between 2015 and 2019 according to sites of metastases (data from NCI Cancer Registry). NCI, National Cancer Institute.

      Screening

      In Sudan, the health care system is markedly weakened by limited financial resources in addition to the shortage of trained health care professionals. In our limited-resource setting, there is a limited number of low-dose computed tomography (CT) scans that proved to reduce lung cancer mortality among the high-risk populations.
      National Lung Screening Trial Research Team
      Lung cancer incidence and mortality with extended follow-up in the National Lung Screening Trial.
      ,
      • Pastorino U.
      • Silva M.
      • Sestini S.
      • et al.
      Prolonged lung cancer screening reduced 10-year mortality in the MILD trial: new confirmation of lung cancer screening efficacy.
      Moreover, the prevalence of lung cancer in our population is very low.
      • Awadelkarim K.D.
      • Mariani-Costantini R.
      • Elwali N.E.
      Cancer in the Sudan: an overview of the current status of knowledge on tumor patterns and risk factors.
      ,
      • Saeed I.E.
      • Weng H.Y.
      • Mohamed K.H.
      • Mohammed S.I.
      Cancer incidence in Khartoum, Sudan: first results from the Cancer Registry, 2009-2010.
      Thus, screening recommendations for lung cancer are less likely to be successful or cost-effective if adopted.

      Diagnosis

      Pathology

      Tissue diagnosis is usually obtained by pulmonary physicians, interventional radiologists, or thoracic surgeons. Methods of obtaining an initial biopsy depend on the availability of expertise, resources, and tumor location. More invasive diagnostic tools such as flexible bronchoscopy and CT-guided biopsies are available only in Khartoum. Therefore, lung cancer is often diagnosed on the basis of pleural fluid cytology (with its limitations) when patients develop pleural effusion. In addition, pathologists, from time to time, receive sputum specimens, a simple test usually done in three consecutive days, from lung cancer–suspected cases. Sputum cytology, if positive, can provide an accurate diagnosis of central lung cancers. The quality of the specimen is usually poor and saliva is diluted with large amounts of mucin, sometimes masking cellular details. Central lesions are also more likely to yield positive cytologic results than peripheral lesions.
      • Neumann T.
      • Meyer M.
      • Patten F.W.
      • et al.
      Premalignant and malignant cells in sputum from lung cancer patients.
      Few cases of aspergilloma are seen from time to time and sometimes are misdiagnosed as lung cancer. In some cases, it would be challenging for the pathologist to distinguish SCLC from NSCLC on a cytology sample. In expert hands, fine-needle aspiration cytology allows typing of NSCLC with high accuracy and can be regarded as an acceptable diagnostic method in most NSCLC cases, especially when more invasive approaches are not feasible.
      • Nizzoli R.
      • Tiseo M.
      • Gelsomino F.
      • et al.
      Accuracy of fine needle aspiration cytology in the pathological typing of non-small cell lung cancer.
      Data from Central Sudan reveal that the diagnosis of 37% of all patients with lung cancer registered at NCI between 2015 and 2019 was based on cytology (Table 3).
      Studies assessing the pathologic characteristics of lung cancer in Sudan are lacking. Data from NCI found that NSCLC represents 89%, whereas SCLC accounted for 11% of cases. NSCLC cases were further classified according to the WHO criteria: adenocarcinoma, squamous cell carcinoma, and large cell carcinoma (Fig. 4). NSCLCs were reported in 25% of cases as NSCLC–not otherwise specified, particularly on cytology or small biopsy samples.
      Figure thumbnail gr4
      Figure 4Distribution of lung cancer–typing diagnosis among patients (n = 138) treated at the NCI, Sudan between 2015 and 2019 (data from NCI Cancer Registry). ADC, adenocarcinoma; LCC, large cell carcinoma; NCI, National Cancer Institute; NSCLC-NOS, NSCLC–not otherwise specified; SQC, squamous cell carcinoma.
      Pathology practice in Sudan lacked funding, making it difficult for practicing pathologists to have access to immunohistochemistry staining of the tumors to identify lung cancer subtypes. Therefore, histopathologists depend largely on routine hematoxylin-eosin stains (with its limitations) to reach a diagnosis. Molecular studies, including testing for EGFR, ALK, and programmed death-ligand 1 (PD-L1) are not yet available in Sudan.

      Diagnostic Imaging

      In Sudan, diagnostic imaging modalities, such as chest and skeletal radiography and abdominal ultrasound, are available in most tertiary hospitals. CT scans and magnetic resonance imaging are available in some regions of the country with an increasing number of referrals for diagnosis and staging. However, most of these imaging modalities are owned by the private sector. Radioisotope bone scans are only available in Khartoum state and Gezira state. Diagnostic facilities that provide bronchoscopes and CT-guided biopsy services are lacking outside Khartoum. Positron emission tomography CT is not available in Sudan. Data from NCI (Table 3) reveal that CT-guided biopsies are the investigations of choice to obtain tissue for diagnosis in 38% of the cases with lung cancer. Although cancer treatments are free of charge, the financial aspects of investigations represent a huge burden for patients with very limited financial support.

      Management

      The management of patients with lung cancer requires a multidisciplinary approach to treatment. However, in our limited-resource setting, the number of specialists involved in the management of lung cancer is limited and tend to work in isolation in areas where they exist. Furthermore, the necessary medical equipments for lung cancer diagnosis and treatment is deficient. In the face of these challenges (among many others such as the lack of national guidelines for lung cancer management), the National Comprehensive Cancer Network Clinical Practice Guidelines in Oncology has developed regional treatment practice guidelines that provide adapted treatment strategies for lung cancer in the Middle East and North Africa region and Sub-Saharan Africa.
      National Comprehensive Cancer Network
      NCCN harmonized Guidelines™ for sub-Saharan Africa.
      ,
      • Jazieh A.R.
      • Bamefleh H.
      • Demirkazik A.
      • et al.
      Modification and implementation of NCCN guideline on non–small cell lung cancer in the Middle East and North Africa region.
      These guidelines provide detailed evidence-based recommendations with the available resources while working to improve services and supportive care. In Sudan, the predominance of late stages of lung cancer at presentation reflects the palliative pattern of treatment.

      Surgical Approaches

      In Sudan, there is a lack of trained thoracic surgeons who are managing lung cancer and also a paucity of centers performing thoracic surgeries—all of which are in Khartoum. Moreover, most patients with lung cancer present with locally advanced or metastatic stages. Therefore, curative surgical intervention is rare. Data regarding the type and outcome of lung cancer surgery in Sudan are lacking.

      Radiation Approaches

      Radiotherapy (RT) is an essential part of the treatment of lung cancer. In resource-limited settings such as Sudan, the need for RT is much greater owing to the late presentation and inoperability of tumors. Moreover, RT plays an important role in disease palliation in the thorax and distant metastatic sites such as the brain, bone, and other regions. In Sudan, RT planning relies on the two-dimension technique (with its limitation) using fluoroscopy—that is, RT is delivered in the form of square or rectangular fields, with modification of the beam by using blocks. The patient setup for RT treatment is on the basis of marks placed on the skin matching the bony structures.
      As a result of the limited number of RT machines as presented in Figure 2 and Table 4, access to RT treatment for most patients is severely limited. Moreover, RT units are located in Central Sudan at the Khartoum Oncology Hospital in Khartoum and the NCI in Wad Madani. Therefore, patients from different regions of Sudan are referred to these centers for RT. In this regard, the cost of travel and accommodation represents a huge burden for the patients and their caregivers. Moreover, a long waiting time is required to start RT because of the large volume of patients with cancer referred to the only two RT centers for treatment.
      Table 4Number of Radiation Therapy Centers as Presented in Figure 2 and Radiation Therapy Machines
      Radiotherapy CenterYear of EstablishmentCityRadiotherapy Machines
      Cobalt 60LINAC
      Khartoum Oncology Hospital1968Khartoum32
      Currently not functioning.
      National Cancer Institute1999Wad Madani21
      Currently not functioning.
      LINAC, linear accelerator.
      a Currently not functioning.

      Systemic Therapy

      Chemotherapy

      Chemotherapy and supportive medications are available at no cost to Sudanese citizens at public cancer centers. Chemotherapy agents currently available to patients with lung cancer are listed in Table 5. In Sudan, lung cancer systemic treatment is provided by clinical oncologists or medical oncologists. Chemotherapy is dispensed by a pharmacist and administered by trained nurses under the supervision of an oncology registrar and a consultant oncologist. Platinum-based doublet is the mainstay of treatment for most patients. Paclitaxel-carboplatin or gemcitabine-platinum combinations are preferred regimens for patients with advanced NSCLC. Platinum-etoposide combination is the mainstay of systemic treatment in SCLC
      Table 5Systemic Therapy Available in Sudan for Patients With Lung Cancer
      ChemotherapyAvailabilityWho Pays for Chemotherapy
      Cisplatinroutinely available in the essential listavailable without cost to Sudanese citizens at public cancer centers
      Carboplatinroutinely available in the essential list
      Docetaxelroutinely available in the essential list
      Paclitaxelroutinely available in the essential list
      Etoposideroutinely available in the essential list
      Vinorelbineroutinely available in the essential list
      Gemcitabineroutinely available in the essential list
      Irinotecanoccasionally available not in the essential listPatients pay
      Pemetrexedoccasionally available not in the essential listPatients pay

      Access to Molecular Testing and Innovative Treatments

      In recent decades, important progress has been made in the landscape of the management of lung cancer from chemotherapy through targeted therapies to immuno-oncology agents; and now, molecular testing is a crucial part of the clinical decision process.
      • Planchard D.
      • Popat S.
      • Kerr K.
      • et al.
      Metastatic non-small cell lung cancer: ESMO Clinical Practice Guidelines for diagnosis, treatment and follow-up.
      These significant advancements have changed the approach to treating patients with lung cancer and improved the survival outcome, with better quality of life. The basis for this paradigm shift in the management of lung cancer is the understanding of the biology of this disease.

      Kinase Inhibitors Targeting Molecular Aberrations

      In the era of personalized medicine, the availability of molecular testing is becoming a crucial part of the clinical decision process. Access to targeted therapies depends on the accurate identification of patients’ biomarkers through molecular testing. Nevertheless, access to those high-cost molecular tests is lacking in Sudan because of limited economic resources.
      In Sudan, as with many other countries with limited resources, the health care system has not prepared for affording the high cost of kinase inhibitors targeting BRAF, EGFR, ALK, ROS1, MET, RET, NTRK, and KRAS. At the current price, these novel agents are not cost-effective in our limited-resource settings. The International Association for the Study of Lung Cancer's global survey on molecular testing in lung cancer found that usage of molecular testing in the diagnosis of lung cancer is relatively low across the world (<50% of patients are tested).
      • Smeltzer M.P.
      • Wynes M.W.
      • Lantuejoul S.
      • et al.
      The International Association for the Study of Lung Cancer global survey on molecular testing in lung cancer.
      The barriers identified included cost, access, turnaround time, quality, and lack of awareness. Therefore, there is an urgent need to develop innovative ways to try to establish more affordable pricing and increase access to these agents in countries with limited resources.

      Immune Checkpoint Inhibitors

      Immune checkpoint inhibitors, programmed cell death protein 1/PD-L1, and CTLA-4 have altered the treatment paradigm for metastatic lung cancer. Unfortunately, these immunotherapy agents are not available in Sudan because of barriers related to high costs. Therefore, the issue of PD-L1 testing becomes a moot point.

      Palliative Care Services

      Almost all patients with lung cancer presented to cancer treatment centers with advanced stages that are only suitable for palliative care. In our limited-resource setting, limited palliative care service is available at the main oncology centers.
      • Gafer N.
      • Elhaj A.
      Palliative care for cancer patients in Sudan: an overview.
      Moreover, referral to palliative care services occurs late in the disease trajectory. Hospice palliative care services, the cost-effective options that could reduce the symptoms of these patients, are not available in Sudan. However, the palliative care staff at Khartoum Oncology Hospital and the NCI volunteered to conduct home-care visits to a small number of patients because of limited resources.
      • Gafer N.
      • Elhaj A.
      Palliative care for cancer patients in Sudan: an overview.
      Although palliative care medications such as analgesics are dispensed free of charge to patients with cancer at cancer treatment centers, the cost of travel from remote areas represents a huge burden for the patients.
      • Elhassan M.M.
      • Taha S.I.
      • Maatoug M.M.
      Unplanned attendances of cancer patients to an outpatient unit in a low-income country: a prospective study from Sudan.
      In Sudan, there is an urgent need to expand and improve palliative care services to cover all those in need. In this regard, international palliative care organizations are invited to provide support for the development and strengthening of local skills.

      Survival

      Despite recent advances in the management of lung cancer, the disease remains the leading cause of cancer death in 2020.
      • Sung H.
      • Ferlay J.
      • Siegel R.L.
      • et al.
      Global cancer Statistics 2020: GLOBOCAN estimates of incidence and mortality worldwide for 36 cancers in 185 countries.
      The lack of a population-based cancer registry in Sudan represents a major challenge to obtaining accurate data about cancer survival. According to the WHO data published in 2018, lung cancer deaths in Sudan reached 401 or 0.16% of the total deaths.
      World Life Expectancy
      World health ranking: Sudan lung cancer.
      To our knowledge, there is no previous study that estimated the survival of lung cancer in Sudan. Data from NCI in Central Sudan found that the median survival of Sudanese patients with lung cancer treated at the NCI (Fig. 5) was 7.23 months (95% confidence interval: 5.18–9.28). This survival data should be interpreted with caution because it is estimated from single-institution case series—settings that cannot be generalized to the whole country. However, because the NCI is the main cancer referral center in Central Sudan and is one of the only two cancer treatment centers that provide RT treatment in Sudan, our findings could give an insight into lung cancer survival in our limited-resource setting. This poor survival outcome could be owing to limited access to proper therapy and advanced stages at presentation.
      Figure thumbnail gr5
      Figure 5Overall survival of patients with lung cancer (n = 126) treated at the NCI, Sudan between 2015 and 2019 (data from NCI Cancer Registry). The total number of patients with lung cancer treated between 2015 and 2019 was 138 patients; 12 patients were excluded from survival analysis because of missing survival data. NCI, National Cancer Institute.
      In conclusion, information on lung cancer in Sudan is lacking. Thus, there is a great need to implement research projects to determine the prevalence of smoking among the Sudanese population, and also the epidemiology, pathology, and treatment outcome of lung cancer in Sudan. In this regard, research institutions from developed countries and regional and international academic organizations are being called to assist in the development and strengthening of local facilities and skills. The outcome of such research projects would increase awareness among policy makers and the public.
      Available data reveal that lung cancer incidence is low, similar to other countries in Eastern, Western, and Central African regions. Most patients with lung cancer present late with advanced stages that are rarely amenable to curative treatment. In our limited-resource setting, patients with lung cancer are challenged by poor economic circumstances and limited access to proper diagnostic and therapeutic options.

      CRediT Authorship Contribution Statement

      Moawia Mohammed Ali Elhassan, Ahmed Abdalla Mohamedani, Sahar Abdelrahman Hamid Mohamed, Anas Osman Ahmed Hamdoun, Dafalla Omer Abuidris, Alsideeg Mohammed Alamin Mohammed, Khalid Dafaallah Awadelkarim: Conceptualization, Design, Data – acquisition, analysis, and interpretation.
      Moawia Mohammed Ali Elhassan: Writing – original draft.
      Ahmed Abdalla Mohamedani, Sahar Abdelrahman Hamid Mohamed, Anas Osman Ahmed Hamdoun, Dafalla Omer Abuidris, Alsideeg Mohammed Alamin Mohammed, Khalid Dafaallah Awadelkarim: Draft revision.

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