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Figure 1. Ratios of cancer mortality to incidence stratified by a country's wealth demonstrate the clear disparity in outcomes related to income (calculated from International Agency for Research on Cancer data). Reprinted from Farmer P, Frenk J, Knaul FM, et al. Expansion of cancer care and control in countries of low and middle income: a call to action. Lancet. 2010;376(9747):1186-1193. With permission from Elsevier.

Figure 1. Ratios of cancer mortality to incidence stratified by a country's wealth demonstrate the clear disparity in outcomes related to income (calculated from International Agency for Research on Cancer data).3 Reprinted from Farmer P, Frenk J, Knaul FM, et al. Expansion of cancer care and control in countries of low and middle income: a call to action. Lancet. 2010;376(9747):1186-1193. With permission from Elsevier.

Figure 2. Number of cases by patient sex seen at Kamuzu Central Hospital.

Figure 2. Number of cases by patient sex seen at Kamuzu Central Hospital.

Figure 3. Proportion of patients treated at Kamuzu Central Hospital compared with proportional incidence from the Surveillance Epidemiology and End Results (SEER) database (2006) for each cancer type by age.

Figure 3. Proportion of patients treated at Kamuzu Central Hospital compared with proportional incidence from the Surveillance Epidemiology and End Results (SEER) database (2006) for each cancer type by age.

Figure 4. Comparison of proportion of cancer types seen in Malawi with that reported by the International Agency for Research on Cancer (GLOBOCAN) for less developed countries in 2008. Upper gastrointestinal (GI) cancer refers to both esophageal and gastric cancers. Cervical cancer cases were not included in the Malawi analysis. Skin cancer and head and neck cancer were not included in the GLOBOCAN data.

Figure 4. Comparison of proportion of cancer types seen in Malawi with that reported by the International Agency for Research on Cancer (GLOBOCAN) for less developed countries in 2008. Upper gastrointestinal (GI) cancer refers to both esophageal and gastric cancers. Cervical cancer cases were not included in the Malawi analysis. Skin cancer and head and neck cancer were not included in the GLOBOCAN data.

Table 1. Demographic Characteristics by Tumor Type of 255 Patients Treated at Kamuzu Central Hospital
Table 1. Demographic Characteristics by Tumor Type of 255 Patients Treated at Kamuzu Central Hospital
Table 2. Operations Performed at Kamuzu Central Hospital for Each Cancer Type
Table 2. Operations Performed at Kamuzu Central Hospital for Each Cancer Type
1.
Ferlay JSH, Bray F, Forman D, Mathers CD, Parkin D. GLOBOCAN 2008, Cancer Incidence and Mortality Worldwide: IARC CancerBase No. 10. Lyon, France: International Agency for Research on Cancer; 2010
2.
Kachroo S, Etzel CJ. Decreasing the cancer burden in developing countries: concerns and recommendations.  Eur J Cancer Care (Engl). 2009;18(1):18-21PubMedArticle
3.
Farmer P, Frenk J, Knaul FM,  et al.  Expansion of cancer care and control in countries of low and middle income: a call to action.  Lancet. 2010;376(9747):1186-1193PubMedArticle
4.
World Health Organization.  National Cancer Control Programmes, policies and managerial guidelines. 2002. http://www.who.int/cancer/media/en/409.pdf. Accessed November 11, 2011
5.
Narayan KM, Ali MK, del Rio C, Koplan JP, Curran J. Global noncommunicable diseases: lessons from the HIV-AIDS experience.  N Engl J Med. 2011;365(10):876-878PubMedArticle
6.
Council on Foreign Relations.  Political Declaration of the High-Level Meeting of the General Assembly of the United Nations on the Prevention and Control of Non-communicable Diseases. 2011. http://www.cfr.org/global-health/political-declaration-high-level-meeting-general-assembly-prevention-control-non-communicable-diseases/p25953. Accessed September 4, 2012
7.
Zere E, Walker O, Kirigia J, Zawaira F, Magombo F, Kataika E. Health financing in Malawi: evidence from national health accounts.  BMC Int Health Hum Rights. 2010;10:27PubMedArticle
8.
Lavy C, Tindall A, Steinlechner C, Mkandawire N, Chimangeni S. Surgery in Malawi: a national survey of activity in rural and urban hospitals.  Ann R Coll Surg Engl. 2007;89(7):722-724PubMedArticle
9.
Ferlay J, Shin HR, Bray F, Forman D, Mathers C, Parkin DM. Estimates of worldwide burden of cancer in 2008: GLOBOCAN 2008.  Int J Cancer. 2010;127(12):2893-2917PubMedArticle
10.
Jemal A, Bray F, Center MM, Ferlay J, Ward E, Forman D. Global cancer statistics.  CA Cancer J Clin. 2011;61(2):69-90PubMedArticle
11.
Msyamboza KP, Dzamalala C, Mdokwe C,  et al.  Burden of cancer in Malawi; common types, incidence and trends: national population-based cancer registry.  BMC Res Notes. 2012;5(1):149PubMedArticle
12.
Clegg-Lamptey J, Dakubo J, Attobra YN. Why do breast cancer patients report late or abscond during treatment in Ghana? a pilot study.  Ghana Med J. 2009;43(3):127-131PubMed
13.
Dye TD, Bogale S, Hobden C,  et al.  Complex care systems in developing countries: breast cancer patient navigation in Ethiopia.  Cancer. 2010;116(3):577-585PubMedArticle
14.
Malik IA, Gopalan S. Use of CAM results in delay in seeking medical advice for breast cancer.  Eur J Epidemiol. 2003;18(8):817-822PubMedArticle
15.
Kushner AL, Cherian MN, Noel L, Spiegel DA, Groth S, Etienne C. Addressing the Millennium Development Goals from a surgical perspective: essential surgery and anesthesia in 8 low- and middle-income countries.  Arch Surg. 2010;145(2):154-159PubMedArticle
16.
Farmer PE, Kim JY. Surgery and global health: a view from beyond the OR.  World J Surg. 2008;32(4):533-536PubMedArticle
17.
Thumbs A, Borgstein E, Vigna L,  et al.  Self-expanding metal stents (SEMS) for patients with advanced esophageal cancer in Malawi: an effective palliative treatment.  J Surg Oncol. 2012;105(4):410-414PubMedArticle
18.
Pagni F, Bono F, Di Bella C, Faravelli A, Cappellini A. Virtual surgical pathology in underdeveloped countries: The Zambia Project.  Arch Pathol Lab Med. 2011;135(2):215-219PubMed
19.
Hazin R, Qaddoumi I. Teleoncology: current and future applications for improving cancer care globally.  Lancet Oncol. 2010;11(2):204-210PubMedArticle
20.
Bumpous JM, Randolph GW. The expanding utility of office-based ultrasound for the head and neck surgeon.  Otolaryngol Clin North Am. 2010;43(6):1203-1208, viPubMedArticle
21.
Layeequr Rahman R, Crawford S, Hall T, Bavosi D, Quinlan R. Surgical-office-based versus radiology-referral-based breast ultrasonography: a comparison of efficiency, cost, and patient satisfaction.  J Am Coll Surg. 2008;207(5):763-766PubMedArticle
22.
Usman HR, Rahbar MH, Kristensen S,  et al.  Randomized controlled trial to improve childhood immunization adherence in rural Pakistan: redesigned immunization card and maternal education.  Trop Med Int Health. 2011;16(3):334-342PubMedArticle
23.
Olapade-Olaopa EO, Obamuyide HA, Yisa GT. Management of advanced prostate cancer in Africa.  Can J Urol. 2008;15(1):3890-3898PubMed
24.
El Saghir NS, Adebamowo CA, Anderson BO,  et al.  Breast cancer management in low resource countries (LRCs): consensus statement from the Breast Health Global Initiative.  Breast. 2011;20:(suppl 2)  S3-S11PubMedArticle
25.
Jazieh AR, Azim HA, McClure J, Jahanzeb M. The process of NCCN guidelines adaptation to the Middle East and North Africa region.  J Natl Compr Canc Netw. 2010;8:(suppl 3)  S5-S7PubMed
Original Article
Dec 2012

Cancer Surgery in Low-Income CountriesAn Unmet Need

Author Affiliations

Author Affiliations: Departments of Surgery, Memorial Sloan-Kettering Cancer Center, New York, New York (Drs Gyorki, Brennan, and Kingham); Kamuzu Central Hospital, Lilongwe, Malawi (Dr Muyco); and Columbia University, New York, New York (Dr Kushner).

Arch Surg. 2012;147(12):1135-1140. doi:10.1001/archsurg.2012.1265
Abstract

Objectives To describe the surgical oncology experience at a major regional hospital in Malawi and to identify barriers to improved outcomes.

Design Retrospective review of operating logbooks from a single tertiary referral center.

Setting Major tertiary referral center (Kamuzu Central Hospital) in Lilongwe, Malawi, in sub-Saharan Africa.

Patients Patients were identified with a suspected diagnosis of cancer from January 1, 2004, through March 7, 2007.

Main Outcome Measures Cancer cases were classified according to patient demographic characteristics, disease location, and therapeutic intent. The Malawi data were compared with US data from the Surveillance Epidemiology and End Results database.

Results A malignant diagnosis was suspected in 255 of the 1440 patients undergoing a major resection (17.8%) (mean patient age, 53 years). The most common cancers in males were prostate, esophageal, and gastric. In females, the most common cancers were breast, colon, and esophageal. Many of the procedures were performed with palliative intent.

Conclusions Cancer surgery comprises a significant proportion of the surgical caseload in low-income countries. Patients often present with late-stage, inoperable cancer. The participation of the surgical community is critical for addressing barriers to effective cancer care.

The global burden of cancer is increasingly borne by patients in the developing world. The International Agency for Research on Cancer predicts that by 2030, the global burden of cancer will reach 21.4 million and the annual number of cancer deaths worldwide will reach 13.2 million.1 The World Health Organization (WHO) predicts that by 2020, approximately 60% of all new cancer cases will occur in the least developed nations.2

In wealthy countries, the paradigm for treating some cancers is changing because patients' cancers are diagnosed at an earlier stage and many of those with advanced disease are surviving for longer periods with the aid of systemic therapy. In contrast, in low- and middle-income countries (LMICs), patients with cancer often present late, and the mortality rates are sobering (Figure 1). These diseases are becoming a leading cause of death in patients older than 15 years.4 Public health efforts are slowly beginning to emphasize cancer care as a global priority. For example, the Global Task Force on Expanded Access to Cancer Care and Control in Developing Countries was established in 2009. This collaboration of the Dana Farber Cancer Institute, Harvard Global Equity Initiative, Harvard Medical School, and Harvard School of Public Health published a call to action for the global medical community in 2010.3 The United Nations (UN) is also increasingly aware of the mortality in LMICs caused by noncommunicable diseases, including cancer. During the September 2011 meeting of the UN General Assembly, a high-level meeting was held for 2 days with a focus on noncommunicable diseases, analogous to the Declaration of Commitment to human immunodeficiency virus and AIDS that occurred a decade ago.5 A declaration was formulated, with global leaders agreeing on a need for global monitoring targets and increased efforts to prevent and treat noncommunicable diseases and improve health care.6 Recognizing that the burden of cancer is a global problem, we sought to identify surgically treated cancers in a major tertiary referral center in Malawi in order to expose a growing need for surgical involvement in global cancer efforts.

Malawi is a small country in sub-Saharan Africa with a population of approximately 12 million. The annual per capita expenditure on health care is one of the lowest in the world at approximately US$25.7 Approximately 60% of surgical care is provided in the public system, with the remainder provided in private and mission hospitals.8 We compared data from a tertiary referral center in Malawi with data from throughout Africa and from the US Surveillance Epidemiology and End Results (SEER) database to characterize the surgical oncology patient population in a major Malawian treatment center.

METHODS

Data from the operating room logbooks dated January 1, 2004, through March 7, 2007, from Kamuzu Central Hospital (KCH) in Lilongwe, Malawi, were retrospectively collected. The logbooks dated November 23, 2005, through November 1, 2006, were unavailable for examination. Therefore, the total study period is 28 months. All cancer cases during this period were recorded and categorized according to subspecialty and body region. An attempt was made to classify the intention of treatment as curative or palliative. Follow-up data were not available because medical records are kept by the patient and not stored at the hospital. No histopathology services are available at the KCH. Some patients hand carried their specimens to the lone pathologist in the country, located in Blantyre, Malawi. Thus, many diagnoses of cancer are based on clinical impressions. Cases were only included in this survey if the clinical impression of the treating clinician was a diagnosis of cancer.

To compare age-standardized incidence between the KCH patients and patients in the United States, we queried the SEER database. The incidence data for 2006 (per 100 000 people) were multiplied by population data from the US Census Bureau for the same year. Population proportions were calculated from the sum of these age groups.

RESULTS

The operating room logbooks at the KCH revealed that 1440 general and urologic operations were performed during the 28-month study period. (Minor procedures, such as debridement and abscess drainage, were excluded.) Of these operations, 255 (17.8%) resulted in a diagnosis suggestive of cancer. The most common cancer in males was prostate, followed by esophageal and gastric (Figure 2). In females, the 3 most common cancers were breast, colon, and esophageal.

Demographic data regarding patient age were available in 83.5% of cases. The mean (SD) age of patients was 53 (18.3) years (median, 52 years; range, 3-94 years) (Table 1). This number is an approximation, however, because in Malawi, patients often do not have birth certificates and therefore estimate their ages. Many patients presented before the age of 50 years. In patients with testicular, breast, and colon cancer, 80.0%, 77.8%, and 51.7%, respectively, were younger than 50 years (Figure 3). In comparison, in the United States, the proportions of patients 49 years or younger diagnosed as having testicular, breast, and colon cancer are 86%, 22%, and 9%, respectively, according to SEER data from 2006.

Many of the procedures were performed with a palliative or noncurative intent (Table 2), especially procedures for gastrointestinal cancers, which often presented at a late and inoperable stage. In patients with esophageal cancer, 76.0% of surgical interventions involved placement of palliative gastric feeding tubes. Similarly, for patients with gastric cancer, 58.6% of cases were palliative and involved a feeding tube (24.1%) or laparotomy without resection (34.5%). In colorectal cancer cases, only a few patients (29.4%) could be treated with curative intent.

We compared the proportion of cancer types seen at KCH with previously published global data (Figure 4). This comparison group reflects age-standardized cancer incidence in less developed countries as calculated for the year 2008 by the International Agency for Research on Cancer (GLOBOCAN).9 There is strong concordance for many cancer types between the surgical caseload at KCH and the published cancer incidence in low-income countries. Lung and hepatocellular carcinomas, which make up 12% and 9% of new cancer diagnoses in less developed countries,9 are not seen in the KCH surgical data set. This finding may reflect regional differences in the GLOBOCAN estimates, especially because calculations on cancer incidence in Africa were based on only 7 cancer registries, representing less than 6% of the African population.9 Lung cancer has been previously shown to be underrepresented in sub-Saharan Africa, including in Malawi.10,11 The absence of these tumor types in the surgical oncology caseload may also reflect a lack of surgical expertise in thoracic and hepatobiliary surgery or the fact that these cancers present at an advanced stage.

COMMENT

Since the declaration of the war on cancer in the early 1970s, vast resources have been committed to cancer research. Our understanding of the etiology and pathogenesis of malignant cancer has advanced and is reflected in improved patient outcomes. A new challenge is to translate these developments to resource-poor settings, which increasingly bear the bulk of the world's cancer burden.

Our data from a tertiary care center in Malawi demonstrate a different patient population from that in developed countries. Patients present at a younger age, and most patients described in this study presented at an advanced stage of disease. A variety of reports in the breast cancer literature from African institutions have identified key factors for delayed presentation, including low levels of awareness, barriers to health care accessibility, lack of early detection, and alternative health care models.1214

Surgery is a central component of all aspects of cancer care, including biopsies for diagnosis, resections for definitive treatment, and procedures for palliation. Surgery remains the most effective therapy for the treatment of most solid tumors. Cancer surgery for many tumor types can be performed safely and efficiently with minimal resources and requires only basic surgical instruments. The small number of surgeons in most developing countries makes access to surgical care a major barrier to cancer care. A recent analysis of surgical resources in LMICs using a standardized WHO tool identified major infrastructure shortfalls in district hospitals.15 For example, almost half (45%) of district hospitals in these countries do not have an anesthesia machine, and more than 52% lack a steady supply of sterile gloves. Beyond material resources, a small workforce is also a major obstacle. The KCH serves approximately 5 million people in the central district of Malawi and is staffed by only 4 or 5 fully trained surgeons, a variable number of clinical officers, and a fledgling surgical residency program. In addition, surgeons are underrepresented in the public health community, so surgery is often an overlooked component of public health efforts.16

We compared the patients with cancer who presented for surgery at KCH with recently published cancer registry data from Malawi.11 The WHO publication describes the almost 19 000 patients recorded in the country's cancer registry between 2007 and 2010. These data reveal that in the younger than 60-year age group from the Malawi cancer registry (which makes up 84% of new cancer diagnoses), the 2 most common cancers are Kaposi sarcoma and cervical cancer, both of which are associated with viral causes. These 2 cancer types are not treated by surgeons at KCH, so they are not represented in this data set. In the older than 60-year group, esophageal cancer becomes the most frequent and prostate, bladder, and gastrointestinal tumors are seen far more commonly. The surgical oncology case mix at KCH more closely resembles the older than 60-year cancer population in Malawi. This finding is reflected in the median age of the patient group, which is 52 years (range, 3-94 years), in a country where the overall median age is 17.2 years.

The intention of surgery for many of the patients was likely palliative from the outset. The surgeons at KCH are competent at resections for bulky cancers; therefore, it is likely that in many cases, the decision for palliative surgery was determined by tumor biology rather than technical deficiency. Palliative interventions have an important role to play in low-resource settings. In Malawi, KCH was a participating center in a study that demonstrated durable results with palliative interventions in a central hospital setting.17

Some of the limitations to adequate cancer care identified at KCH are emphasized in the Malawi cancer registry.11 Only 17.9% of cancers were diagnosed based on histologic analysis, cytologic testing, or laboratory values, with most diagnoses based on clinical or radiologic suspicion. These data demonstrate that beyond the availability of surgeons and basic supplies, there are additional barriers to providing basic cancer surgical services in low-income countries. Patients require an accurate cancer diagnosis and appropriate cancer staging to optimize surgical decision making.

Malawi has a single pathologist who serves a population of 15 million, and the approximate time for pathologic test result reporting is 3 months. Many specimens are not sent for analysis, and even if the specimens are sent, many patients are lost to follow-up in the intervening time. It is possible that some of the cases diagnosed as malignant in this series may actually have been benign. The converse is also true: tumors treated as benign may have actually harbored an undiagnosed malignant cancer. Similarly, Zambia, a country of 12 million people, has a single pathology laboratory. In an attempt to relieve this huge burden, the Italian Association of Pathologists (Patologi Oltre Frontiera) created a virtual pathology laboratory using telepathology to perform hematoxylin-eosin microscopy and cytologic testing of surgical specimens.18 This novel approach may allow for accurate diagnoses and guide the management of the growing burden of surgical disease.

Staging cancer is also a challenge in LMICs. Despite being among the biggest hospitals in Malawi, KCH does not have access to computed tomography, and therefore cancers cannot be preoperatively staged and some cannot even be diagnosed. Malawi's cancer registry contains staging information on a mere 0.7% of cancer cases.11 As technology for cross-sectional imaging becomes cheaper, efforts should be made to have these services available at major treatment centers across the globe. Teleoncology initiatives have been implemented in many developing countries to aid in the interpretation of results and in education and are becoming increasingly available as Internet access becomes more affordable.19 Furthermore, surgeons could be trained to use less expensive imaging tools, such as ultrasonography, as has occurred in many fields in modern medicine.20,21

Data collection is a difficult but crucial component of improving diagnoses and managing cancer in the developing world. A simple intervention would be the implementation of a basic data card containing information such as age, sex, date of suspected cancer diagnosis, treatment to date, and an estimate of tumor stage. This card would be held by each patient diagnosed as having cancer to ensure integrity and recall of data. Similar data cards have been used to improve adherence to childhood vaccination22 and for other maternal and child health programs throughout the developing world.

Many of the limitations described in this article clearly render the implementation of the National Comprehensive Cancer Network guidelines impossible in low-income economies. The lack of patient follow-up in Malawi and many LMICs makes it challenging to determine optimal therapy, particularly when surgery is the only therapeutic option because of the absence of chemotherapy and radiotherapy. Although some procedures, such as orchiectomy for prostate cancer, are established with some benefit,23 others, such as toilet mastectomy for metastatic breast cancer, are unlikely to improve outcomes for patients.24 Because of the lack of data to support alternative treatment regimens in LMICs, working groups have been established to adapt these guidelines for the Middle East and Africa, as well as other regions of the world.25 A good example of an existing program is the Breast Health Global Initiative, which is composed of a group of international breast cancer experts who have developed a consensus statement for the management of breast cancer in low-resource countries.24 These guidelines are created with an awareness of the limited resources in these settings, such as difficulties of access to radiation therapy and limited access to certain chemotherapeutic agents.

This article has obvious limitations in the quality of the data collection and lack of patient follow-up. However, the data capture the demographic characteristics of patients with malignant cancer treated with surgery in Malawi and serve to highlight the major resource deficiencies in cancer care in low-income countries, which is particularly important because malignant disease is increasingly being appreciated as a disease burden in these countries. The surgical workforce in these countries is an important resource for meeting this challenge. In addition, the need for prospective research endeavors is highlighted because disparities in age at presentation and tumor incidence suggest there may be differences in causes and biology that currently are not understood. Four key strategies that can be implemented in a low-resource setting are improvement of pathology services, improvement of radiology services, data collection, and modified guideline implementation. Without increased representation by surgeons in the global health arena of the UN, the WHO, and other global initiatives, the major modality used to cure patients with solid tumors will continue to be severely underused. General surgeons and surgical oncologists in the developed world can fill a major void by increasing awareness, collaborating globally, and supporting surgical colleagues in developing countries.

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Article Information

Correspondence: T. Peter Kingham, MD, Department of Surgery, Memorial Sloan-Kettering Cancer Center, 1275 York Ave, New York, NY 10065 (kinghamt@mskcc.org).

Accepted for Publication: April 27, 2012.

Author Contributions:Study concept and design: Gyorki and Kingham. Acquisition of data: Kingham and Muyco. Analysis and interpretation of data: Gyorki, Kushner, Brennan, and Kingham. Drafting of the manuscript: Gyorki, Kushner, Brennan, and Kingham. Study supervision: Kingham.

Conflict of Interest Disclosures: None reported.

REFERENCES
1.
Ferlay JSH, Bray F, Forman D, Mathers CD, Parkin D. GLOBOCAN 2008, Cancer Incidence and Mortality Worldwide: IARC CancerBase No. 10. Lyon, France: International Agency for Research on Cancer; 2010
2.
Kachroo S, Etzel CJ. Decreasing the cancer burden in developing countries: concerns and recommendations.  Eur J Cancer Care (Engl). 2009;18(1):18-21PubMedArticle
3.
Farmer P, Frenk J, Knaul FM,  et al.  Expansion of cancer care and control in countries of low and middle income: a call to action.  Lancet. 2010;376(9747):1186-1193PubMedArticle
4.
World Health Organization.  National Cancer Control Programmes, policies and managerial guidelines. 2002. http://www.who.int/cancer/media/en/409.pdf. Accessed November 11, 2011
5.
Narayan KM, Ali MK, del Rio C, Koplan JP, Curran J. Global noncommunicable diseases: lessons from the HIV-AIDS experience.  N Engl J Med. 2011;365(10):876-878PubMedArticle
6.
Council on Foreign Relations.  Political Declaration of the High-Level Meeting of the General Assembly of the United Nations on the Prevention and Control of Non-communicable Diseases. 2011. http://www.cfr.org/global-health/political-declaration-high-level-meeting-general-assembly-prevention-control-non-communicable-diseases/p25953. Accessed September 4, 2012
7.
Zere E, Walker O, Kirigia J, Zawaira F, Magombo F, Kataika E. Health financing in Malawi: evidence from national health accounts.  BMC Int Health Hum Rights. 2010;10:27PubMedArticle
8.
Lavy C, Tindall A, Steinlechner C, Mkandawire N, Chimangeni S. Surgery in Malawi: a national survey of activity in rural and urban hospitals.  Ann R Coll Surg Engl. 2007;89(7):722-724PubMedArticle
9.
Ferlay J, Shin HR, Bray F, Forman D, Mathers C, Parkin DM. Estimates of worldwide burden of cancer in 2008: GLOBOCAN 2008.  Int J Cancer. 2010;127(12):2893-2917PubMedArticle
10.
Jemal A, Bray F, Center MM, Ferlay J, Ward E, Forman D. Global cancer statistics.  CA Cancer J Clin. 2011;61(2):69-90PubMedArticle
11.
Msyamboza KP, Dzamalala C, Mdokwe C,  et al.  Burden of cancer in Malawi; common types, incidence and trends: national population-based cancer registry.  BMC Res Notes. 2012;5(1):149PubMedArticle
12.
Clegg-Lamptey J, Dakubo J, Attobra YN. Why do breast cancer patients report late or abscond during treatment in Ghana? a pilot study.  Ghana Med J. 2009;43(3):127-131PubMed
13.
Dye TD, Bogale S, Hobden C,  et al.  Complex care systems in developing countries: breast cancer patient navigation in Ethiopia.  Cancer. 2010;116(3):577-585PubMedArticle
14.
Malik IA, Gopalan S. Use of CAM results in delay in seeking medical advice for breast cancer.  Eur J Epidemiol. 2003;18(8):817-822PubMedArticle
15.
Kushner AL, Cherian MN, Noel L, Spiegel DA, Groth S, Etienne C. Addressing the Millennium Development Goals from a surgical perspective: essential surgery and anesthesia in 8 low- and middle-income countries.  Arch Surg. 2010;145(2):154-159PubMedArticle
16.
Farmer PE, Kim JY. Surgery and global health: a view from beyond the OR.  World J Surg. 2008;32(4):533-536PubMedArticle
17.
Thumbs A, Borgstein E, Vigna L,  et al.  Self-expanding metal stents (SEMS) for patients with advanced esophageal cancer in Malawi: an effective palliative treatment.  J Surg Oncol. 2012;105(4):410-414PubMedArticle
18.
Pagni F, Bono F, Di Bella C, Faravelli A, Cappellini A. Virtual surgical pathology in underdeveloped countries: The Zambia Project.  Arch Pathol Lab Med. 2011;135(2):215-219PubMed
19.
Hazin R, Qaddoumi I. Teleoncology: current and future applications for improving cancer care globally.  Lancet Oncol. 2010;11(2):204-210PubMedArticle
20.
Bumpous JM, Randolph GW. The expanding utility of office-based ultrasound for the head and neck surgeon.  Otolaryngol Clin North Am. 2010;43(6):1203-1208, viPubMedArticle
21.
Layeequr Rahman R, Crawford S, Hall T, Bavosi D, Quinlan R. Surgical-office-based versus radiology-referral-based breast ultrasonography: a comparison of efficiency, cost, and patient satisfaction.  J Am Coll Surg. 2008;207(5):763-766PubMedArticle
22.
Usman HR, Rahbar MH, Kristensen S,  et al.  Randomized controlled trial to improve childhood immunization adherence in rural Pakistan: redesigned immunization card and maternal education.  Trop Med Int Health. 2011;16(3):334-342PubMedArticle
23.
Olapade-Olaopa EO, Obamuyide HA, Yisa GT. Management of advanced prostate cancer in Africa.  Can J Urol. 2008;15(1):3890-3898PubMed
24.
El Saghir NS, Adebamowo CA, Anderson BO,  et al.  Breast cancer management in low resource countries (LRCs): consensus statement from the Breast Health Global Initiative.  Breast. 2011;20:(suppl 2)  S3-S11PubMedArticle
25.
Jazieh AR, Azim HA, McClure J, Jahanzeb M. The process of NCCN guidelines adaptation to the Middle East and North Africa region.  J Natl Compr Canc Netw. 2010;8:(suppl 3)  S5-S7PubMed
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