Cardiovascular Imaging in the Developing World

In the developing world, growing rates of CVD 

At the beginning of the 20th century, cardiovascular disease (CVD) was responsible for fewer than 10% of all deaths worldwide. Today, that figure is about 30%, with 80% of the burden now occurring in developing countries. Over the past several years, the United Nations has been calling attention to the dramatic and increasing burden of non-communicable diseases in developing nations, especially the high mortality rates due to CVD. Globally, CVDs, which include coronary heart disease, strokes, rheumatic heart disease (RHD), cardiomyopathy, and other heart diseases, represent the leading cause of death, far outstripping deaths due to malaria, HIV/AIDS, and tuberculosis. Fortunately, there is a growing understanding of the importance of strategies that foster early detection and treatment as critical steps toward altering expected trends in CVD. Imaging is a critical component of diagnosis and triage of patients with CVD. In the developing world, accessible imaging services suffer from a lack of equipment and appropriately trained personnel; however, the versatility of ultrasound and other emerging technologies may provide increased access to necessary cardiovascular imaging. 

In this article, readers will encounter a multiplicity of terms used to express the complex classification of healthcare-related resource disparity in our world. There is no perfect terminology to describe the countries, communities, or hospitals that either lack services or could benefit from their improvement. Unfortunately, phrases like “developing world” and “resource-limited countries” are common, but considered by authorities to be ambiguous and inadequate. The World Bank classifies countries using terminology such as “low income”, “middle income” and “high income”, yet even high-income countries may have areas of poverty. Our use of these descriptive phrases simply reflects those phrases used by the sources complied for this article.

The World Health Organization reports that an estimated 17.5 million people died from CVDs in 2012. Of these deaths, an estimated 7.4 million were due to coronary heart disease and 6.7 million were due to stroke. Over three quarters of CVD deaths take place in low- and middle-income countries. (LMICs). Out of the 16 million deaths under the age of 70 due to noncommunicable diseases, 82% are in low- and middle-income countries, and 37% are caused by CVDs. During the years 1990 to 2020, expected increases in coronary heart disease rates alone are projected to be 137% in men and 120% in women in developing countries, compared with 60% and 30% in developed countries. Going ten years further into 2030, projected increases in CVD deaths for developing countries far exceed that for higher income nations by nearly twofold; with a 120-137% increase expected.

These statistics are alarming, because patients with CVD in LMICs tend to have poorer outcomes than their counterparts in the United States and other high-income countries. CVD deaths usually happen at an earlier age and during the peak productive decades of life in developing countries, in contrast to developed countries, where the CVD-related death usually occurs later in life. This can have a large impact on a developing country’s economic viability. In the recent report “A Race Against Time”, the authors evaluated the potential loss due to early CVD. In the five countries surveyed (Brazil, India, China, South Africa, and Mexico), conservative estimates indicated that at least 21 million years of future productive life are lost because of CVD each year. This fact magnifies the economic problems for nations in need of manpower. In developing countries, the consequences of a lack of available diagnostic modalities may delay care and presentation at a more advanced stage of illness, potentially resulting in increased hospitalizations for heart failure or treatment for more extensive cardiovascular disease. 

CVD confers a heavy financial burden in low- and middle-income countries. In addition to the great suffering and loss of life associated with CVD, developing countries face great economic challenges associated with the epidemic. The projected economic burden of CVD in developing countries in the near term is expected to be dramatic, encompassing significant costs on existing healthcare systems and the national economy. In South Africa, for example, 2% to 3% of the country’s gross national income, or roughly 25% of South African healthcare expenditures, was devoted to the direct treatment of CVD. Zhao et al report in Global Heart that noncommunicable diseases, including CVD and diabetes, are estimated to reduce gross domestic product by up to 6.77% in low- and middle-income countries. Over the period from 2011 to 2025, the cumulative lost output in low- and middle-income countries associated with CVD is projected to be USD$3.76 trillion. According to the World Health Organization, the combination of heart disease, stroke, and diabetes reduces gross domestic product by an estimated 1-5% in rapidly growing LMICs.

Insufficient access to diagnostic imaging: possible solutions

Strategies to develop healthcare centers utilizing effective diagnostic imaging approaches have the potential to dramatically influence the course of heart disease within these populations. Diagnostic ultrasound, angiography, computed tomography, and nuclear cardiology are some of the most powerful medical technologies available to diagnose cardiovascular disease. Yet, globally, these services are still insufficiently available. For example, the World Health Organization has stated that although the use of x-rays and ultrasound can resolve between 70% and 80% of diagnostic problems, nearly two-thirds of the world’s population has no access to basic diagnostic imaging. Despite the billions of dollars spent each year on an ever-increasing array of medical devices and equipment, many countries still do not recognize the management of devices as an integral part of public health policy. Approximately 95% of medical technology in developing countries is imported, but much of it does not meet the needs of national healthcare systems. It is estimated that over 50% of equipment is not being used, either because of a lack of maintenance or spare parts, because it is too sophisticated or in disrepair, or simply because the health personnel have not been adequately trained to use it. 

Techniques for the early detection of CVDs have provided important insights into disease patterns and pathogenesis, and especially the effects of progressive urbanization on cardiovascular risk. Furthermore, certain other diseases affecting the cardiovascular system remain prevalent and important causes of cardiovascular morbidity and mortality in developing countries, including the cardiac effects of rheumatic heart disease and the vascular effects of malaria. Imaging and functional studies of early cardiovascular changes in those disease processes have also recently been published by various groups, allowing for the consideration of screening and early treatment opportunities. 

People with cardiovascular disease or those who are at high cardiovascular risk need early detection, regardless of their economic realities. There are many challenges to the use of cardiac imaging technology in developing countries. However, some patients in very poor areas do receive cardiac diagnostic care. This section will review approaches in the developing world.

It is difficult to say how much of the reduction in mortality observed in developed nations has to do with the use of technology and advanced cardiac imaging. Certainly, we do not have data for a definitive and precise answer. Nevertheless, we can say that an effective way to reduce CVD mortality is to promote primary prevention, identify and control modifiable risk factors, and to initiate secondary prevention when individuals at a higher risk with established CVD are identified. This approach has a very intimate relationship to cardiovascular imaging.

Ultrasound: the promise of handheld

The value of ultrasound as a diagnostic cardiac modality is in many respects unparalleled; consequently, the bulk of this section will focus on the potential of this imaging modality. In the 1980s, we began to see researchers using general-purpose ultrasound to evaluate CVD. In Sudan, for example, cardiac abnormalities were identified via ultrasound use, including valvular disease, pericardial effusion, dilated cardiomyopathy, congenital heart disease, mitral valve prolapse, and cardiac masses. Research concluded that echocardiography is applicable even in remote tropical areas and that its value, considering costs, therapeutic consequences, and clinical benefit in developing countries, can be substantial. In Nigeria, several trials have employed echo in the investigation of various CVDs, including hypertensive heart disease, congestive heart failure, and mitral stenosis. Portable echo has proven to be helpful in the evaluation of many other diseases endemic to developing countries and has been used to assess cardiac function and hemodynamic status in children admitted to a Kenyan hospital with severe malaria. 

Although the incidence of coronary artery disease (CAD) is growing in LMICs, hypertensive heart disease, cardiomyopathies, and valvular defects as sequelae of infectious etiologies make up a large percentage of cardiac disease. These conditions are easily evaluated by echo. Rheumatic heart disease (RHD), the only long-term consequence of acute rheumatic fever, continues unabated among middle-income and low-income countries, and in some indigenous communities of the industrialized world. RHD results in significant morbidity and mortality in low-resource settings. It is currently estimated that at least 15.6-20 million people have clinically recognized RHD, which has an annual mortality rate between 3 and 12.5%. Even more concerning is the potential volume of unrecognized cases detectable by echocardiographic screening. The global burden of disease caused by rheumatic fever currently falls disproportionately on children living in the developing world. Prevalence studies from across four continents have shown 1.5-5.7% of asymptomatic primary schoolchildren in high-risk settings demonstrate echocardiographic evidence of RHD. Armed with evidence like this, it is not surprising that the World Health Organization recommends echocardiographic screening for RHD when feasible in RHD “endemic” areas and the World Heart Federation has provided evidence-based guidelines.

One barrier to implementation of echocardiographic screening is the expense of standard echocardiography machines. Fortunately, innovation in echo technology continues to expand its utility in the developing world. In a 2004 study in Gambia, physicians used a hand-held ultrasound to identify high-risk patients with cardiovascular disease and hypertension. Of the 1,997 patients seen, 17% were found to have elevated blood pressure, and all of these patients underwent echocardiography to identify left ventricular hypertrophy, as a marker for those at highest risk of a cardiovascular event. Sixty-five percent of this hypertensive population demonstrated left ventricular hypertrophy by ultrasound and were started on antihypertensive medications. As a result, of this screening, the identification of high-risk hypertensive patients enabled a more effective use of limited healthcare resources. 

The development of battery-powered, hand-carried echocardiography has allowed clinicians to extend their reach in areas with limited access to diagnostic equipment and offers the promise of sensitive case detection at a fraction of the expense. Nevertheless, limited data exist on their use in RHD, and the current guidelines for echocardiographic diagnosis of RHD depend on a fully functional system. However, a recent study by Andrea Beaton and associates compared handheld echocardiography with a standard portable echocardiography machine, and demonstrated the potential of these handheld devices. The large-scale field screening showed that handheld devices have good sensitivity and specificity for diagnosis of early RHD. As data begin to accumulate on the cost-effectiveness of echo-based screening, handheld is proving to be a less expensive alternative to the standard portable echocardiography machine. However, strategies that evaluate simplified screening protocols and training of non-physicians are needed before widespread deployment of handheld-based protocols. 

The recognition of the value of simplified screening protocols and training of non-physicians is of particular importance in the developing world. There are 57 countries with a critical shortage of healthcare workers. The continent of Africa, for example, has 2.3 healthcare workers per 1000 people, compared with the Americas, which have 24.8 healthcare workers per 1000 people. Physicians, nurses, and medical officers have demonstrated the ability to perform and interpret a large variety of ultrasound exams, and a growing body of literature supports the use of point-of-care ultrasound in developing nations. As reported in Circulation: Cardiovascular Imaging, Mirabel et al prospectively compared focused cardiac ultrasound (FCU) to a reference approach for RHD screening in a school children population. FCU included the use of a pocket-sized echocardiography machine, non-expert staff (2 nurses with specific training), and a simplified set of echocardiographic criteria. They found that FCU by non-experts using pocket devices was feasible and yielded acceptable sensitivity and specificity for RHD detection when compared with the state-of-the-art approach, thereby opening new perspectives for mass screening for RHD in low-resource settings. Findings such as this are especially relevant to the inadequate health systems developing nations, which have been badly damaged by the migration of their health professionals. 

Pocket-size ultrasound has increased echocardiographic portability, but expert point-of-care interpretation may not be readily available. Remote interpretation on a smartphone with dedicated medical imaging software has the potential to be as accurate as on a workstation. An interesting study by Michelis et al described transmitting images for verification of point-of-care diagnosis directly from the field via a dial-up modem (or via a broadband connection in an urban center when connectivity was limited) to two expert echocardiographers in the United States. They concluded that remote expert echocardiographic interpretation can provide backup support to point-of-care diagnosis by non-experts when read on a dedicated smartphone-based application. Mobile-to-mobile consultation may soon improve access in previously inaccessible locations, so that echocardiographic interpretation can be performed by experienced cardiologists.

Angiography and interventional cardiology

While the risk factors, management, and outcome of acute myocardial infarction (AMI) have been extensively studied in the developed world, limited data is available on this subject from developing countries. Moreover, data on the use of diagnostic angiography and revascularization procedures in patients in developing countries is very scarce as well. Many developing countries are not able to provide enough cardiac catheterization laboratories to support programs for primary angioplasty as a primary modality of treatment for AMI. This inability is why the use of thrombolytic therapy remains mainstay of treatment for ST-elevation MI in these countries, and is higher than what is reported in developed countries. Obstacles cited that prevent the implementation of cardiac catheterization in developing countries are numerous, including economic hardship, lack of interest, lack of qualified personnel, deficiency in infrastructures for the diagnosis and treatment of cardiac pathologies, and cost of equipment. Angiography and catheter interventions are expensive due to the installation costs of expensive equipment, the requirement of dedicated personnel, and the need to stock a large inventory of expensive hardware such as catheters, balloons, and stents that must be imported from countries of high development. As a result, many catheter intervention procedures are beyond the reach of the average patient in the developing world. Believing that thousands of children suffering from heart disease cannot be ignored, a team from Chain of Hope-Belgium concluded that although pediatric cardiology in developing countries is by no means a top priority, cardiac catheterization can be performed safely and very effectively in a country with limited resources. The team concluded that if patients are well selected, this mode of treatment is possible without the support of a sophisticated catheterization laboratory. Using inexpensive equipment, namely, an x-ray c-arm and a portable echocardiography machine, they successfully used catheterization to treat pathologies that are the source of high mortality among children in developing countries. 

Computerized tomography

The presence of coronary artery calcium (CAC) indicates subclinical CAD and is associated with a greater progression of atherosclerosis. CAC scanning with CT can be of benefit in the early detection of CAD before the onset of clinical symptoms, and has great potential to direct scarce healthcare resources to patients at higher risk for CVD. Research in developing countries have generally been done in large cities; therefore, there might be selection bias that needs to be considered when examining the reported CAC distribution, severity, and relationship to events in these studies. Despite these limitations, these studies from developing countries have, remarkably, demonstrated conclusions (with regard to the epidemiology and prognosis associated with CAC) similar to those from developed countries. Although evidence is lacking, the cost effectiveness of CAC screening may differ greatly between developed and developing countries. In developing countries, future research on CAC screening will focus on more generalized populations, including rural populations. Longitudinal randomized trials should focus on how CAC scanning might change long-term outcomes and cost-effectiveness assessments focused on CAC scanning should include the downstream cost of preventive therapies. 

Nuclear cardiology

While nuclear cardiology is widely used in developed countries, unfortunately its utilization in the developing world is quite heterogeneous or just non-existent. Utilization of nuclear cardiology worldwide generally mirrors a countries’ gross domestic product. The development of nuclear cardiology services and other advanced imaging modalities are currently hindered by many factors, including lack of worldwide maintenance and service, high cost equipment, as well as insufficient cardiac-specific training and, in some cases, lack of cardiologist involvement in this field. In some regions, equipment and drug or isotope costs exceed that of the United States. We are beginning to see reports of developing countries creating nuclear cardiology networks. There are numerous efforts to expand its use worldwide, including programs through the World Health Organization and World Bank, and to devise decentralized strategies within low-middle income countries to help confront the impending CVD epidemic. Regional centers can serve as hubs for service, access to equipment sales, and radioisotope production, as well as educational and training programs for physicians and technical staff in neighboring cities and countries. In this manner, the development of advanced cardiac imaging services, such as nuclear cardiology, can be promoted by experienced physicians who hold superior image interpretation knowledge, and can train others how to devise quality assurance programs and develop optimal image quality standards. Interestingly, the United States’ neighbor, Mexico, has significantly higher utilization rates when compared to other Central American and Caribbean countries, suggesting a greater penetration and utilization of nuclear cardiology for developing nations that border “high use” countries.

Local training remains critical

Comprehensive training programs in cardiac imaging for technologists and cardiologists are scarce in the developing world. Consequently, inadequate images may be acquired or patients may be exposed to unnecessary or excessive radiation. In addition, doctors may inappropriately order exams or misinterpret results, leading to erroneous diagnoses and poor patient outcomes. Delays in intervention due to the absence of accessible and reliable interpretation only worsen the growing prevalence of CVD. Telemedicine is an area of great promise, as proven by the accuracy of remote interpretation of echocardiographic images transmitted via a secure mobile-to-mobile system, but calculations made by the World Health Organization and others suggest that only about 0.1% of the potential telemedicine demand from the developing world is being met. In advanced healthcare systems, cardiac images are now transferred over wireless networks and stored digitally, but many developing nations lack the necessary high bandwidth, limiting the potential for telemedicine. According to a recent survey, telemedicine has progressed far less in lower-income countries than in high-income countries, both in terms of the proportion of countries with established services and the proportion offering pilot telemedicine services. Barriers include equipment breakdowns (early use of inexpensive but low-quality goods may have compounded this problem); a lack of maintenance support in rural hospitals, IT specialists, and medical engineers; slow Internet bandwidth (sometimes too slow for synchronous connection); and some staff reported they were reluctant to change practice patterns and uptake new technologies. 

Improvement in local training will be critical, paired with the concomitant expansion of imaging services to provide improved distribution imaging. The development of programs aimed at creating centralized centers for training, education, research, and service may provide opportunities for advanced imaging techniques to meet the needs of the growing at-risk patient population in low- to middle-income countries. Future programs should be considered that provide support for geographically diverse, but centrally located, high-quality cardiac imaging centers that could serve as hubs for training, education, research, and equipment maintenance or service. While increasing global CVD risk is a daunting adversary, incremental steps can be taken by global organizations and individual countries to directly impact the risk of CVD morbidity and mortality. For example, several telemedicine networks around the world deliver humanitarian services on a routine basis, many to low-income countries.

Conclusion

Health conditions in developing countries are becoming more like those in developed countries, with non-communicable diseases predominating and infectious diseases declining. The increased awareness of changing health needs, however, has not yet translated into significant shifts in resources or policy level attention from international donors or governments in affected countries. The Center for Global Development states that less than 3% of development assistance from 2001 through 2007 was aimed at chronic diseases. Funding for cardiac imaging modalities is crucial, since these services are very important in the diagnosis of CVDs, but can be costly. Unfortunately, many stakeholders in the economies of developing countries, such as large international donors, may simply not be aware of the urgency in addressing CVDs. 

There have been great advances in the field of global cardiac imaging. However, the need for further research, continued innovation, and advocacy is tremendous.  

Bibliography and recommended reading

1. Abdallah MH, Arnaout S, Karrowni W, Dakik HA. The management of acute myocardial infarction in developing countries. Int J Cardiol. 2006; 111(2): 189-194. 
2. Beaton A, Lu JC, Aliku T, et al. The utility of handheld echocardiography for early rheumatic heart disease diagnosis: a field study. Eur Heart J Cardiovasc Imaging. 2015; 16(5): 475-482. 
3. Carapetis JR, Steer AC, Mulholland EK, Weber M. The global burden of group A streptococcal diseases. Lancet Infect Dis. 2005; 5(11): 685-694. 
4. Celermajer DS, Chow CK, Marijon E, Anstey NM, Woo KS. Cardiovascular disease in the developing world: prevalences, patterns, and the potential of early disease detection. J Am Coll Cardiol. 2012; 60(14): 1207-1216. 
5. Choi BG, Mukherjee M, Dala P, et al. Interpretation of remotely downloaded pocket-size cardiac ultrasound images on a web-enabled smartphone: validation against workstation evaluation. J Am Soc Echocardiogr. 2011; 24(12): 1325-1330. 
6. Dakik HA, Koubeissi Z, Kleiman NS, et al. Acute myocardial infarction: clinical characteristics, management and outcome in a university medical centre in a developing Middle Eastern country. Can J Cardiol. 2004; 20(8): 789-793.
7. Feigl RANAB. Where Have All the Donors Gone? Scarce Donor Funding for Non-Communicable Diseases - Working Paper 228. Center for Global Development; 2010. Available online at https://ideas.repec.org/p/cgd/wpaper/228.html. Accessed July 26, 2016.
8. Fuster V, Voûte J. MDGs: chronic diseases are not on the agenda. Lancet. 2005; 366(9496): 1512-1514.
9. Gaziano TA. Cardiovascular disease in the developing world and Its cost-effective management. Circulation. 2005; 112(23): 3547-3553. 
10. A Race Against Time: The Challenge of Cardiovascular Disease in Developing Economies. The Center for Global Health and Economic Development. Available online at https://www.earth.columbia.edu/news/2004/images/raceagainsttime_FINAL_0410404.pdfAccessed July 27, 2016.
11. How does the World Bank classify countries? World Bank Data Help Desk. Available online at https://datahelpdesk.worldbank.org/knowledgebase/articles/378834-how-does-the-world-bank-classify-countries. Accessed July 23, 2016.
12. Kumar RK, Tynan MJ. Catheter interventions for congenital heart disease in third world countries. Pediatr Cardiol. 2005; 26(3): 241-249. 
13. Lopez AD, Mathers CD, Ezzati M, Jamison DT, Murray CJ, eds. Global Burden of Disease and Risk Factors. Washington (DC): World Bank; 2006. Available online at https://www.ncbi.nlm.nih.gov/books/NBK11812/. Accessed July 17, 2016.
14. Mensah GA, Roth GA, Sampson UKA, et al. Mortality from cardiovascular diseases in sub-Saharan Africa, 1990-2013: a systematic analysis of data from the Global Burden of Disease Study 2013. Cardiovasc J Afr. 2015; 26(2 Suppl 1): S6-S10. 
15. Michelis KC, Choi BG. Cardiovascular imaging in global health radiology. In: Mollura DJ, Lungren MP, eds. Radiology in Global Health. Springer New York; 2014:189-203. Available online at https://link.springer.com/chapter/10.1007/978-1-4614-0604-4_18. Accessed July 11, 2016.
16. 1Mirabel M, Bacquelin R, Tafflet M, et al. Screening for rheumatic heart disease: evaluation of a focused cardiac ultrasound approach. Circ Cardiovasc Imaging. 2015; 8(1): e002324. 
17. Naicker S, Plange-Rhule J, Tutt RC, Eastwood JB. Shortage of healthcare workers in developing countries--Africa. Ethn Dis. 2009; 19(1 Suppl 1): S1-60-64.
18. World radiography day: two-thirds of the world’s population has no access to diagnostic imaging. Pan American Health Organization/World Health Organization. Available online at https://www.paho.org/hq/index.php?option=com_content&view=article&id=7410%3A2012-dia-radiografia-dos-tercios-poblacion-mundial-no-tiene-acceso-diagnostico-imagen&catid=740%3Apress-releases&Itemid=1926&lang=en. Published November 12, 2012. Accessed July 23, 2016.
19. Prinz C, Voigt J-U. Diagnostic accuracy of a hand-held ultrasound scanner in routine patients referred for echocardiography. J Am Soc Echocardiogr. 2011; 24(2): 111-116. 
20. Reményi B, Wilson N, Steer A, et al. World Heart Federation criteria for echocardiographic diagnosis of rheumatic heart disease--an evidence-based guideline. Nat Rev Cardiol. 2012; 9(5): 297-309. 
21. Richter J, Dengler A, Mohammed EGER, et al. Results of echocardiographic examinations in a regional hospital of central Sudan. Trans R Soc Trop Med Hyg. 1990; 84(5): 749-752. 
22. Senga J, Rusingiza E, Mucumbitsi J, et al. Catheter interventions in congenital heart disease without regular catheterization laboratory equipment: the chain of hope experience in Rwanda. Pediatr Cardiol. 2012; 34(1): 39-45. 
23. Sicari R, Galderisi M, Voigt J-U, et al. The use of pocket-size imaging devices: a position statement of the European Association of Echocardiography. Eur Heart J Cardiovasc Imaging. 2011; 12(2): 85-87. 
24. Sippel S, Muruganandan K, Levine A, Shah S. Review article: use of ultrasound in the developing world. Int J Emerg Med. 2011; 4: 72. 
25. Telemedicine: opportunities and developments in member states. The World Health Organization. 2010. Available online at https://www.who.int/goe/publications/goe_telemedicine_2010.pdf. Accessed July 26, 2016.
26. Vitola JV. Nuclear cardiology and CVD in the developing world: Are we applying our scarce resources appropriately? Why is our mortality rate so high? J Nucl Cardiol. 2016 Jun 8. [Epub ahead of print] 
27. Vitola JV, Shaw LJ, Allam AH, et al. Assessing the need for nuclear cardiology and other advanced cardiac imaging modalities in the developing world. J Nucl Cardiol. 2009; 16(6): 956-961. 
28. World Health Organization Department of Essential Health. Essential Health Technologies Strategy 2004-2007. Available online at: https://peacesat.hawaii.edu/30PROGRAM/Activities/2004-01-24-USTTI_Pacific_Rim/Strategy.pdf.pdf Accessed July 11, 2016.
29. Zhao Y, Malik S, Wong ND. Evidence for coronary artery calcification screening in the early detection of coronary artery disease and implications of screening in developing countries. Glob Heart. 2014; 9(4): 399-407. 
30. Vitola JV, Shaw LJ, Allam AH, et al. Assessing the need for nuclear cardiology and other advanced cardiac imaging modalities in the developing world. J Nucl Cardiol. 2009; 16(6): 956-961. 
31. WHO | Cardiovascular diseases (CVDs). WHO. Available online at https://www.who.int/mediacentre/factsheets/fs317/en/. Accessed July 17, 2016.
32. Wootton R, Geissbuhler A, Jethwani K, et al. Long-running telemedicine networks delivering humanitarian services: experience, performance and scientific output. Bull World Health Organ. 2007 May;85(5):341-347. 
33. Wootton R. Telemedicine support for the developing world. J Telemed Telecare. 2008; 14(3): 109-114. 

Chris Steelman can be contacted at csteelman@x-rayintl.org.