ATS REPORTS Gaps in Capacity for Respiratory Care in Developing Countries Nigeria as a Case Study Daniel Obaseki1, Bamidele Adeniyi2, Tolulope Kolawole3, Cajetan Onyedum4, and Gregory Erhabor1 1
Department of Medicine, Obafemi Awolowo University, Ile-Ife, Osun State, Nigeria; 2Department of Medicine, Federal Medical Centre, Owo, Ondo State, Nigeria; 3Department of Medicine, Federal Teaching Hospital, Ido-Ekiti, Ekiti State, Nigeria; and 4Department of Medicine, University of Nigeria, Enugu Campus, Enugu State, Nigeria
Abstract There are unmet needs for respiratory medical care in developing countries. We sought to evaluate the quality and capacity for respiratory care in low- and lower-middle-income countries, using Nigeria as a case study. We obtained details of the respiratory practice of consultants and senior residents (fellows) in respiratory medicine in Nigeria via a semistructured questionnaire administered to physician attendees at the 2013 National Congress of the Nigerian Thoracic Society. Out of 76 society-registered members, 48 attended the congress, 40 completed the questionnaire, and 35 provided complete data (73% adjusted response rate). Respondents provided information on the process and costs of respiratory medicine training and facility, equipment, and supply capacities at the institutions they represented. Approximately 83% reported working at a tertiary level (teaching) hospital; 91% reported capacity for sputum smear analysis for acid alcohol–fast bacilli, 37%
for GeneXpert test cartridges, and 20% for BACTEC liquid sputum culture. Only 34% of respondents could perform full spirometry on patients, and none had the capacity for performing a methacholine challenge test or for measuring the diffusion capacity for carbon monoxide. We estimated the proportion of registered respiratory physicians to the national population at 1 per 2.3 million individuals. Thirteen states with an estimated combined population of 57.7 million offer no specialist respiratory services. Barriers to development of this capacity include the high cost of training. We conclude that substantial gaps exist in the capacity and quality of respiratory care in Nigeria, a pattern that probably mirrors most of sub-Saharan Africa and other countries of similar economic status. Health policy makers should address these gaps systematically. Keywords: capacity building; education; spirometry; bronchoscopy; Nigeria
(Received in original form October 1, 2014; accepted in final form February 25, 2015 ) Correspondence and requests for reprints should be addressed to Daniel Obaseki, M.D., M.P.H., Obafemi Awolowo University, Medicine, Ife-Ibadan Expressway, Faculty of Clinical Sciences, Ile-Ife, Osun, Nigeria, 282220. E-mail: [email protected] This article has an online supplement, which is accessible from this issue’s table of contents at www.atsjournals.org Ann Am Thorac Soc Vol 12, No 4, pp 591–598, Apr 2015 Copyright © 2015 by the American Thoracic Society DOI: 10.1513/AnnalsATS.201410-443AR Internet address: www.atsjournals.org
Respiratory diseases constitute a major proportion of the global burden of human disease (1). In a recent report, respiratory diseases, notably lower respiratory tract infections, chronic obstructive pulmonary disease, and lung cancer, rank among the five leading categories of diseases causing death worldwide. Nearly 80% of deaths due to noncommunicable chronic respiratory diseases worldwide occur in low- and middle-income countries (2, 3). In an analysis of 23 countries that account for 80% of these deaths, the Global Burden of Disease study estimated that Nigeria has one of the highest age-standardized death ATS Reports
rates from chronic respiratory diseases in sub-Saharan Africa (4). In addition, HIV/ AIDS and HIV-associated opportunistic respiratory infections continue to challenge the Nigerian healthcare system. However, there is a paucity of medical personnel with specialist training in respiratory medicine. As a result, general practitioners often take responsibility for managing patients with core respiratory conditions (5). The need to build capacity and support education in respiratory care is attaining recognition in many developing countries, especially in sub-Saharan Africa. This is largely due to a growing recognition of the burden of chronic noninfectious respiratory disease in
addition to the previously recognized burden of respiratory infections, especially tuberculosis (TB) (3, 6, 7). Previous studies have shown gaps in the management of specific respiratory diseases in resource-constrained settings (5, 8), but none has examined the quality and capacity for respiratory specialty practice in low-income countries. To encourage policies that can improve access to quality respiratory care, it is important to understand these gaps. The aim of the current study was to assess the quality, capacity, and resources available for the practice of specialist respiratory care in Nigeria as a case study for sub-Saharan 591
ATS REPORTS African countries and for developing countries in general.
specialist training in respiratory medicine, and responsible public health policies. Study Design and Participants
Methods
A written questionnaire was administered to Nigerian physicians who attended the November 2013 Annual National Congress of the Society, which was held in Ile-Ife, Osun State, southwest Nigeria. Participants included consultants (attending physicians) who have completed specialized training in respiratory medicine and senior residents (fellows) who were currently training in respiratory medicine. The training pathway to attainment of consultant status in Nigeria is detailed in the online supplement.
Setting and Organizational Support
This cross-sectional study was conducted in Nigeria with the approval and support of the Nigerian Thoracic Society. Nigeria is categorized by the World Bank as a lower middle income country (gross national income per capita, $5,360 in 2013) (9). The Nigerian Thoracic Society is the recognized professional association of adult and pediatric respiratory physicians and thoracic surgeons in Nigeria. The association’s overriding mission is to champion the practice of high quality and affordable respiratory care in the country. The society holds annual scientific conferences to encourage research, 4˚0'0"E
Study Questionnaire
Participants were administered a semistructured and pretested questionnaire designed to gather information on current respiratory 8˚0'0"E
medicine training and practice. The pretesting comprised initial selfadministration of the questionnaire to a small group of physicians to check for consistency, flow, and clarity of the questions. We used the feedback received from this process to modify the questionnaire as appropriate. The revised questionnaire included queries regarding level of training and the availability of equipment, facilities, and services for respiratory care. A copy of the questionnaire is included in the online supplement. Competencies were categorized into “essential” and “preferred.” Essential competencies are those skills and institutional capacities considered mandatory to provide basic respiratory care, whereas preferred are additional skills and competencies considered useful and desirable. We also assessed the capacity of the various medical centers represented by the
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Figure 1. Map of Nigeria showing the geographic distribution of registered respiratory physicians and respondents to the survey. Nigeria has 36 states and a Federal Capital Territory (FCT).
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ATS REPORTS respondents using the benchmarks set by the British Thoracic Society for respiratory practice. In addition to the data collected, we obtained a copy of the official list and contacts of registered members of the Nigerian Thoracic Society to assess response rates and external validity of the data collected. We verified the current institutions and locations of registered physicians through direct inquiry via phone calls. Estimation of Costs of Training
We estimated the costs of specialist training in respiratory medicine based on information provided by the department of clinical service of Obafemi Awolowo University Teaching Hospital, Ile-Ife, Nigeria. We complemented this information with further details obtained directly from interaction with resident doctors presently undergoing the training. The details include the cost of update courses, conferences, examinations, salaries, external rotation, practicing license, books, and other supplies. Data Analysis
The data were analyzed using Stata version 11.2 (10). Simple frequency tables were used to determine the proportion of respondents who responded affirmatively to each of the questionnaire items. Only questionnaires with complete data were included in the analysis.
Table 1. Description of survey participants Variables
Category
N (%)
Senior Registrar (Respiratory) Consultant Adult Respiratory Physician Consultant Respiratory Pediatrician Consultant Cardiothoracic Surgeon
12 (34) 17 (49) 4 (11)
Duration of practice since primary medical qualification, yr
1–5 6–10 11–15 16–20 .20
3 (9) 8 (23) 10 (29) 4 (11) 10 (29)
Setting of practice
State hospital Federal medical center Federal teaching hospital Private hospital
1 (3) 5 (14) 29 (83) 0
Staff grade
Table 1 shows the general characteristics of the respondents, including the setting of medical practice and years since primary medical qualification. Among the 35 respondents, 83% reported working in a tertiary level (teaching) hospital, and 69% of all the respondents had upwards of 10 years of practice since graduation from medical school.
2 (6)
Table 2 shows the responses to questions regarding equipment, facilities, and capacities in the medical centers represented by the respondents, categorized into essential and preferred. Altogether, 91% of the respondents reported access to resources for sputum smear analysis to detect acid alcohol–fast bacilli (AAFB), 37% for GeneXpert test cartridges, and 20% for BACTEC sputum culture. In addition, 17%
Table 2. Percent of survey respondents who reported access to resources for respiratory disease diagnostic studies and therapeutic interventions in Nigeria Essential Studies
%
Preferred studies
%
Results Out of a total of 76 registered members of the Nigerian Thoracic Society, 48 attended the 2013 National Congress of the Society. The questionnaire was distributed to all 48 attendees. A total of 40 questionnaires were returned, and 35 contained answers to all questions (73% adjusted response rate). Figure 1 shows the geographic distribution of respondents who submitted complete data and the states in which they work. It also shows the number of respondents from the same institution (indicated by the size of the circles). Generally, most institutions had one respondent, but some had higher representation in the survey. Except in a few states in the federation, there is usually only one tertiary hospital with specialist services in a state territory, and all specialist respiratory physicians tend to work in the same hospital. ATS Reports
Full spirometry (including expiratory and inspiratory maneuvers and respiratory muscle function testing) Ziehl Neelsen (acid-fast) staining Peak flow meters Pulse oximetry (in medical ward apart from ICU) Lowenstein-Jensen culture media BACTEC culture media GeneXpert cartridges Full functional respiratory laboratory Arterial blood gas analysis Sputum induction Pleural biopsy Therapeutic thoracentesis Chest radiography (day case investigation in clinic) Chest CT Flexible fiberoptic bronchoscopy Washings Brushings Bronchoalveolar lavage Transbronchial biopsies (blind)
34 Methacholine challenge testing Radio-allergosorbent test (RAST) Allergen skin prick testing 91 Pleurodesis 86 PleurX catheter insertion 86 Medical thoracoscopy Body plethysmography 40 CT pulmonary angiography 20 Ventilation-perfusion scanning 37 Oxygen titration testing 17 Carbon monoxide transfer factor (DLCO) 31 Flexible fiberoptic bronchoscopy 14 biopsies with fluoroscopic guidance 69 80 77
0 0 11 60 0 11 3 37 20 7 0 11
71 46 31 31 37 43
Definition of abbreviations: CT = computed tomography; ICU = intensive care unit. “Essential” competencies were those skills and institutional capacity considered mandatory to provide basic respiratory care, whereas “preferred” are additional skills and competencies we considered useful and desirable if there are sufficient resources available.
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ATS REPORTS reported access to a respiratory diagnostic laboratory. Approximately 34% could perform full spirometric evaluation, and 31% had access to equipment for determination of arterial pH and blood gas tensions. Only 7% had the capacity to perform an oxygen titration test (oxygen saturation assessment during a 6-minwalk test). None had the capacity for a methacholine challenge testing or for measurement of the diffusion capacity for carbon monoxide. We also assessed capacity for respiratory care based on the standards of the British Thoracic Society (Table 3). Only 11% of the respondents reported having staffed specialist respiratory wards in their hospitals; 43% had facility for bronchoscopy and pleural investigations.
Only 3% reported ready access to computer monitor display of electronic medical records with computer screens and an efficient imaging display service in the clinic. None of the respondents reported having facilities for polysomnographic sleep studies, continuous positive airway pressure, or ambulatory oxygen services. Few respondents had expertise and facilities for basic or advanced interventional pulmonary services. To estimate the costs of training a respiratory physician, we considered the cost of qualifying examinations, courses, conference attendance, salaries, books, supplies, external postings, and licensing fees. Although the costs of examinations, courses, conferences, external postings, and salaries are generally borne by the
sponsoring or training institution, trainees may be required to bear the other costs in some centers. Because basic and specialist training is linked as a whole and performed exclusively in accredited institutions, we evaluated the entire package of costs, from entrance for residency to completion of subspecialty training, a process that requires a minimum of 6 years. On average, the estimated direct and indirect cost of training a respiratory physician with competencies in modern diagnostics and a contemporary standard of practice is upwards of $165,000 U.S. by our most conservative estimate (Table 4). Concerning the ratio and spread of respiratory physicians in Nigeria, we estimated a proportion of 1 registered respiratory specialist per 2.3 million
Table 3. Percent of survey respondents who reported access to resources recommended by the British Thoracic Society standards for respiratory practice Setting
BTS Standards
%
Inpatients
Facilities for day-case investigation and care High-dependency unit and step-down wards with access to noninvasive ventilation Endoscopy unit for bronchoscopic and pleural investigations Easy access to ultrasound for pleural procedures Fully staffed specialist respiratory ward
37 14 43 46 11
Outpatient services
Dedicated outpatient unit with natural lighting and of sufficient size for members of the multidisciplinary team Quiet room for the bereaved and to give bad news/counseling Seminar room for unit meetings and MDT meetings Lung function service in each clinic, with support from a fully equipped lung function laboratory High-definition computer screens in each clinic room for access to picture archiving and patient data communication system and an efficient imaging department in close proximity Relevant pharmacy service Immediately bookable slots for endoscopy and all imaging Adequate secretarial and clerical staff, who are trained in running respiratory services Flexible appointment system
34
Diagnostic and therapeutic facilities
Bronchoscopy suite with facilities for advanced diagnostic and therapeutic procedures (endobronchial ultrasound, stenting, laser therapy, etc.) Fully equipped and staffed lung function laboratory with facilities to perform routine and highly specialized investigations Investigation, treatment, and ongoing support of patients with sleep-related breathing disorders, including equipment for CPAP and ongoing technical and clinical support Full polysomnography, dedicated sleep beds, and soundproofed facilities for undertaking sleep tests Assessment of causes of alveolar hypoventilation (neuromuscular, obesity, or pulmonary in origin) Provision of domiciliary oxygen, including clinical and technical support Ambulatory and long-term oxygen and inhaled therapy assessment service Facilities and beds for the provision of expert end-of-life care by the respiratory physician
11 54 20 3 57 23 3 37 14 9 0 0 0 17 0 6
Definition of abbreviations: BTS = British Thoracic Society; CPAP = continuous positive airway pressure; MDT = multidisciplinary team.
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ATS REPORTS Table 4. Estimated cost of training a respiratory specialist physician in Nigeria Item
Rate (₦)
Duration
Total (₦)
Books and supplies 355,450 per stage of training 3 Segments (primary, part 1, part 2) 1,066,350 Examinations* 250,000 per stage per attempt 3 Stages and 2 examination attempts 1,500,000 Post-graduate courses (primary/part 250,000 per course per stage 6 Courses 1,500,000 1/part 2a & 2b)* Salaries (Registrar) 262,850 per month 3 yr (36 mo) 9,462,600 Salaries (Senior Registrar) 328,400 per month 3 yr (36 mo) 11,822,400 Thesis 650,000 — 650,000 International conference 683,620 — 683,620 Attendance at the Nigerian Thoracic 190,000 2 yr 380,000 Society annual conference External rotations and offshore posting 2,550,000 — 2,550,000 Annual college fees (post part 1) 50,000 3 yr* 150,000 Annual medical license 10,000 6 yr* 60,000 TOTAL 29,824,970 (US $165,786) Definition of abbreviation: ₦ = Naira. Unless otherwise indicated, the monetary figures are in Nigerian naira. 1 naira = USD 0.0056, CAD 0.0064, GBP 0.0035, Euro 0.0045 (as of December 12, 2014; www.xe.com). Estimates are based on current rates at the time of analysis and are subject to change based on prevailing inflation rates and currency exchange rate. These expenses are usually borne by the sponsoring institution but there are variations between centers in the details. There are two post-graduate medical colleges (West African College of Physicians, and National Postgraduate Medical College of Nigeria) and three levels of postgraduate medical training in Nigeria: primary, part 1, part 2. A pass in the primary examinations qualifies for commencement of residency training, a pass in part 1 examinations after 3 years of training qualifies for senior residency training, and a pass in the part 2 examinations after another 3 years of training qualifies for fellowship of the relevant post-graduate college. 2a is a course on research methods; 2b is a course on health management. *Estimates are based on two attempts at the examinations and two attendances of courses in one of the two post-graduate examination colleges, which is the minimum. However, the above examination and course attendance costs may be doubled if a candidate applies to both post-graduate examination colleges. Candidates often apply for the examination of both post-graduate colleges to improve their chance of passing to the next level of training.
individuals, based on the current national census estimate of Nigeria’s population (177 million) (11). Although many of Nigeria’s 36 states had only one registered respiratory physician, 13 states (with an estimated combined population of 57.7 million) had no recognized respiratory physician at the time of this survey.
Discussion As recognition grows of the incidence and prevalence of chronic respiratory disease in low- and middle-income countries, so does recognition of the need for trained respiratory clinicians and certain resources to respond to this epidemic. Several previously published studies have examined gaps in the approach to management of specific respiratory conditions such as asthma in developing countries (5, 8). But after a careful and systematic review of the literature, we did not find any study that has examined, in a broad sense, the quality and capacity for the practice of respiratory medicine in a country or geographic region. In this survey, we gathered information on the number and capacity of respiratory clinicians in Nigeria, a lower-middle-income country in sub-Saharan Africa (9). We found a marked deficiency in the number of respiratory physicians in Nigeria. ATS Reports
With an estimated population of 177 million and a substantial burden of chronic respiratory diseases (12), Nigeria is served by 76 registered respiratory physicians (one respiratory physician per 2.3 million population). In comparison, the United Kingdom, with a national population of 64 million (13), is served by more than 1,000 respiratory physicians (14). According to a recent report by the International Monetary Fund, Nigeria has the largest economy in sub-Saharan Africa (Figure 2), being the country with the largest gross domestic product (15). Because gross domestic product correlates with national health spending (16), we speculate that apart from South Africa, there is probably a similar or more severe dearth of respiratory physicians in other sub-Saharan African countries. Equipment, supply, and facility resources for expert respiratory care are similarly limited. As might be expected, given the public health emphasis in Nigeria and other similar countries on combating TB and HIV infection, we found a substantial capacity for microbiological investigation of infectious respiratory diseases, including TB. However, there are notable gaps in the capacity for basic respiratory diagnostic procedures and for expert management of patients afflicted by
noninfectious chronic respiratory diseases. Using as a reference standard, the minimum resources required by the British Thoracic Society for a district general hospital to provide a high-quality respiratory service, we found a low capacity in Nigeria’s tertiary hospitals for competitive inpatient, outpatient, and diagnostic services (17). The capability to perform full lung function and bronchoscopic services is limited. Lung function laboratories to assess physiologic abnormalities and bronchoscopy facilities to characterize both airway and parenchymal processes in a specific manner are cardinal features of centers of excellence in respiratory care globally. Currently, only five teaching hospitals have full accreditation of the Nigerian post-graduate medical college to train respiratory physicians, and they are all public institutions (18). On average, two or three trainees graduate from these programs each year to become specialist respiratory physicians in Nigeria (personal communication, G. Erhabor, chief examiner, West African College of Physicians). Expansion of respiratory disease training programs within Nigeria is inhibited by the high cost of training (Table 4). As a result, healthcare institutions in Nigeria and other similar countries often prefer to deploy generalist 595
Countries
ATS REPORTS
Nigeria South Africa Angola Kenya Ethiopia Tanzania Côte d’Ivoire Democratic Republic of the Congo Cameroon Ghana Zambia Uganda Gabon Mozambique Botswana Chad Senegal Republic of Congo Burkina Faso Zimbabwe Equatorial Guinea Mauritius South Sudan Mali Namibia Madagascar Benin Niger Rwanda Guinea Sierra Leone Togo Malawi 0
100
200
300
400
500
600
700
Gross Domestic Product (US Dollar - Billions)
Figure 2. Gross domestic product of some sub-Saharan African countries (U.S. dollars, in billions).
physicians to provide basic nonspecialist services, rather than engage in the long, arduous, and expensive process of specialist training. This tendency has serious ramifications for the quality of care received by patients in need of complex or advanced respiratory care. The risk of misdiagnosis, undertreatment, or mismanagement of respiratory conditions is particularly high if the care of patients with complex or less common conditions is left entirely to general practitioners. Other strategies have been developed to fill the gap in respiratory care in developing countries. Of note is an integrated practical approach for lung health developed by the World Health Organization that is non–physician based (19). This program aims to expand the current TB treatment strategies at primary care institutions to incorporate screening for lung diseases and the provision of basic respiratory care and treatments. However, such a program’s success hinges on an appropriate and responsive referral system for expert secondary and tertiary care, where necessary. 596
There is a weak participation in respiratory care from the private healthcare sector. Consistent with the absence of any survey respondent from a private healthcare institution, the society’s official register indicates only one member working in a private specialist respiratory care facility. Although we are uncertain about the number of graduating trainees who leave the country to practice elsewhere, professional relocation is unlikely to account for the low numbers of respiratory physicians in Nigeria or sub-Saharan Africa, as the annual turnover of specialist respiratory physicians is low in the first place. One possible approach for increasing the number of respiratory specialists in Nigeria might be to combine respiratory medicine training with critical care training. This approach appears to be gaining traction elsewhere. The General Medical Council of the United Kingdom has recently approved a dual-training pathway in intensive care and respiratory medicine in line with current practice in the United States (20, 21). In contrast, in Nigeria and
many other low- and lower-middle-income countries, respiratory medicine is a separate specialty from intensive care medicine. Patients in need of intensive care are often managed by anesthesiologists alone or jointly with respiratory physicians. This separation likely is a result of several convergent factors. First, the lack of ability for diagnosis of noninfectious respiratory diseases (either due to manpower or equipment deficiencies) translates into an inability to determine what is required at a critical level to support respiratory patients. Second, the development of intensive care medicine in developing countries is often based on the need for postsurgical support, leading to the involvement of anesthesiologists as the primary team leaders. Separation of the two specialties mirrors the historical development of intensive care medicine in the developed world, which originally grew out of the ability to provide ventilatory support to postoperative chest surgery patients in the 1950s and early 1960s (22, 23). Perhaps this approach of strictly
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ATS REPORTS separating the two specialties should be reconsidered in light of the pressing need to increase physician specialist capacity in both respiratory and critical care medicine. As the world grapples with the growing burden of chronic respiratory diseases and a transition in disease pattern in developing countries from infectious to noncommunicable diseases (1, 4), there is a pressing need for policy makers to implement programs that support capacity development in low- and middle-income countries. This capacity development includes goals to develop in-country training capacity as well as the development of the necessary infrastructure for supporting trained respiratory physicians, assistants, and therapists to practice effectively. This infrastructure must soon extend beyond physiologic and bronchoscopic testing capacity to the development of radiologic imaging centers, pathologic training and laboratory capacity, nursing expertise in respiratory care, oxygen delivery, rehabilitation medicine, and access to affordable pharmacologic agents for symptomatic treatment. Additional transfer of expertise from developed to developing countries is also needed. The Nigerian Thoracic Society recommends development of opportunities for rotation of Nigerian respiratory medicine residents to teaching hospitals in developed countries for intensive
exposure to world-class teaching and medical care. Our study is probably the first to estimate the capacity for respiratory care and practice in a developing country and provides previously unavailable information. Nonetheless, there are weaknesses in our study design. To estimate the number of respiratory specialists in Nigeria, we counted registered specialists and members of the Nigerian Thoracic Society. This approach may have underestimated the total number of formally trained respiratory specialists in the country. However, we think it is unlikely that an important fraction of well-trained respiratory practitioners in Nigeria are not registered members of the society or known to members of the Society. Other limitations in study design might have resulted in an overestimate of respiratory specialist capacity. Our assessment of respiratory care resources was not exhaustive, as some basic respiratory tools, such as diagnostic thoracentesis and non-TB microbiology, were not assessed. We cannot rule out a reporting bias because we did not sample systematically at a facility level, and some centers had multiple respondents. Institutions located near the venue of the scientific congress had a higher representation in the survey. However it is worth noting that the density of respiratory physicians per state is higher in southwest Nigeria, where the survey was held. Additionally, our inventory of respiratory care resources is based on self-report by
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participating physicians. We did not conduct a direct on-site audit of facilities or survey of hospitals or clinics. We believe, however, that these findings are credible, because the details were provided by specialists who are directly involved in the use of these services for patient care. Anecdotal reports from respiratory physicians in Nigeria and many developing countries also agree with our findings. In conclusion, our study confirms that there are remarkable gaps in the quality and capacity for respiratory care in Nigeria, which likely mirrors the situation in other countries of comparable economic status. These gaps require urgent strategic and concerted systematic improvement. Our findings call for a visionary effort to advance respiratory care in developing countries as the burden due to lung diseases attains significant proportions. There is a need to develop policies that support the provision of basic and advanced facilities for respiratory diagnosis and an integrated approach to respiratory care that is sustainable in developing economies. n Author disclosures are available with the text of this article at www.atsjournals.org. Acknowledgment: The authors thank the leadership of the Nigerian Thoracic Society for supporting the conduct of this survey. They also thank Professor Fatiu Arogundade of the Department of Medicine, Obafemi Awolowo University, Professor Sonia Buist of Oregon Health and Sciences University, and Professor Jane Carter of Brown University for their helpful comments in the writing of this manuscript.
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Department of Medicine, Obafemi Awolowo University, Ile-Ife, Osun State, Nigeria; 2Department of Medicine, Federal Medical Centre, Owo, Ondo State, Nigeria; 3Department of Medicine, Federal Teaching Hospital, Ido-Ekiti, Ekiti State, Nigeria; and 4Department of Medicine, University of Nigeria, Enugu Campus, Enugu State, Nigeria
Abstract There are unmet needs for respiratory medical care in developing countries. We sought to evaluate the quality and capacity for respiratory care in low- and lower-middle-income countries, using Nigeria as a case study. We obtained details of the respiratory practice of consultants and senior residents (fellows) in respiratory medicine in Nigeria via a semistructured questionnaire administered to physician attendees at the 2013 National Congress of the Nigerian Thoracic Society. Out of 76 society-registered members, 48 attended the congress, 40 completed the questionnaire, and 35 provided complete data (73% adjusted response rate). Respondents provided information on the process and costs of respiratory medicine training and facility, equipment, and supply capacities at the institutions they represented. Approximately 83% reported working at a tertiary level (teaching) hospital; 91% reported capacity for sputum smear analysis for acid alcohol–fast bacilli, 37%
for GeneXpert test cartridges, and 20% for BACTEC liquid sputum culture. Only 34% of respondents could perform full spirometry on patients, and none had the capacity for performing a methacholine challenge test or for measuring the diffusion capacity for carbon monoxide. We estimated the proportion of registered respiratory physicians to the national population at 1 per 2.3 million individuals. Thirteen states with an estimated combined population of 57.7 million offer no specialist respiratory services. Barriers to development of this capacity include the high cost of training. We conclude that substantial gaps exist in the capacity and quality of respiratory care in Nigeria, a pattern that probably mirrors most of sub-Saharan Africa and other countries of similar economic status. Health policy makers should address these gaps systematically. Keywords: capacity building; education; spirometry; bronchoscopy; Nigeria
(Received in original form October 1, 2014; accepted in final form February 25, 2015 ) Correspondence and requests for reprints should be addressed to Daniel Obaseki, M.D., M.P.H., Obafemi Awolowo University, Medicine, Ife-Ibadan Expressway, Faculty of Clinical Sciences, Ile-Ife, Osun, Nigeria, 282220. E-mail: [email protected] This article has an online supplement, which is accessible from this issue’s table of contents at www.atsjournals.org Ann Am Thorac Soc Vol 12, No 4, pp 591–598, Apr 2015 Copyright © 2015 by the American Thoracic Society DOI: 10.1513/AnnalsATS.201410-443AR Internet address: www.atsjournals.org
Respiratory diseases constitute a major proportion of the global burden of human disease (1). In a recent report, respiratory diseases, notably lower respiratory tract infections, chronic obstructive pulmonary disease, and lung cancer, rank among the five leading categories of diseases causing death worldwide. Nearly 80% of deaths due to noncommunicable chronic respiratory diseases worldwide occur in low- and middle-income countries (2, 3). In an analysis of 23 countries that account for 80% of these deaths, the Global Burden of Disease study estimated that Nigeria has one of the highest age-standardized death ATS Reports
rates from chronic respiratory diseases in sub-Saharan Africa (4). In addition, HIV/ AIDS and HIV-associated opportunistic respiratory infections continue to challenge the Nigerian healthcare system. However, there is a paucity of medical personnel with specialist training in respiratory medicine. As a result, general practitioners often take responsibility for managing patients with core respiratory conditions (5). The need to build capacity and support education in respiratory care is attaining recognition in many developing countries, especially in sub-Saharan Africa. This is largely due to a growing recognition of the burden of chronic noninfectious respiratory disease in
addition to the previously recognized burden of respiratory infections, especially tuberculosis (TB) (3, 6, 7). Previous studies have shown gaps in the management of specific respiratory diseases in resource-constrained settings (5, 8), but none has examined the quality and capacity for respiratory specialty practice in low-income countries. To encourage policies that can improve access to quality respiratory care, it is important to understand these gaps. The aim of the current study was to assess the quality, capacity, and resources available for the practice of specialist respiratory care in Nigeria as a case study for sub-Saharan 591
ATS REPORTS African countries and for developing countries in general.
specialist training in respiratory medicine, and responsible public health policies. Study Design and Participants
Methods
A written questionnaire was administered to Nigerian physicians who attended the November 2013 Annual National Congress of the Society, which was held in Ile-Ife, Osun State, southwest Nigeria. Participants included consultants (attending physicians) who have completed specialized training in respiratory medicine and senior residents (fellows) who were currently training in respiratory medicine. The training pathway to attainment of consultant status in Nigeria is detailed in the online supplement.
Setting and Organizational Support
This cross-sectional study was conducted in Nigeria with the approval and support of the Nigerian Thoracic Society. Nigeria is categorized by the World Bank as a lower middle income country (gross national income per capita, $5,360 in 2013) (9). The Nigerian Thoracic Society is the recognized professional association of adult and pediatric respiratory physicians and thoracic surgeons in Nigeria. The association’s overriding mission is to champion the practice of high quality and affordable respiratory care in the country. The society holds annual scientific conferences to encourage research, 4˚0'0"E
Study Questionnaire
Participants were administered a semistructured and pretested questionnaire designed to gather information on current respiratory 8˚0'0"E
medicine training and practice. The pretesting comprised initial selfadministration of the questionnaire to a small group of physicians to check for consistency, flow, and clarity of the questions. We used the feedback received from this process to modify the questionnaire as appropriate. The revised questionnaire included queries regarding level of training and the availability of equipment, facilities, and services for respiratory care. A copy of the questionnaire is included in the online supplement. Competencies were categorized into “essential” and “preferred.” Essential competencies are those skills and institutional capacities considered mandatory to provide basic respiratory care, whereas preferred are additional skills and competencies considered useful and desirable. We also assessed the capacity of the various medical centers represented by the
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NIGER N CHAD
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Nasarawa Taraba Ekiti
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Figure 1. Map of Nigeria showing the geographic distribution of registered respiratory physicians and respondents to the survey. Nigeria has 36 states and a Federal Capital Territory (FCT).
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ATS REPORTS respondents using the benchmarks set by the British Thoracic Society for respiratory practice. In addition to the data collected, we obtained a copy of the official list and contacts of registered members of the Nigerian Thoracic Society to assess response rates and external validity of the data collected. We verified the current institutions and locations of registered physicians through direct inquiry via phone calls. Estimation of Costs of Training
We estimated the costs of specialist training in respiratory medicine based on information provided by the department of clinical service of Obafemi Awolowo University Teaching Hospital, Ile-Ife, Nigeria. We complemented this information with further details obtained directly from interaction with resident doctors presently undergoing the training. The details include the cost of update courses, conferences, examinations, salaries, external rotation, practicing license, books, and other supplies. Data Analysis
The data were analyzed using Stata version 11.2 (10). Simple frequency tables were used to determine the proportion of respondents who responded affirmatively to each of the questionnaire items. Only questionnaires with complete data were included in the analysis.
Table 1. Description of survey participants Variables
Category
N (%)
Senior Registrar (Respiratory) Consultant Adult Respiratory Physician Consultant Respiratory Pediatrician Consultant Cardiothoracic Surgeon
12 (34) 17 (49) 4 (11)
Duration of practice since primary medical qualification, yr
1–5 6–10 11–15 16–20 .20
3 (9) 8 (23) 10 (29) 4 (11) 10 (29)
Setting of practice
State hospital Federal medical center Federal teaching hospital Private hospital
1 (3) 5 (14) 29 (83) 0
Staff grade
Table 1 shows the general characteristics of the respondents, including the setting of medical practice and years since primary medical qualification. Among the 35 respondents, 83% reported working in a tertiary level (teaching) hospital, and 69% of all the respondents had upwards of 10 years of practice since graduation from medical school.
2 (6)
Table 2 shows the responses to questions regarding equipment, facilities, and capacities in the medical centers represented by the respondents, categorized into essential and preferred. Altogether, 91% of the respondents reported access to resources for sputum smear analysis to detect acid alcohol–fast bacilli (AAFB), 37% for GeneXpert test cartridges, and 20% for BACTEC sputum culture. In addition, 17%
Table 2. Percent of survey respondents who reported access to resources for respiratory disease diagnostic studies and therapeutic interventions in Nigeria Essential Studies
%
Preferred studies
%
Results Out of a total of 76 registered members of the Nigerian Thoracic Society, 48 attended the 2013 National Congress of the Society. The questionnaire was distributed to all 48 attendees. A total of 40 questionnaires were returned, and 35 contained answers to all questions (73% adjusted response rate). Figure 1 shows the geographic distribution of respondents who submitted complete data and the states in which they work. It also shows the number of respondents from the same institution (indicated by the size of the circles). Generally, most institutions had one respondent, but some had higher representation in the survey. Except in a few states in the federation, there is usually only one tertiary hospital with specialist services in a state territory, and all specialist respiratory physicians tend to work in the same hospital. ATS Reports
Full spirometry (including expiratory and inspiratory maneuvers and respiratory muscle function testing) Ziehl Neelsen (acid-fast) staining Peak flow meters Pulse oximetry (in medical ward apart from ICU) Lowenstein-Jensen culture media BACTEC culture media GeneXpert cartridges Full functional respiratory laboratory Arterial blood gas analysis Sputum induction Pleural biopsy Therapeutic thoracentesis Chest radiography (day case investigation in clinic) Chest CT Flexible fiberoptic bronchoscopy Washings Brushings Bronchoalveolar lavage Transbronchial biopsies (blind)
34 Methacholine challenge testing Radio-allergosorbent test (RAST) Allergen skin prick testing 91 Pleurodesis 86 PleurX catheter insertion 86 Medical thoracoscopy Body plethysmography 40 CT pulmonary angiography 20 Ventilation-perfusion scanning 37 Oxygen titration testing 17 Carbon monoxide transfer factor (DLCO) 31 Flexible fiberoptic bronchoscopy 14 biopsies with fluoroscopic guidance 69 80 77
0 0 11 60 0 11 3 37 20 7 0 11
71 46 31 31 37 43
Definition of abbreviations: CT = computed tomography; ICU = intensive care unit. “Essential” competencies were those skills and institutional capacity considered mandatory to provide basic respiratory care, whereas “preferred” are additional skills and competencies we considered useful and desirable if there are sufficient resources available.
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ATS REPORTS reported access to a respiratory diagnostic laboratory. Approximately 34% could perform full spirometric evaluation, and 31% had access to equipment for determination of arterial pH and blood gas tensions. Only 7% had the capacity to perform an oxygen titration test (oxygen saturation assessment during a 6-minwalk test). None had the capacity for a methacholine challenge testing or for measurement of the diffusion capacity for carbon monoxide. We also assessed capacity for respiratory care based on the standards of the British Thoracic Society (Table 3). Only 11% of the respondents reported having staffed specialist respiratory wards in their hospitals; 43% had facility for bronchoscopy and pleural investigations.
Only 3% reported ready access to computer monitor display of electronic medical records with computer screens and an efficient imaging display service in the clinic. None of the respondents reported having facilities for polysomnographic sleep studies, continuous positive airway pressure, or ambulatory oxygen services. Few respondents had expertise and facilities for basic or advanced interventional pulmonary services. To estimate the costs of training a respiratory physician, we considered the cost of qualifying examinations, courses, conference attendance, salaries, books, supplies, external postings, and licensing fees. Although the costs of examinations, courses, conferences, external postings, and salaries are generally borne by the
sponsoring or training institution, trainees may be required to bear the other costs in some centers. Because basic and specialist training is linked as a whole and performed exclusively in accredited institutions, we evaluated the entire package of costs, from entrance for residency to completion of subspecialty training, a process that requires a minimum of 6 years. On average, the estimated direct and indirect cost of training a respiratory physician with competencies in modern diagnostics and a contemporary standard of practice is upwards of $165,000 U.S. by our most conservative estimate (Table 4). Concerning the ratio and spread of respiratory physicians in Nigeria, we estimated a proportion of 1 registered respiratory specialist per 2.3 million
Table 3. Percent of survey respondents who reported access to resources recommended by the British Thoracic Society standards for respiratory practice Setting
BTS Standards
%
Inpatients
Facilities for day-case investigation and care High-dependency unit and step-down wards with access to noninvasive ventilation Endoscopy unit for bronchoscopic and pleural investigations Easy access to ultrasound for pleural procedures Fully staffed specialist respiratory ward
37 14 43 46 11
Outpatient services
Dedicated outpatient unit with natural lighting and of sufficient size for members of the multidisciplinary team Quiet room for the bereaved and to give bad news/counseling Seminar room for unit meetings and MDT meetings Lung function service in each clinic, with support from a fully equipped lung function laboratory High-definition computer screens in each clinic room for access to picture archiving and patient data communication system and an efficient imaging department in close proximity Relevant pharmacy service Immediately bookable slots for endoscopy and all imaging Adequate secretarial and clerical staff, who are trained in running respiratory services Flexible appointment system
34
Diagnostic and therapeutic facilities
Bronchoscopy suite with facilities for advanced diagnostic and therapeutic procedures (endobronchial ultrasound, stenting, laser therapy, etc.) Fully equipped and staffed lung function laboratory with facilities to perform routine and highly specialized investigations Investigation, treatment, and ongoing support of patients with sleep-related breathing disorders, including equipment for CPAP and ongoing technical and clinical support Full polysomnography, dedicated sleep beds, and soundproofed facilities for undertaking sleep tests Assessment of causes of alveolar hypoventilation (neuromuscular, obesity, or pulmonary in origin) Provision of domiciliary oxygen, including clinical and technical support Ambulatory and long-term oxygen and inhaled therapy assessment service Facilities and beds for the provision of expert end-of-life care by the respiratory physician
11 54 20 3 57 23 3 37 14 9 0 0 0 17 0 6
Definition of abbreviations: BTS = British Thoracic Society; CPAP = continuous positive airway pressure; MDT = multidisciplinary team.
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ATS REPORTS Table 4. Estimated cost of training a respiratory specialist physician in Nigeria Item
Rate (₦)
Duration
Total (₦)
Books and supplies 355,450 per stage of training 3 Segments (primary, part 1, part 2) 1,066,350 Examinations* 250,000 per stage per attempt 3 Stages and 2 examination attempts 1,500,000 Post-graduate courses (primary/part 250,000 per course per stage 6 Courses 1,500,000 1/part 2a & 2b)* Salaries (Registrar) 262,850 per month 3 yr (36 mo) 9,462,600 Salaries (Senior Registrar) 328,400 per month 3 yr (36 mo) 11,822,400 Thesis 650,000 — 650,000 International conference 683,620 — 683,620 Attendance at the Nigerian Thoracic 190,000 2 yr 380,000 Society annual conference External rotations and offshore posting 2,550,000 — 2,550,000 Annual college fees (post part 1) 50,000 3 yr* 150,000 Annual medical license 10,000 6 yr* 60,000 TOTAL 29,824,970 (US $165,786) Definition of abbreviation: ₦ = Naira. Unless otherwise indicated, the monetary figures are in Nigerian naira. 1 naira = USD 0.0056, CAD 0.0064, GBP 0.0035, Euro 0.0045 (as of December 12, 2014; www.xe.com). Estimates are based on current rates at the time of analysis and are subject to change based on prevailing inflation rates and currency exchange rate. These expenses are usually borne by the sponsoring institution but there are variations between centers in the details. There are two post-graduate medical colleges (West African College of Physicians, and National Postgraduate Medical College of Nigeria) and three levels of postgraduate medical training in Nigeria: primary, part 1, part 2. A pass in the primary examinations qualifies for commencement of residency training, a pass in part 1 examinations after 3 years of training qualifies for senior residency training, and a pass in the part 2 examinations after another 3 years of training qualifies for fellowship of the relevant post-graduate college. 2a is a course on research methods; 2b is a course on health management. *Estimates are based on two attempts at the examinations and two attendances of courses in one of the two post-graduate examination colleges, which is the minimum. However, the above examination and course attendance costs may be doubled if a candidate applies to both post-graduate examination colleges. Candidates often apply for the examination of both post-graduate colleges to improve their chance of passing to the next level of training.
individuals, based on the current national census estimate of Nigeria’s population (177 million) (11). Although many of Nigeria’s 36 states had only one registered respiratory physician, 13 states (with an estimated combined population of 57.7 million) had no recognized respiratory physician at the time of this survey.
Discussion As recognition grows of the incidence and prevalence of chronic respiratory disease in low- and middle-income countries, so does recognition of the need for trained respiratory clinicians and certain resources to respond to this epidemic. Several previously published studies have examined gaps in the approach to management of specific respiratory conditions such as asthma in developing countries (5, 8). But after a careful and systematic review of the literature, we did not find any study that has examined, in a broad sense, the quality and capacity for the practice of respiratory medicine in a country or geographic region. In this survey, we gathered information on the number and capacity of respiratory clinicians in Nigeria, a lower-middle-income country in sub-Saharan Africa (9). We found a marked deficiency in the number of respiratory physicians in Nigeria. ATS Reports
With an estimated population of 177 million and a substantial burden of chronic respiratory diseases (12), Nigeria is served by 76 registered respiratory physicians (one respiratory physician per 2.3 million population). In comparison, the United Kingdom, with a national population of 64 million (13), is served by more than 1,000 respiratory physicians (14). According to a recent report by the International Monetary Fund, Nigeria has the largest economy in sub-Saharan Africa (Figure 2), being the country with the largest gross domestic product (15). Because gross domestic product correlates with national health spending (16), we speculate that apart from South Africa, there is probably a similar or more severe dearth of respiratory physicians in other sub-Saharan African countries. Equipment, supply, and facility resources for expert respiratory care are similarly limited. As might be expected, given the public health emphasis in Nigeria and other similar countries on combating TB and HIV infection, we found a substantial capacity for microbiological investigation of infectious respiratory diseases, including TB. However, there are notable gaps in the capacity for basic respiratory diagnostic procedures and for expert management of patients afflicted by
noninfectious chronic respiratory diseases. Using as a reference standard, the minimum resources required by the British Thoracic Society for a district general hospital to provide a high-quality respiratory service, we found a low capacity in Nigeria’s tertiary hospitals for competitive inpatient, outpatient, and diagnostic services (17). The capability to perform full lung function and bronchoscopic services is limited. Lung function laboratories to assess physiologic abnormalities and bronchoscopy facilities to characterize both airway and parenchymal processes in a specific manner are cardinal features of centers of excellence in respiratory care globally. Currently, only five teaching hospitals have full accreditation of the Nigerian post-graduate medical college to train respiratory physicians, and they are all public institutions (18). On average, two or three trainees graduate from these programs each year to become specialist respiratory physicians in Nigeria (personal communication, G. Erhabor, chief examiner, West African College of Physicians). Expansion of respiratory disease training programs within Nigeria is inhibited by the high cost of training (Table 4). As a result, healthcare institutions in Nigeria and other similar countries often prefer to deploy generalist 595
Countries
ATS REPORTS
Nigeria South Africa Angola Kenya Ethiopia Tanzania Côte d’Ivoire Democratic Republic of the Congo Cameroon Ghana Zambia Uganda Gabon Mozambique Botswana Chad Senegal Republic of Congo Burkina Faso Zimbabwe Equatorial Guinea Mauritius South Sudan Mali Namibia Madagascar Benin Niger Rwanda Guinea Sierra Leone Togo Malawi 0
100
200
300
400
500
600
700
Gross Domestic Product (US Dollar - Billions)
Figure 2. Gross domestic product of some sub-Saharan African countries (U.S. dollars, in billions).
physicians to provide basic nonspecialist services, rather than engage in the long, arduous, and expensive process of specialist training. This tendency has serious ramifications for the quality of care received by patients in need of complex or advanced respiratory care. The risk of misdiagnosis, undertreatment, or mismanagement of respiratory conditions is particularly high if the care of patients with complex or less common conditions is left entirely to general practitioners. Other strategies have been developed to fill the gap in respiratory care in developing countries. Of note is an integrated practical approach for lung health developed by the World Health Organization that is non–physician based (19). This program aims to expand the current TB treatment strategies at primary care institutions to incorporate screening for lung diseases and the provision of basic respiratory care and treatments. However, such a program’s success hinges on an appropriate and responsive referral system for expert secondary and tertiary care, where necessary. 596
There is a weak participation in respiratory care from the private healthcare sector. Consistent with the absence of any survey respondent from a private healthcare institution, the society’s official register indicates only one member working in a private specialist respiratory care facility. Although we are uncertain about the number of graduating trainees who leave the country to practice elsewhere, professional relocation is unlikely to account for the low numbers of respiratory physicians in Nigeria or sub-Saharan Africa, as the annual turnover of specialist respiratory physicians is low in the first place. One possible approach for increasing the number of respiratory specialists in Nigeria might be to combine respiratory medicine training with critical care training. This approach appears to be gaining traction elsewhere. The General Medical Council of the United Kingdom has recently approved a dual-training pathway in intensive care and respiratory medicine in line with current practice in the United States (20, 21). In contrast, in Nigeria and
many other low- and lower-middle-income countries, respiratory medicine is a separate specialty from intensive care medicine. Patients in need of intensive care are often managed by anesthesiologists alone or jointly with respiratory physicians. This separation likely is a result of several convergent factors. First, the lack of ability for diagnosis of noninfectious respiratory diseases (either due to manpower or equipment deficiencies) translates into an inability to determine what is required at a critical level to support respiratory patients. Second, the development of intensive care medicine in developing countries is often based on the need for postsurgical support, leading to the involvement of anesthesiologists as the primary team leaders. Separation of the two specialties mirrors the historical development of intensive care medicine in the developed world, which originally grew out of the ability to provide ventilatory support to postoperative chest surgery patients in the 1950s and early 1960s (22, 23). Perhaps this approach of strictly
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ATS REPORTS separating the two specialties should be reconsidered in light of the pressing need to increase physician specialist capacity in both respiratory and critical care medicine. As the world grapples with the growing burden of chronic respiratory diseases and a transition in disease pattern in developing countries from infectious to noncommunicable diseases (1, 4), there is a pressing need for policy makers to implement programs that support capacity development in low- and middle-income countries. This capacity development includes goals to develop in-country training capacity as well as the development of the necessary infrastructure for supporting trained respiratory physicians, assistants, and therapists to practice effectively. This infrastructure must soon extend beyond physiologic and bronchoscopic testing capacity to the development of radiologic imaging centers, pathologic training and laboratory capacity, nursing expertise in respiratory care, oxygen delivery, rehabilitation medicine, and access to affordable pharmacologic agents for symptomatic treatment. Additional transfer of expertise from developed to developing countries is also needed. The Nigerian Thoracic Society recommends development of opportunities for rotation of Nigerian respiratory medicine residents to teaching hospitals in developed countries for intensive
exposure to world-class teaching and medical care. Our study is probably the first to estimate the capacity for respiratory care and practice in a developing country and provides previously unavailable information. Nonetheless, there are weaknesses in our study design. To estimate the number of respiratory specialists in Nigeria, we counted registered specialists and members of the Nigerian Thoracic Society. This approach may have underestimated the total number of formally trained respiratory specialists in the country. However, we think it is unlikely that an important fraction of well-trained respiratory practitioners in Nigeria are not registered members of the society or known to members of the Society. Other limitations in study design might have resulted in an overestimate of respiratory specialist capacity. Our assessment of respiratory care resources was not exhaustive, as some basic respiratory tools, such as diagnostic thoracentesis and non-TB microbiology, were not assessed. We cannot rule out a reporting bias because we did not sample systematically at a facility level, and some centers had multiple respondents. Institutions located near the venue of the scientific congress had a higher representation in the survey. However it is worth noting that the density of respiratory physicians per state is higher in southwest Nigeria, where the survey was held. Additionally, our inventory of respiratory care resources is based on self-report by
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8
9
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participating physicians. We did not conduct a direct on-site audit of facilities or survey of hospitals or clinics. We believe, however, that these findings are credible, because the details were provided by specialists who are directly involved in the use of these services for patient care. Anecdotal reports from respiratory physicians in Nigeria and many developing countries also agree with our findings. In conclusion, our study confirms that there are remarkable gaps in the quality and capacity for respiratory care in Nigeria, which likely mirrors the situation in other countries of comparable economic status. These gaps require urgent strategic and concerted systematic improvement. Our findings call for a visionary effort to advance respiratory care in developing countries as the burden due to lung diseases attains significant proportions. There is a need to develop policies that support the provision of basic and advanced facilities for respiratory diagnosis and an integrated approach to respiratory care that is sustainable in developing economies. n Author disclosures are available with the text of this article at www.atsjournals.org. Acknowledgment: The authors thank the leadership of the Nigerian Thoracic Society for supporting the conduct of this survey. They also thank Professor Fatiu Arogundade of the Department of Medicine, Obafemi Awolowo University, Professor Sonia Buist of Oregon Health and Sciences University, and Professor Jane Carter of Brown University for their helpful comments in the writing of this manuscript.
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