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Infectious Diseases in Clinical Practice:
doi: 10.1097/IPC.0b013c31815d8d61
Original Articles

Diagnostic and Treatment Delay in Tuberculosis in 7 Countries of the Eastern Mediterranean Region

Bassili, Amal MD, MPH, DrPH*; Seita, Akihiro MD*; Baghdadi, Samiha MD*; AlAbsi, Amin MD†; Abdilai, Ismail MD‡; Agboatwalla, Mubina MD§; Maamari, Fadia MD∥; Nasehi, Mahshid MD¶; Nasir, Hashim MD#; Soliman, Sahar MPH**; Enarson, Donald A. MD††

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Author Information

*Stop Tuberculosis, Division of Communicable Diseases, World Health Organization, Regional Office of the Eastern Mediterranean Region, Cairo, Egypt; †National Tuberculosis Control Programme, Sana'a, Republic of Yemen; ‡National Tuberculosis Control Programme, Hargeisa, Somalia; §HOPE NGO, Karachi, Pakistan; ∥National Tuberculosis Control Programme, Damascus, Syrian Arab Republic; ¶National Tuberculosis Control Programme, Tehran, Islamic Republic of Iran; #Respiratory and Chest Diseases Institute, Baghdad, Iraq; **National Tuberculosis Control Programme, Cairo, Egypt; and ††International Union Against Tuberculosis and Lung Diseases, The Union, Paris, France.

This project was technically and financially supported by the EMRO/Special Programme for Research and Training in Tropical Diseases Small Grants Scheme for Operational Research in Tropical and Other Communicable Diseases. This project could not have succeeded without the support of the national authorities and the NTPs.

Address correspondence and reprint requests to Amal Bassili, MD, MPH, DrPH, Regional Office of the Eastern Mediterranean Region, Abdulrazak Sanhouri Street, Nasr City, Cairo, Egypt. E-mail: bassilia@emro.who.int.

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Abstract

Objectives: A multicountry study was conducted during 2003-2004 to study the extent of delay in the diagnosis and treatment of patients with tuberculosis and its determinants.

Methods: The study was conducted in 7 countries of the Eastern Mediterranean Region. Five thousand fifty-three newly diagnosed, adult, smear-positive, pulmonary tuberculosis cases were enrolled in the study. They were interviewed according to a pretested and structured questionnaire about the various factors affecting timely treatment.

Results and Conclusions: The mean delay duration between the onset of symptoms until treatment with antituberculosis drugs ranged from 1.5 to 4 months in different countries.

Patient delay-defined as the time interval between the onset of symptoms and first health-seeking behavior-ranged from a mean of 9.9 days in Pakistan to 69 days in Somalia, whereas system delay-defined as the time interval between the first health-seeking behavior and treatment-ranged from 5 days in Iraq to 90.7 days in Pakistan.

The private sector was the first choice for more than two thirds of patients. The main determinants of delay were sociodemographic, economic, stigma, time to reach the health facility, seeking care at nonspecialized individuals, and visiting more than 1 health care encounter before diagnosis.

In 2003, Directly Observed Treatment, Short Course (DOTS) programs successfully treated 84% of all registered, new, smear-positive patients, but detected only 28% of the estimated tuberculosis cases in the world.1 Therefore, the target of 70% case detection might not be reached until 2013, unless interventions are made that are able to increase the case-detection rate.

Early diagnosis and prompt effective therapy form the key elements of the tuberculosis control program. Delay in diagnosis results in increased infectivity in the community, and it is estimated that an untreated smear-positive patient can infect, on average, 10 contacts annually and more than 20 during the natural history of the disease until death.2 Delay in tuberculosis diagnosis may also lead to a more advanced disease state at presentation, which contributes to late sequelae and overall mortality. Smear-positive cases are more likely to infect other individuals.

DOTS coverage has been increased in all the health facilities of ministries of health in many countries of the region since the late 1990s. However, such increased coverage was not coupled with a parallel rise in the case-detection rate. Although coverage is crucial to ensure proper disease control, it is not the only factor that would influence timely access of patients to appropriate health services. There is growing evidence that access to treatment remains difficult for a high number of patients with tuberculosis. Several factors have been identified as influencing delay in diagnosis and start of treatment, including the individual's perception of disease, socioeconomic level, stigma, extent of awareness about the disease, the severity of the disease, distance between the patient's residence and health services, and expertise of the health personnel.

Such delay may occur at the level of the patient (patient delay) or at the level of the health system (system delay). Factors which contribute to patient or system delay are numerous, and it is important to identify and address these factors to devise strategies for the National Tuberculosis Control Program (NTP).

The challenge posed by the low case-detection rate in the region can be addressed by studying the delay in case finding. Understanding the causes behind the delay in diagnosis and treatment is essential for all partners involved in tuberculosis control.

Delays in case finding are common and have been studied in many countries whether developed or developing and low or high prevalence.3-6 In countries with low prevalence, delay is mainly attributed to the fact that tuberculosis is not suspected or to disintegration of the previous infrastructure for tuberculosis control. In countries with high prevalence, delays are often prolonged and relate to both delays on the side of patients in seeking treatment and on the side of physicians in diagnosis. Reported determinants of delay include being part of specific patient groups (ie, women, rural vs urban residents, nationality, etc)3 or the availability of and accessibility to health services.4-6 These studies also highlight the association between delay and an increased economic burden and mortality attributed to tuberculosis. Country-specific determinants of delay must be studied, clearly identified, and addressed to improve the quality and effectiveness of the NTPs.

The aim of the present study was to evaluate the extent of delay in diagnosis and treatment of patients with tuberculosis, identify the major contributors to such delay (whether patient or system), and study its various determinants in 7 countries, 4 high- and 3 middle-burden countries of the World Health Organization (WHO) Eastern Mediterranean Region. The ultimate goal of the study was to identify the barriers interfering with case-finding activities under DOTS and to devise solutions to increase the case detection in the community and by the NTPs. It is envisaged that the information obtained by this study will assist these programs in achieving their targets.

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MATERIALS AND METHODS

A multicountry study was designed and coordinated by the Eastern Mediterranean Regional Office (EMRO)/UNICEF/UNDP/World Bank/WHO/Special Programme for Research and Training in Tropical Diseases Small Grants Scheme for Operational Research in Tropical and Other Communicable Diseases. The study was conducted during the period 2003-2004 in 7 countries of the WHO Eastern Mediterranean Region: Egypt, Islamic Republic of Iran, Iraq, Pakistan, Somalia, Syrian Arab Republic, and Yemen.

In Pakistan, the study was conducted in the city of Karachi. Three chest centers where DOTS had been implemented were chosen as study sites. The centers were Nazimabad Chest Clinic, Malir Chest Clinic, and Ojha Institute of Chest Diseases. In Iraq, the study was conducted at the Respiratory and Chest Disease Institute in Baghdad and in 3 tuberculosis centers in other governorates (Missan, Babylon, and Qadissiah). In Somalia, a convenience sample was selected from accessible centers implementing DOTS in Somalia. The selected centers in southern and central Somalia were Mercy Mogadishu and Jawhar. In the north, the selected centers were Hargeisa, Borama, and Borao. In Islamic Republic of Iran, Egypt, Syrian Arab Republic, and Yemen, nationwide cross-sectional studies were conducted.

Representative samples of newly diagnosed, smear-positive, pulmonary tuberculosis cases, 15 years of age and older, diagnosed in the study settings of the 7 countries, were consecutively included in the study. Based on the estimated incidence of tuberculosis for each of the countries studied, a maximum allowed error of 10%, and a 95% confidence interval, the least reliable sample size for the 7 countries would have been 3097 patients. However, as it was planned to perform multivariate logistic regression analysis, the rule of thumb was used; hence, the sample size per country was calculated at 800 study subjects owing to the large number of studied variables. The smaller sample size initially estimated would have affected the study power. Iraq and Yemen could not achieve this big sample size because of the war situation in the former and difficulties in enrolment of patients in the latter.

Therefore, the total sample size was 5053 patients, distributed as follows: 802 in Egypt, 800 in Islamic Republic of Iran, 400 in Iraq, 844 in Pakistan, 809 in Somalia, 800 in Syrian Arab Republic, and 598 in Yemen.

In the countries where nationwide surveys were conducted, lists of all smear-positive cases in all the tuberculosis centers were obtained, and the patients were randomly selected from the different centers in these countries using the probability proportional-to-size cluster sampling technique. In the other countries, all new pulmonary tuberculosis cases managed in the selected centers were consecutively enrolled until the required sample size was reached from each center.

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Data Collection Techniques and Tools
Questionnaire

Patients were interviewed according to the questionnaire developed for this multicountry study. The questionnaire was pretested and translated into the local language of each country. Health workers, who included doctors and paramedical staff, underwent intense training on interview and probing techniques. They then directly interviewed the patients during the first 2 weeks of their treatment, after obtaining their informed consent.

The questionnaire included information about sociodemographic characteristics, risk factors of tuberculosis, and health-seeking behavior. The patients were also asked questions regarding the elements that might influence their health-seeking behavior, such as fear of what would be found on diagnosis, fear of social isolation, stigma, knowledge regarding the disease, satisfaction with care, and others.

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Socioeconomic Status

The socioeconomic status was measured using a summation score of the following variables: education, occupation, and income (0 best and 7 worst).

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Stigma

Variables measuring stigma were recorded on a 5-point Likert scale (0 the highest and 4 the lowest degree of stigma). These variables included feeling ashamed of having tuberculosis, having to hide tuberculosis diagnosis from others, cost incurred by the long disease duration, isolation due to tuberculosis, whether a girl is able to decide about getting tuberculosis treatment, and the extent to which tuberculosis affects the following: relation with others, work performance, marital relations, family responsibilities, chances of marriage, family relations; female infertility, complications during pregnancy, breast-feeding, and pregnancy outcome.

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Satisfaction With Care

Variables measuring satisfaction with care were recorded on a 4-point Likert scale (0 best and 3 worst). These included availability of services in tuberculosis centers, prompt action from primary health care personnel, adequacy of equipment and free medications in these centers, proper coverage of tuberculosis centers in the area, health facility workload, and waiting time.

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Knowledge

Variables measuring knowledge were recorded on a 3-point Likert scale (0 best and 2 worst). These included knowledge about the type of disease, its causes, curability, existence of vaccine, type of antituberculosis drugs, and duration of treatment.

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Definitions

The total delay is the time interval from the onset of illness until the initiation of antituberculosis drugs. It is the sum of 2 time intervals: diagnostic delay and treatment delay. These are defined as follows:

* Diagnostic delay: time interval between the onset of symptoms and labeling of the patient as a patient with tuberculosis (tuberculosis diagnosis).

* Treatment delay: time interval between the tuberculosis diagnosis and initiation of antituberculosis drugs.

The total delay is also the sum of patient and health care system delay because it can be attributed to these types of delay which are defined as follows:

* Patient delay: time interval between the onset of symptoms and presentation to a health care provider.

* Health care system delay: time interval between the date of health-seeking behavior at a health care provider and the initiation of antituberculosis treatment.

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Pilot Study and Questionnaire Testing

A pilot study was carried out to

* test the whole system of communication and supervision,

* assess the suitability of the study tools (interviews and questionnaire),

* estimate the required time for filling in the questionnaire and for data collection, and

* assess the performance of the data collectors and quality of training.

The instrument was first tested for content validity to determine if it still measured what it was intended to test. To carry out this procedure, it was initially reviewed by the experts in WHO's Regional Office for the Eastern Mediterranean and several researchers experienced in this field to clarify confusing items and to comment on the apparent validity of each item. After examination by these individuals, several items were changed. The resulting form was then administered to interviewers who were asked to comment on and to clarify the items which were not easily understood.

To examine the internal consistency of the items of the questionnaire, Cronbach α was calculated and was found acceptable.

A small number of individuals (n = 30) were interviewed to evaluate the questionnaire's reliability. Test-retest reliability was assessed by giving the questionnaire to the same person twice at an interval of 2 weeks and measuring the intraclass correlation coefficient to evaluate the intrarater reliability. Reinterviewing the same person by 2 different interviewers and measuring the intraclass correlation coefficient were also performed to measure the interrater reliability.

The questionnaire was modified according to the results of the pilot phase, and the final form was translated into local languages.

Training of health workers and field supervisors included discussion of the objectives and importance of the study and orientation about the formats used. Training on data collection, filling in the forms, and revising the formats was performed through demonstration and role playing.

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Data Management and Statistical Analysis

With regard to scoring system, the score was first reversed before addition to its domain to reflect the increase in the studied variable. The mean percentage score for socioeconomic level, stigma, satisfaction with care, and knowledge was calculated as follows: (Sum of scores obtained/Maximum scores that could be obtained) × 100.

Then the mean percentage scores were computed, and the studied variables were expressed as falling between 0 and 100%, with the highest percentage reflecting the increase in that characteristic/variable. For example, a 100% of socioeconomic level, knowledge, or satisfaction with care would indicate the best score for these variables, and for stigma, it would indicate the highest level of stigma experienced.

Cases with longer delays were categorized as "cases," whereas others with shorter delays were considered as "controls." The cutoff point(s) for "longer" delays was defined according to the median value obtained for each country. The latter was also used to categorize other variables, such as stigma, knowledge, and satisfaction with care, into adequate/acceptable and inadequate/unacceptable.

Data analysis was performed using the statistical packages SPSS for Windows version 11 (SPSS 10.01 Inc, Chicago, Ill) and Epi Info 2000 (CDC, Atlanta, Ga). Descriptive statistics were used such as frequency, mean, and SD, median, minimum and maximum, and so on. Comparisons between groups were made using the χ2 test or Fisher exact test as appropriate for qualitative/categorical variables, and using the t test or Mann-Whitney U test for quantitative variables. A multivariate regression analysis was performed to adjust for the confounding effect of several identified determinants of diagnostic and treatment delay of patients with tuberculosis. Level of significance was determined at 95% (P < 0.05), and all tests were 2-sided.

All countries, except the Islamic Republic of Iran and Iraq, adopted the same variables while studying the determinants of delay. However, the Islamic Republic of Iran used another group of variables that were previously tested in a baseline study conducted in 1995, for comparability purposes. Therefore, analysis was performed separately and using multiple linear regression rather than multivariate logistic regression analysis.

Similarly, the Iraqi study was greatly interrupted by the war in the country and was analyzed independently using univariate analysis.

For the above-mentioned reasons, data from these 2 countries might be missed in some sections of the results.

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Ethical Considerations

The proposals were approved by the institutional ethical review committees respective to each country and obtained national endorsement. Feedback about the major findings and recommendations was given to and requested from the managers and health staff.

With regard to informed consent and confidentiality, the following points were thoroughly clarified to all subjects:

* objectives, steps, and expected outcome of the research;

* benefits of the research, both benefits to the subject and benefits to others;

* absolute confidentiality of information obtained; and

* the right to withdraw from the study at any time without any way affecting his/her current care.

All participants gave their verbal consent voluntarily.

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RESULTS

Sociodemographic Characteristics of Patients With Tuberculosis

With the exception of the Islamic Republic of Iran, the majority of patients were 35 years old and younger. Tuberculosis was common in males in Egypt, Iraq, Syrian Arab Republic, Somalia, and Republic of Yemen, with a male/female ratio ranging from 1.4 in Yemen to 2.5 in Somalia. By contrast, it was slightly more common in females in 2 countries (Islamic Republic of Iran and Pakistan) with a male/female ratio of 0.98 for each.

The proportion of patients who were illiterate or can read and write ranged from 34.6% to 75.2%, and the unemployment rate ranged from 43% to 74.3%. In Iraq, Islamic Republic of Iran, and Somalia, the majority of patients were living in urban areas, in Egypt and Syrian Arab Republic in rural areas, and in Pakistan in suburban areas. In Yemen, they were equally distributed in urban and rural areas. A limited proportion of patients were divorced, separated, or widowed, and being in debt was reported by a considerable proportion of patients (Table 1).

Table 1
Table 1
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Delay in Diagnosing and Treating Patients With Tuberculosis

Table 2 shows a comparison between the extent of delay recorded in the different countries and the different types of delay. The mean duration of delay between the onset of symptoms and treatment ranged from 46 days in Iraq to 127 in the Islamic Republic of Iran. The health system was the main contributing factor to the delay in the Islamic Republic of Iran, Pakistan, and Egypt. The delay was mainly attributed to the patient in the Syrian Arab Republic, Somalia, Yemen, and Iraq (Fig. 1).

Table 2
Table 2
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Figure 1
Figure 1
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Risk Factors of Total Delay

The duration of delay was significantly longer in patients treated in the private sector compared with those treated by the NTP health services in all countries except Somalia and Syrian Arab Republic, where the duration of delay in the private sector was longer but was not significant (Table 3).

Table 3
Table 3
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Table 4 shows the predictors/risk factors for total delay in Egypt, Pakistan, Somalia, Syrian Arab Republic, and Yemen. The significant predictors/risk factors for total delay in Egypt were being illiterate (2.76-fold increased risk), time to reach the health facility more than half an hour and more than 1 hour (1.73- and 1.75-fold increased risk compared with those ≤0.5 hour), high crowding index (1.2-fold), and more than 1 health care encounter before diagnosis (2.55-fold increased risk). Being female or a student was protective in motivating patients to seek health care earlier than others.

Table 4
Table 4
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In Pakistan, the significant risk factors for total delay were living in suburbs (2.5-fold increased risk, as compared with living in urban area); belief that low-cost services were inadequate, hence reluctance to seek care from public services; being diagnosed in health facilities not belonging to the NTP (4-fold increased risk); visiting several health care providers before diagnosis (2-fold increased risk for each encounter); inadequate knowledge regarding the disease (1.13-fold increased risk); and poor satisfaction with care (1.15-fold).

In Somalia, the significant risk factors for total delay were living in suburbs (2.2-fold increased risk compared with urban areas), seeking care from nonspecialized individuals (2.2-fold increased risk compared with health care provider), and more than 1 health care encounter before diagnosis (1.5-fold increased risk). High degree of stigma was protective.

The significant risk factors for total delay in the Syrian Arab Republic were age older than 35 years (1.02-fold), living far from the health facility (2.5-fold increased risk), high degree of stigma (1.2-fold increased risk), seeking care from nonspecialized individuals (not a health care provider) (3.6-fold increased risk compared to health care provider), and more than 1 health care encounter before diagnosis (2.0-fold increased risk).

The significant risk factors for total delay in Yemen were being female (2.3-fold increased risk), time to reach the health facility more than half an hour (1.8-fold increased risk), and high degree of stigma (1.7-fold increased risk).

The significant risk factors for total delay in Islamic Republic of Iran were age older than 35 years (1.01-fold increased risk), economic constraint (1.3-fold), non-Iranian nationality (1.3-increased risk), number of symptoms at first attendance (1.12-fold), positive history of chronic pulmonary disease (1.3-fold increased risk), and having negative sputum smear results for acid-fast bacilli on entering the health system (1.6-fold increased risk). Fever as the first symptom, presenting with cough at the first attendance to the health facility, performance of sputum smear or chest radiograph on first attendance at the health facility, and high tuberculosis notification rate in the governorate were associated with reduced risk for total delay (Table 5).

Table 5
Table 5
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In Iraq, the significant risk factors for total delay (according to univariate analysis) were age older than 35 years (1.66-fold increased risk), suburban and rural residence (3.0- and 1.8-fold increased risks, respectively), overcrowded houses (1.6-fold increased risk), smoking (2.3- and 2.2-fold for current and ex-smokers, respectively), self-medication with onset of illness (2.5-fold increased risk), initially diagnosed by general practitioner rather than chest specialists (2.1-fold), inadequate satisfaction with care (10.5-fold increased risk), high degree of stigma (2.1-fold increased risk), and poor knowledge regarding the disease (1.7-fold). Living far from the health facility, lower educational levels, and coexistent diabetes mellitus were protective factors (Table 6).

Table 6
Table 6
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DISCUSSION

This study reported the unacceptably long delay duration between the onset of symptoms until treatment with antituberculosis drugs. This duration ranged, on average, from 1.5 to 4 months in the different countries during which the diseased person is transmitting infection in the community.

Detailed analysis of the various factors interplaying to affect the health-seeking behavior and timely treatment showed that they could be categorized into either patient or health system factors, the former being the major contributor to delay in Somalia, Syria, Iraq and Yemen, and the latter in the remaining countries.

As the socioeconomic indicators are strong determinants of the health-seeking behavior of the patients which is, in turn, the main determinant of patient delay, their in-depth analysis was crucial to provide detailed information about the situation. Such analysis showed that patients with tuberculosis are a disadvantaged group in their communities. The illiteracy rates reported were significantly higher than those of the general population in most of these countries, as follows: Egypt (67.3% vs 30% in the general population), Islamic Republic of Iran (52.1% vs 6%), Iraq (46% vs 44%), Pakistan (56.6% vs 47%), Somalia (75.2% vs 65%), Syrian Arab Republic (34.6% vs 14%), and Yemen (55.7% vs 53%).7

Similarly, the unemployment rate ranged from 43% in Egypt up to 74.3% in Somalia compared with a range of3% to 12% recorded for the general population in the studied countries, except Iraq, which recorded a high unemployment rate of 50%, mainly attributed to the war situation.7

More than one quarter of patients reported being in debt. This known association between poverty and tuberculosis has been well documented, and tuberculosis has been labeled as a "disease of poverty." Hence, poverty reduction, one of the United Nation's millennium development goals, would contribute to reduction of the tuberculosis burden in endemic countries.8,9

In all the countries studied, females were of significantly lower socioeconomic status compared with males. However, their knowledge regarding the disease was not significantly different from males, except in Egypt and Yemen. Gender did not seem to affect the knowledge and attitudes of patients with tuberculosis, in line with what has been previously reported from the region.10 Females experienced a significantly higher level of stigma regarding tuberculosis in Syrian Arab Republic and Yemen, but their level of satisfaction with care was not significantly different from males in all the 7 countries. Such gender differences in regard to stigma and satisfaction with care are consistent with reports from other developing countries.11

Across the countries, there were significant differences in socioeconomic status, feeling of stigma, knowledge, and satisfaction with care, but detailed comparison was considered outside the scope of this study.

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Total Delay

The mean duration between the onset of symptoms and treatment was 46 days in Iraq, 57 in Egypt, 59.2 in Yemen, 79.5 in Somalia, 80.4 in Syrian Arab Republic, 100 in Pakistan, and 127 in Islamic Republic of Iran.

Various mean delay durations were reported from the different endemic countries: 60 days from India, 87.5 days from Malaysia, and a median delay of 99 days from Nepal.12-14 The delay reported from Pakistan was comparable to the rates reported from Vietnam, that is, a mean of 69.3 days and median of 44.1 days.15

Sociodemographic characteristics proved to be significant predictors of delay in almost all countries. Age older than 35 years was associated with a 1.01- to 1.7-fold increased risk per year in Syrian Arab Republic, Islamic Republic of Iran, and Iraq. Female gender was associated with an increased risk for delay in Yemen but was protective in Egypt, prompting patients to seek timely health care. Illiteracy and overcrowding were also significant risk factors in Egypt and Iraq, respectively. Residence proved to be a significant risk factor for delay in Iraq, Somalia, and Pakistan, where living in suburban areas was associated with a 3-, 2.2-, and 2.5-fold increased risk for delay in treatment, respectively, compared with urban areas.

Accessibility of the health facility was a significant predictor of delay in Egypt, Syrian Arab Republic, and Yemen, where patients spending more than half an hour to reach the health facility were at a significantly higher risk for delay compared with those living closer to the health facility.

Stigma was associated with significantly higher risk for delay in Syrian Arab Republic, Yemen, and Iraq (1.2-, 1.7-, and 2.1-fold, respectively). Inadequate knowledge regarding the disease and poor satisfaction with care were significant predictors of delay in Pakistan and Iraq.

Interestingly, having a negative sputum smear examination on entering the health system in the Islamic Republic of Iran was associated with a 3-fold increased risk of delay. This could be explained by the fact that the patients feel reassured about their health condition and do not proceed with the necessary investigations to diagnose the condition. Fever and performance of chest radiograph were protective factors, prompting patients to seek early health care.

Smoking, whether current or ex-smoking, was also reported as a significant risk factor for delay. Smokers often do not present themselves to the health facilities in the belief that their cough is due to smoking.

An overall assessment of the delay in initiating treatment after the onset of symptoms brings forth the important point that in Egypt, Islamic Republic of Iran, and Pakistan, patients are sufficiently knowledgeable to consult health care providers within a short time after the onset of their symptoms. However, the private health system is accessed rather than the public health system. In fact, in almost all the countries, seeking initial care from a nonspecialized individual or the private sector and seeking care from more than 1 health care provider before diagnosis were invariably significant risk factors for delay.

Private health care providers do not have strong linkages with the mainstream public health system. In addition, lack of continuing medical education contributes to poor knowledge and therefore poor ability to immediately diagnose a case of tuberculosis. Patient dissatisfaction results in repeated consultations with private health care providers, including homeopaths or traditional healers. Repeated and unfruitful consultations drain the patients' financial resources, which would otherwise be used for antituberculosis treatment. There is a dire need to integrate the private health sector with the mainstream public health intervention: DOTS. An important step in this context could be to allow the private sector to access the central laboratory for sputum microscopy through the Tuberculosis Control Program as well as to enable the NTP to register these patients. Patients could then easily pass between the public and private health systems without redundant investigations, unnecessary paperwork, and associated delay. One of the reasons cited for all the delays was the long travel time to tuberculosis centers. One of the reasons for initial consultation with a private health care provider was the proximity of the general practitioner's clinic to the patient's residence. The private health care providers could be used to dispense antituberculosis treatment through their own clinics which could be part of the DOTS strategy. There is also a need to decentralize the tuberculosis centers so as to have more treatment and diagnostic facilities in the peripheral centers to allow easy access for the patients. This needs to be accompanied by awareness raising in the population regarding tuberculosis.

Patients with tuberculosis in Egypt spent, on average, US $21 before diagnosis, and a total of US $16,870 was spent by all patients before diagnosis. Similarly, in Pakistan, an average of US $18.6 was spent per patient before diagnosis. These results indicate the extent of economic burden that such delay exerts on families without a corresponding gain in health care.

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Other Factors Affecting Tuberculosis Control

Age and gender distribution of the studied patients are considered indicators of the progress in the control of the tuberculosis epidemic. Patients are, on average, around 30 to 35 years of age or younger, except in Islamic Republic of Iran where the mean age (SD) was 45.9 years (20.1 years). A shift in the mean age toward older age groups points at a lessening of the problem in the society. It indicates that transmission of tubercle bacilli is decreasing and that an increasing proportion of cases emanates from the pool of infected many years in the past. The shift implies that cohorts with less infection are successfully replacing cohorts born at the time when risk of infection was much higher.16,17

A male predominance existed in Egypt, Iraq, Somalia, Syrian Arab Republic, and Yemen, ranging from 2.5:1 in Somalia to 1.4:1 in Yemen, whereas a slight female predominance was reported from Pakistan and Islamic Republic of Iran. This observed difference in gender distribution in tuberculosis could be attributed to racial, genetic, or sociocultural factors. It could be also attributed to a combination of the fairly similar (but slightly lower) prevalence of tuberculosis infection among females compared with males, but a higher risk of progression to disease among young females. Experiences from developed countries have shown that with an improving epidemiological situation, the age of patients with tuberculosis increased to the point in age where the risk of progression from infection to disease inverted among sexes and became larger for men than for women.16,17

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CONCLUSIONS AND RECOMMENDATIONS

The risk factors for delay identified in this study should be the subject of future interventions to reduce the delay in delivery of treatment to patients with tuberculosis and hence transmission of the disease in the community. As the delay in the treatment of patients with tuberculosis is attributed to both the patient and the health system, countries where the patient component is large should put more emphasis on increasing awareness of the community about tuberculosis symptoms. Countries where the delay is mainly attributed to their health systems should put more efforts into building effective collaboration between the NTP and the private sector, often the recipient of the first health-seeking action of the community.

In view of these conclusions, the following are the study recommendations to NTPs.

1. Detection, follow-up, and treatment of tuberculosis among people living in suburbs and rural areas, especially among females in all areas and among the poor, should be improved by: integrating the tuberculosis program into other existing health services at all levels, involving outreach community workers and other agencies working in the health sector, and increasing community awareness through health education, using appropriate channels.

2. Efforts should be made to increase public awareness about the symptoms of tuberculosis and to educate them about the importance of seeking early care and the availability and location of free diagnostic services. Patients with tuberculosis should be a special target for health education as many of them could infect their contacts.

3. Efforts should be made to educate both public and private physicians about the need to maintain a high index of suspicion of tuberculosis and rapidly perform appropriate tests. Sputum must be examined in all patients with prolonged productive cough, negative investigations should be repeated, and patients should be informed to return if symptoms persist.

4. Effective collaboration should be developed between private and public providers to ensure an effective public-private mix of services.

5. Training and retraining of health care providers about tuberculosis at regular intervals should be instituted. Integration of tuberculosis retraining courses into national systems of continuing medical education for private physicians is also recommended to ensure early case detection.

6. The various delay durations and the significant determinants of delay identified in the present study should be incorporated into routine surveillance reports. This would allow monitoring of the effectiveness of the interventions and control measures in reducing the duration of the delay, hence reducing the transmission and burden of tuberculosis in the community.

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MULTICOUNTRY GROUP OF THE DELAY STUDY

Scientific and Writing Committee

* Dr Amal Bassili, focal point, tropical disease research, Stop Tuberculosis, WHO/EMRO

* Dr Akihiro Seita, regional adviser, Stop Tuberculosis, WHO/EMRO

* Dr Samiha Bahgdadi, medical officer, Stop Tuberculosis, WHO/EMRO

* Dr Donald Enarson, director of scientific activities, International Union Against Tuberculosis and Lung Disease (The Union)

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Research Teams in the 7 Eastern Mediterranean Countries
Egypt

Principal investigator: Dr Sahar Shaker Soliman, National Tuberculosis Control Programme, Central Unit

Coinvestigators and field workers:

Mr Moustafa, National Tuberculosis Control Programme, Central Unit

Mr Tarek Mohamed Tawfik, National Tuberculosis Control Programme, Central Unit

Governorate Coordinators for Tuberculosis (GCT):

Dr Laila Michelle Zaki, Cairo GCT

Dr Maged Zaki Botros, Beni Sweif GCT

Dr Ussama Abd El-Rahman El-Temami, Damietta Chest Hospital

Dr Adel Sami Nashed, Fayoum GCT

Dr Fayka El-Weeshy, Gharbia GCT

Dr Wagdy Abd El-Moneim Amin, Giza Chest Hospital

Dr Saleh Atteya Abbas, Sharqia GCT

Dr Moustafa Lotfy, Alexandria GCT

Dr El-Sayed El-Sayed Nada, Beheira GCT

Dr Mohamed Saad Sheehab, Daqahlia GCT

Dr Wafaa Salah Mohamed, Ismaelia GCT

Dr Ibrahim Mohamed Ibrahim, Kafr Elsheikh Chest Hospital

Dr Fayez Ragab Zayed, Matrouh Chest Hospital

Dr Mahmoud Saber Atteya Shaheen, El-Areesh (North Sinai) Chest Hospital

Dr Mohamed Mohamed El-Desouki, Port Said GCT

Dr Ahmed Hussein Shady, Suez GCT

Dr Mahmoud Nooman Abd El-Wahed, Qalubia GCT

Dr Hassan Shehata Abd El-Rahman, El Marg Chest Hospital

Dr Gamal Abd El-Zaher, Minia GCT

Dr Mohamed Adb El-Hameed, Assyut GCT

Dr Hassan Marzouk, Sohag GCT

Dr Emad Helmy, Qena GCT

Dr Hamdy Abd Allah Abd El-Azeez, Aswan GCT

Dr Abd El-Raouf Mohamed El-Ameer, Luxor GCT

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Islamic Republic of Iran

Principal investigator: Dr Mahshid Nasehi, Manager, National Tuberculosis Control Programme, Ministry of Health and Medical Education

Coinvestigators and field workers:

Dr Kazem Mohammad, Epidemiology and Biostatistics Department, School of Public Health, Tehran University of Medical Sciences

Dr Mohammad Mehdi Gouya, Disease Control Department, Ministry of Health and Medical Education

Dr Seyed Reza Madjdzadeh, Epidemiology and Biostatistics Department, School of Public Health, Tehran University of Medical Sciences

Dr Ghasem Zamani, Epidemiology and Biostatistics Department, School of Public Health, Tehran University of Medical Sciences

Dr Kourosh Holakoii, Epidemiology and Biostatistics Department, School of Public Health, Tehran University of Medical Sciences

Dr Salek Salek, Disease Control Department, Ministry of Health and Medical Education

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Iraq

Principal investigator: Dr Hashim Ali Nassir

Coinvestigators:

Dr Ayed Al-Duleimy, Medical Officer, STB, WHO Somalia

Dr Waleed Al-Ani, Biostatistician, College of Medicine, Al-Mustansiryah University of Baghdad

Coordinators:

Dr Salam Fadhel Najim, TB Center, Al Sader city

Dr Hanan Ibrahim, TB Center, Babylon governorate

Dr Hasan Sharif, TB center, Al-Qadisiyah governorate

Dr Hameed Mahdee Saleh, TB Center, Misan governorate

Dr Hala Adnan Saad, TB Center, Kirkuk governorate

Dr Mohammad Abbas, TB Center, Al Sader city

Health workers:

Mr Abdel Kareem Fazza, Misan TB Center

Mr Hussain Ali, Diwaniyah TB Center

Mrs Haleema Dhaki, Babylon TB Center

Ms Iman Hamed Hussein, Babylon TB Center

Mr Alaa Abdel Hussain, TB Institute, Baghdad

Mr Muhsen Abdel Ameer, TB Institute, Baghdad

Ms Dina Jerjes, TB Center, Baghdad

Ms Tagreed Abdul Kareem, Misan TB Center

Mr Thamer Abbas, TB Institute, Baghdad

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Pakistan

Principal investigator: Dr Mubina Agboatwala

Research officer: Dr Ashiq Domki

Data manager: Mr Sohail Saeed

Health workers: Mss Rohoida, Afsheen, and Huma

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Republic of Yemen

Principal investigator: Dr Amin Noman Al-Absi

Coinvestigator and field worker: Mr Al-Hamady Abdulbary and TB Coordinators in the different Governorates

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Somalia

Principal investigator: Dr Ismail Adam Abdilai, National Tuberculosis Control Programme

Coinvestigators and field workers: Drs Abukar Ali Hilowle and Bashir Abdi Suleiman, National Tuberculosis Control Programme

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Syrian Arab Republic

Principal investigator: Dr Fadia Maamari

Coinvestigators and field workers:

Ms Iman Fallah (Damascus);

Mr Nabil Kassab (rural Damascus)

Mr Abdelrahman El-Shanboor (Deraa)

Mr Hasssan Helel (Swedaa)

Mr Hassan Alwash (Aleppo)

Ms Enaam Rabieh (Homs)

Mr Ghassan Dehis (Hama)

Ms Iman Kassir (Edleb)

Ms Nahla Elhara (Tartous)

Ms Gharam Ahmed and Faten Kanaan (Lazekhia)

Mr Mohamed Eltahey (Elreka)

Ms Rawai El-Aly (Deer El-Zooor)

Mss Sawasan Goreya and Hanady Ahmed (NTP, central unit)

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ACKNOWLEDGMENTS

Dr Nasehi thank the following organizations and institutions in Iran: Ministry of Health, Disease Control Department and Tehran University of Medical Science, School of Public Health, for their financial support.

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