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 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.
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).
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).
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.
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.
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
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.
- 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.
- 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.
- 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.
- Effective collaboration should be developed between private and public providers to ensure an effective public-private mix of services.
- 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.
- 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.
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)
Research Teams in the 7 Eastern Mediterranean Countries
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
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
Principal investigator: Dr Hashim Ali Nassir
Dr Ayed Al-Duleimy, Medical Officer, STB, WHO Somalia
Dr Waleed Al-Ani, Biostatistician, College of Medicine, Al-Mustansiryah University of Baghdad
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
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
Principal investigator: Dr Mubina Agboatwala
Research officer: Dr Ashiq Domki
Data manager: Mr Sohail Saeed
Health workers: Mss Rohoida, Afsheen, and Huma
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
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
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)
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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