Tuberculosis (TB) is a highly infectious disease caused by Mycobacterium tuberculosis, primarily affecting the lungs but capable of spreading to other body parts [1]. TB remains a global health concern; in 1993, the World Health Organization (WHO) declared it a public health emergency due to its high mortality rate and widespread impact [2]. It transmits through airborne particles, making it common in densely populated, low-resource settings that facilitate rapid spread [3]. TB continues to challenge public health, especially in low- and middle-income countries where socioeconomic and environmental factors worsen its impact. In the Southeast Asia Region (SEAR), TB is the top infectious cause of mortality among adults, with the region shouldering 40% of the global TB burden [4]. Countries of the Southeast Asia region harbor 38% of the world's TB cases. Each year, about 3 million persons develop TB in this region, of whom 600,000 die [5]. Tuberculosis is also a major public health problem in Bangladesh. Based on current estimates, approximately 3,00,000 people fall ill due to Tuberculosis and 70,000 die every year [6]. Significant progress in TB control has been achieved through WHO's Directly Observed Treatment Short Course (DOTS) strategy, initiated in 1993, which began in government facilities and expanded to urban areas, especially Dhaka, through public-private partnerships [6,7]. TB control in Bangladesh is challenging due to overcrowding, poverty, limited healthcare infrastructure and high unawareness levels [8]. The National Tuberculosis Control Program (NTP) collaborates with NGOs, expanding DOTS services to urban centers like Dhaka, Chittagong and Sylhet through public-private partnerships (PPP) to control TB [9]. This initiative is crucial as many TB patients initially seek private treatment, which often lacks TB-specific care and relies on radiology for diagnosis, leading to incomplete treatment and potential multidrug-resistant TB (MDR-TB) [10]. MDR-TB poses a growing challenge to TB control in Bangladesh [6]. MDR-TB requires strict DOTS and advanced drug regimens, demanding more financial resources and infrastructure, adding complexity to NTP's responsibilities [11]. Financial support for TB control in Bangladesh primarily comes from the Global Fund to Fight AIDS, Tuberculosis and Malaria (GFATM), aiding the NTP in providing free TB treatment, including MDR-TB incentives to ensure adherence [12]. Most of the TB suspects visit chest clinics without referrals and then are directed to NGO clinics for treatment [13]. This referral system, while effective in parts, faces logistical issues in ensuring patients begin and adhere to treatment [14]. Strengthening referral systems for TB suspects in Dhaka chest clinics is essential to improve access to NGO-provided treatment. A robust referral system promotes early diagnosis and better compliance, which is crucial for controlling TB in high-burden areas [15]. The objective of the study was to assess the impact of incentives given to TB suspects on referral success and compare the impact of TB patient incentives combined with DOTS strengthening with that of general DOTS strengthening and provider referral training.

This was a Quasi-experimental Prospective study using non-equivalent group design. The study was conducted at the two Chest Clinics of Dhaka City: Shyamoli & Chankharpul and TB suspects are referred from these Chest Clinics to diagnostic NTP-NGO clinics (including NSDP & UPHCP) in the Dhaka City. All new TB suspects those were attended at two Chest Clinics from 01 January/2006 to 31 December/2006. A cohort of TB suspects and patients were followed up. Suspects were enrolled as they present at the Chest Clinics. A total of 2500 suspects, 1250 samples from each center were initially diagnosed for TB and out of them 1078 were referred to NGO clinics. All these referred participants were analyzed into two different groups.

Case group (N=631): Participants with incentive

Control group (N=447): Participants without incentive

Inclusion criteria:

Participants of all age and both genders.

Exclusion criteria:

• TB suspects at Shyamoli Chest Clinic coming from Chankharpul catchment area and TB suspects at Chankharpul Chest Clinic coming from Shyamoli catchment area were excluded from the study and not provided with any referral slip. Those suspects were diagnosed at the Chest Clinics and then referred as usual existing procedure for DOTS.
• TB suspects living within 1-2 km of the Chest Clinics were not referred for diagnosis.

Study Instrument:

TB Suspect Register:

Medical Officers of Shyamoli and Chankharpul Chest Clinics maintained Suspect Register for all new TB suspects. Newly developed suspect registers were provided to the Chest Clinics by NTP.

Referral Slip:

For the purpose of referral of the suspects to the NGO centers, the Chest Clinics have used a referral slip. The referral slip, which has also been designed specifically for the purpose of the study, recorded information about the name and address of the suspect, name of the referral NGO clinic and the date of first visit to the Chest Clinic. The referral slips were all numbered and have 03 carbonated pages each. The referring clinic issued the first page to the referred TB suspect and retained the second and the third pages at their clinics. The second page of referral slip were collected from the referral clinics through periodical visit.

Data Collection Procedure:

Purposive sampling technique was used to collect data. TB Suspect Register at Shyamoli and Chankharpul Chest Clinics was meticulously checked, verified and corrected on the spot.

Data Analysis:

All statistical analysis was performed using the statistical package for social science (SPSS) program and Windows. Continuous parameters were expressed as mean±SD and categorical parameters as frequency and percentage. Categorical parameters compared by Chi-Square test. The significance of the results as determined by a value of P<0.05 was considered to be statistically significant.

In this study, age distribution shows that the majority of the individuals are between 15 and 44 years old (78.39%), between 45 and 64 years (15.96%) and 1.39% aged 65 or older, respectively. Gender distribution is relatively balanced, with slightly more females (53.62%) than males (46.38%). Residency data indicates a higher percentage of individuals living in urban areas (58.91%) compared to rural areas (42.02%). Regarding economic conditions, over half of the individuals are in the lower economic category (56.49%). Table 2 compares the referral success rates between the case group and the control group. In the case group, 490 individuals (77.65%) experienced successful referrals, while 141 individuals (22.35%) did not. In contrast, the control group had a lower referral success rate, with 266 individuals (59.51%) experiencing successful referrals and 181 individuals (40.49%) not experiencing successful referrals. The difference in referral success rates between the case and control groups is statistically significant (p<0.001). Table 3 presents a comparison of successfully referred cases between two groups, Case (N=490) and Control (N=266), based on treatment adherence. Among the case group, 56 individuals (11.43%) were sputum-positive, compared to 30 individuals (11.28%) in the control group. The remaining individuals in both groups were sputum-negative, with 434 individuals (88.57%) in the case group and 236 individuals (88.72%) in the control group. These findings suggest that there is no significant difference in the proportion of sputum-positive and sputum-negative cases between the case and control groups concerning treatment adherence (p>0.05).

Table 1: Socio-demographical characteristics of the study participants (N=1078).

Table 2: Comparison of both groups based on referral success rates.

Table 3: Comparison of successfully referred cases in both groups based on treatment adherence.

The incentive study was prospective, quasi-experimental, using a non-equivalent group design, carried out at the two Chest Clinics of Dhaka City - Shyamoli and Chankharpul to ensure increased referral of TB suspects from two Chest Clinics to the diagnostic NTP-NGO clinics in Dhaka City. In this study, TB suspects referred to the NGO clinics for diagnosis from Shyamoli Chest Clinic were considered as CASE and received an incentive (transportation cost). On the other hand, TB suspects referred for diagnosis from Chankharpul were considered as CONTROL and did not receive any incentive. Technical Assistance Incorporated (TAI) has coordinated and supported the interventions designed by the National Tuberculosis Control Program (NTP) of Bangladesh for this study. A total of 1250 cases and 1250 controls were taken for the study purpose. In the meantime, as a part of ongoing urban DOTS expansion and strengthening and to ensure the quality of services to which suspects were referring, providers of both Chest Clinics and all NGO referral clinics of Dhaka City received DOTS training as part of the intervention. Our study found that individuals are between 15 and 44 years old, constituting 78.39% (845 individuals), with a slight predominance of females at 53.62% (578 individuals) compared to males at 46.38% (500 individuals). Regarding residency, a higher percentage of individuals reside in urban areas (58.91%, 635 individuals) compared to rural areas (42.02%, 453 individuals). In terms of economic condition, over half of the individuals are in the lower economic category (56.49%, 609 individuals), with 36.27% (391 individuals) in the middle economic category and a small proportion in the upper economic category (7.24%, 78 individuals). These findings are similar to previous studies [16-18]. The patient incentive consists of reimbursing the transportation cost of visiting another clinic in order to receive the service sought first at the Chest Clinic. Medical Officers of Shyamoli and Chankharpul Chest Clinics maintained suspect registers for all TB suspects. For referral of the suspects to an NGO center, the Chest Clinics used a referral slip. TB suspects at the Shyamoli Chest Clinic coming from the Chankharpul catchment area and TB suspects at the Chankharpul Chest Clinic coming from the Shyamoli catchment area were excluded from the study and not provided with any referral slips. Those suspects were diagnosed at the Chest Clinics and then referred to the usual existing procedure for DOTS. Also, TB suspects living within 1-2 km of the Chest Clinics were not referred for diagnosis. Suspects who were referred from Shyamoli Chest Clinic for the study received an average transportation cost. When issuing the referral slip, TB suspects were informed by the referring clinic that they would be paid a one-time transport allowance equivalent to Tk. 150/- once they report to the NGO center they had been referred to. NTP provided the Chest Clinic doctors with the detailed locations of the selected NGO centers. TAI, who was responsible for coordinating the study, deposited an advance to each of the listed NGO centers within the Shyamoli catchment area for payment of the transport allowance to the suspects upon their reporting to the NGO centers. TAl staff and study coordinator visited the NGO centers periodically to collect the vouchers from the NGO centers and provided further funds if required. At the end of each month during the study period, the coordinator prepared a basic monthly report. The significant difference in referral success rates between the Case and Control groups highlights the importance of transportation incentives. In the Case group, where participants received transportation incentives, 490 individuals (77.65%) experienced successful referrals, compared to only 266 individuals (59.51%) in the Control group, which did not receive incentives. The lower success rate in the Control group, with 181 individuals (40.49%) not experiencing successful referrals, underscores the barriers that transportation costs can pose. The statistically significant difference (p<0.001) demonstrates that providing transportation incentives effectively improves referral success rates by mitigating logistical challenges and encouraging individuals to attend their referral appointments. In the case group (N=490), 56 individuals (11.43%) were sputum positive and 434 individuals (88.57%) were sputum negative. In the Control group (N=266), 30 individuals (11.28%) were sputum positive and 236 individuals (88.72%) were sputum negative. The p-value of >0.05 indicates no statistically significant difference in the proportion of sputum-positive and sputum-negative cases between the two groups, suggesting similar treatment adherence in both groups. Our study suggests that treatment adherence is totally connected to the referral success rate. The more TB suspects are referred to the NGO clinic, the more likely they are to be diagnosed properly and treated properly. Despite the clear impact of transportation incentives on referral success, the study highlights a gap in research on this topic and further studies are needed to better understand the broader implications of such interventions on TB treatment outcomes.

Limitations of the study:

There are several limitations observed during study period:

• There was no previous data of referral rate for comparison with this study result. For study purpose, a three months data prior to incentive study is made available from information of both Chest Clinics.
• Administrative complicacy and negligence to study-work was seen, especially at Chankharpul Chest Clinic. As a result, referral rate was reduced time to time at Chankharpul Chest Clinic.

This study demonstrates the positive impact of transportation incentives on the referral success of tuberculosis (TB) suspects in Dhaka City. The provision of transportation allowances significantly improved referral rates, with 77.65% of participants in the case group successfully referred, compared to 59.51% in the control group. This highlights the importance of addressing logistical barriers to treatment access. However, no significant difference in treatment adherence was observed between the groups, indicating that referral success is crucial for ensuring proper diagnosis and treatment. Further research is necessary to explore the broader implications of such incentives on TB control efforts.

Funding:  Funded by USAID through NTP (WHO), Bangladesh and MSH(Boston) through TAI, Bangladesh

Conflict of interest: None declared

1. Hopewell PC, Jasmer RM. Overview of clinical tuberculosis. Tuberculosis and the tubercle bacillus. 2004 Dec 13:13-31.
2. Raviglione MC. The TB epidemic from 1992 to 2002. Tuberculosis. 2003 Feb 1;83(1-3):4-14.
3. Wells WF. Airborne contagion and air hygiene. Cambridge (MA): Harvard University Press; 1955. p. 13-19.
4. World Health Organization. TB and HIV/AIDS in the South-EAst Asia region. WHO Regional Office for South-East Asia; 2003.
5. World Health Organization. The World health report 1996: fighting disease, fostering development: executive summary. World Health Organization; 1996.
6. World Health Organization. What is DOTS?: a guide to understanding the WHO-recommended TB control strategy known as DOTS. World Health Organization; 1999.
7. Ahmed M. Promoting Public-private partnership in health and education: The case of Bangladesh. Public–private partnerships in the social sector: Issues and country experiences in Asia and the Pacific. 2000:219-91.
8. Ahn DI, World Health Organization. Addressing poverty in TB control: options for national TB control programmes. World Health Organization; 2005.
9. Guda DR, Khandaker IU, Parveen SD, Whitson T. Bangladesh: NGO and public sector tuberculosis service delivery-rapid assessment results. University Research Co, LLC, Bethesda, MD. 2004 Dec.
10. World Health Organization. Involving private medical practitioners in TB and STI control. WHO Regional Office for South-East Asia; 2001.
11. Loddenkemper R, Sagebiel D, Brendel A. Strategies against multidrug-resistant tuberculosis. European respiratory journal. 2002 Jul 1;20(36 suppl):66s-77s.
12. World Health Organization. TB control in the workplace. WHO Regional Office for South-East Asia; 2004.
13. Balasubramanian R, Garg R, Santha T, Gopi PG, Subramani R, Chandrasekaran V, Thomas A, Rajeswari R, Anandakrishnan S, Perumal M, Niruparani C. Gender disparities in tuberculosis: report from a rural DOTS programme in south India. The International Journal of Tuberculosis and Lung Disease. 2004 Mar 1;8(3):323-32.
14. Jaiswal A, Singh V, Ogden JA, Porter JD, Sharma PP, Sarin R, Arora VK, Jain RC. Adherence to tuberculosis treatment: lessons from the urban setting of Delhi, India. Tropical Medicine & International Health. 2003 Jul;8(7):625-33.
15. Mahendradhata Y, Lambert ML, Van Deun A, Matthys F, Boelaert M, Van Der Stuyft P. Strong general health care systems: a prerequisite to reach global tuberculosis control targets. The International journal of health planning and management. 2003 Oct;18(S1):S53-65.
16. Kiwuwa MS, Charles K, Harriet MK. Patient and health service delay in pulmonary tuberculosis patients attending a referral hospital: a cross-sectional study. BMC public health. 2005 Dec;5:1-7.
17. Yimer S, Bjune G, Alene G. Diagnostic and treatment delay among pulmonary tuberculosis patients in Ethiopia: a cross sectional study. BMC infectious diseases. 2005 Dec;5:1-7.
18. Wandwalo ER, Mørkve O. Delay in tuberculosis case-finding and treatment in Mwanza, Tanzania. The International Journal of Tuberculosis and Lung Disease. 2000 Feb 1;4(2):133-8.