Pakistan ranks fifth amongst TB high-burden countries worldwide. In 2015, National TB control (NTP) Pakistan notified 331,809 TB patients, whereas around 1,78,191 of the incident cases were still missing [1] . Case notification in Pakistan has stagnated over recent years, with the key challenges in TB control being limited engagement of the private healthcare sector, lack of community involvement and escalating number of multidrug-resistant tuberculosis cases [2] .

World Health Organization (WHO) recognizes the vital role of engaging the private sector in ending the global TB epidemic and has devised the Public-Private Mix (PPM) approach that aims to engage the private healthcare sector in TB control [3] . In Pakistan, the private sector is the first point of care for 75% of the population [4] . But 27% of TB patients being treated in the private sector are not notified to National TB surveillance system [5] . Pakistan implemented the PPM intervention in 2005 and incentives were introduced in 2015, the contribution of different models of PPM to total notified tuberculosis cases was 22% in 2015 [1] [6] .

Engaging private sector participation in notification of TB cases remains a challenge. As a result, NTP adopted the provision of cash incentives to solo private general physicians (GP) through NTP’s partners from July 2015 onwards [7] . However, this strategy has not been evaluated in Pakistan TB control program. The current study aims to assess the effect of cash incentives on tuberculosis case notification by private healthcare provides (PHCP) and sputum slide positivity rate (SPR) at private laboratories enrolled with the PPM-GP model in Pakistan.

An assessment of the overall tuberculosis case notification by PPM-GP model from 2013 to 2016 shows that twice as many cases were notified to the NTP in 2016 compared to (Figure 1).

During 2014, a total of 618 private healthcare providers (PHCP) were enrolled in the incentive scheme and maintained participation in the PPM program for the duration of January 2014 to December 2016. Among them, more than 50% (393) were situated in Punjab (Table 1).

An After the introduction of incentives, TB case notification increased by 71%, from 8168 patients in 2014 to 13,941 patients in 2016 (Table 2). A significant increase in TB case notification was found in Punjab, whereas a decrease was observed in Azad Jammu Kashmir (AJK), corresponding to the number of GPs situated in the provinces. Among the type of PHCP, pulmonologists notified double the number of TB cases as compared to 2014. The TB case contribution remained similar for medical specialist, pediatrician and others. 67% of PHCP had an increase in case notification, 6% no change and 27% reported a

PHCP = Private healthcare provider; GP = General Practitioner; Others: Surgeon, Orthopedic, Gynecologist, Dermatologis; t AJK = Azad Jammu Kashmir; ICT = Islamabad Capital Territory.

reduced number of cases. Furthermore, only 1% of the PHCPs contributed to 19% increase in case notification (Table 3).

After incentives, diagnostic slide positivity rate declined by 1.9% and follow-up slide positivity rate increased by 0.6%. Number of slides for diagnostic and follow-up testing increased by 82% and 72%, respectively (Table 4).

The study shows that cash incentives have significantly increased (71%)

AJK = Azad Jammu Kashmir ICT = Islamabad Capital Territory KPK = Khyber Pakhtun Khwa; HCP = Healthcare provider.

HCP = Health Care Provider.

SPR = Slide Positivity Rate.

tuberculosis case notification in Pakistan. Incentives are provided by Mercy Corps to the PHCPs in order to encourage participation of private sector in tuberculosis case notification as well as to ensure that the program rather than the patient pays for the consultation cost of the of the private provider. There have been multiple systematic reviews that have indicated an improved performance of PHCPs upon provision of cash incentives [8] [9] [10] [11] . Incentives in the form of free drugs, laboratory reagents, medical supplies, gift vouchers or cash payments have led to increased case notification and improved treatment outcomes [7] [12] . Studies show that little improvement in TB case treatment in different countries was observed when provided with incentives of small amounts [11] . While other studies in India reveal that private providers were willing to participate in TB control activities without any monetary incentives [13] [14] .

As the private sector is largely unregulated, there is a probability of non-adherence to NTP management guidelines. This can lead to delay in diagnosis, increased transmission, and transmission of multi-drug resistant tuberculosis due to poor treatment regimens and lack of compliance [15] . Studies have shown that as a result of engagement of private healthcare sector, there is improved access to TB care with minimization of out of pocket an expense owing to free anti-TB drugs and TB diagnostics [8] [11] [16] . Patients under treatment by specialists other than pulmonologists face a delays in being identified as presumptive TB case [17] . Therefore, one of the principles of the End TB strategy is to engage all care providers [18] . This makes incentives an important element of the PPM-GP model to motivate the for-profit PHCP to participate in TB control and make the program a success.

Among the type of healthcare providers, pulmonologists showed the greatest difference in case notification, with the number doubling after incentives. As pulmonologists are the most relevant specialist in the management of tuberculosis, this group is expected to have a high number of cases present, with incentives encouraging the reporting of their cases [17] .

Cash incentives to laboratory technicians for sputum smear microscopy demonstrate that there is remarkable increase in the number of sputum smear microscopy tests performed with a decrease of slide positivity rate for diagnostic by 1.9 and an increase for follow-up by 0.6 slide positivity rate. A decrease in diagnostic slide positivity rate may be due to high index of suspicion of healthcare providers leading to increased presumptive patient referral. Conversely, the increase in follow-up rate may be due to keen examination of the slides after multiple supervisory visits.

There were several strengths of the study, including a large sample size of all GPs who maintained participation in the program from all four provinces and three regions of Pakistan. In addition, the use of routinely collected data and the results derived from them reflect programmatic realities. Furthermore, large data base of 2 years was used for analysis. A limitation of this study is that review of national program record was relied upon to derive conclusions. Since the data is routinely collected, the accuracy and completeness cannot be ensured. Furthermore, it was not possible to identify other factors that may also have contributed to increased notification other than incentives. These factors are important to elucidate when provided with data that reveals that only 1% of the GPs contributed to 19% increase in case notification, whereas 27% GPs had reported a reduced number of cases.

This study shows that incentives have been effective in motivating a majority of the private healthcare providers in increasing TB patient notification. Thereby, serving as an important advocacy tool for involvement of the private healthcare providers in TB patient management after appropriate training and accompanied regular monitoring. Further quantitative and qualitative research is recommended to explore factors associated with higher case notification, apart from financial incentives.

This research was conducted through the Structured Operational Research and Training Initiative (SORT IT), a global partnership led by the Special Programme for Research and Training in Tropical Diseases at the World Health Organization (WHO/TDR). The training model is based on a course developed jointly by the International Union Against Tuberculosis and Lung Disease (The Union, Paris, France) and Médecins Sans Frontières (MSF, Geneva, Switzerland). The specific SORT IT programme that resulted in this publication was implemented by the National Tuberculosis Control Programme of Pakistan, through the support of the Global Fund to Fight AIDS, Tuberculosis and Malaria (The Global Fund, Geneva, Switzerland).

The authors acknowledge the support of Mr. Aamir Khan, Project Officer, Mercy Corps in compilation of data for this study. The authors are very much thankful to Muhammad Tariq, Ms. Hina Najmi and Mr. Waseemullah for their valuable inputs as participants of SORT IT 2017.

The publication fee was covered by the NTP through Global Fund, grant Pakistan.

Ashraf, R., Naureen, F., Noor, A., Ilyas, J., Fatima, R., Yaqoob, A., Wali, A., Haq, M.U., Latif, A. and Hussain, S. (2018) Does Cash Incentive Effect TB Case Notification by Public Private Mix-General Practitioners Model in Pakistan? Journal of Tuberculosis Research, 6, 166-174. https://doi.org/10.4236/jtr.2018.62016