Monetary incentives for provision of syphilis screening, Yunnan, China

Abstract Problem Early detection of syphilis-infected people followed by effective treatment is essential for syphilis prevention and control. Approach Starting in 2010 the local health authority in Yunnan province, China, developed a network of 670 service sites for syphilis testing, diagnosis and treatment or for testing-only with referral for further diagnosis and treatment. Point-of-care tests for syphilis and syphilis interventions were integrated into the existing human immunodeficiency virus (HIV) prevention and control programme. To improve the syphilis services, a pay-for-performance scheme was introduced in which providers were paid for testing and treating patients. Local setting Yunnan province is the region hardest hit by HIV infection and disproportionately burdened with syphilis cases in China. Relevant changes The proportion of attendees at voluntary counselling and testing clinics who were tested for syphilis increased from 46.2% (32 877/71 162) in 2010 to 98.2% (68 012/69 259) in 2015. Syphilis-infected cases treated with the recommended therapy increased from 26.6% (264/993) in 2010 to 82.5% (453/549) in 2015 at designated testing, diagnosis and treatment sites. Lessons learnt The strategy greatly increased the uptake of syphilis testing and treatment among people at risk. Introduction of point-of-care tests for syphilis increased coverage of the testing services. Introduction of a pay-for-performance scheme seemed to motivate health-care providers to undertake syphilis intervention services.


Introduction
Syphilis is a sexually transmitted disease caused by the bacterium Treponema pallidum subspecies pallidum. Approximately 3 million people aged 15-49 years were infected with syphilis in China in 2011, 1 accounting for a large proportion of the estimated 17 721 000 cases globally in 2012. 2 Despite continuous efforts to promote condom use, 3 syphilis transmission has not been prevented effectively, resulting in an increase of reported cases in the country since 2000. 4 To control the epidemic, in 2010 the health ministry in China launched its National Programme for Prevention and Control of Syphilis (2010-2020). 5,6 Based on evidence from pilot studies, syphilis control efforts in China include early detection of infection through enhanced screening efforts followed by treatment of infected cases. The core intervention strategy has been described as the three-by-one approach, meaning that there are three entry points to screening linked to one standardized mode of care. 5,7 The three settings are: (i) sexually transmitted disease clinics; (ii) human immunodeficiency virus (HIV) testing clinics (usually voluntary counselling and testing centres, and methadone maintenance treatment centres); and (iii) out-of-clinic settings where outreach services are delivered to sex workers and men who have sex with men. Standardized care provided to infected people consists of treatment with benzathine benzylpenicillin, behavioural interventions and partner notification. 5 Screening also started in antenatal clinics after 2011 when syphilis was integrated into a separate programme for prevention of mother-to-child transmission of HIV and hepatitis B virus. 8 We describe the approaches used to scale-up the syphilis screening and treatment interventions in Yunnan province.

Local setting
Yunnan province, with a population of 47 million in 2015, is located in the south-west of the country and is the region hardest hit by HIV infection in China. By the end of 2010, the cumulative reported number of people with HIV infection and acquired immune deficiency syndrome (AIDS) in Yunnan was 83 925; accounting for 21.0% of the total national figure of 399 643. 9 The province is also disproportionately burdened with syphilis cases. Approximately 7000 people with different stages of syphilis infection were reported in 2011 among 45 966 362 residents, an incidence of 15 per 100 000 people. 10 To respond effectively to the increasing epidemic of HIV, a province-wide campaign to prevent and control HIV/AIDS was initiated in Yunnan in 2005. For the initiative, the Yunnan government established a functional network of HIV testing services in health facilities, which provided opportunities for integrating interventions targeted at other sexually transmitted diseases. In addition, introduction of point-of-care tests for syphilis in China allowed an expansion of syphilis testing in clinics and out-of-clinic settings, such as outreach services or sometimes pharmacies, in the province. 11 Moreover, the central government issued a specific policy to ensure the availability of benzathine benzylpenicillin in health facilities for syphilis treatment. 7 Supplies were ensured through advocacy efforts together with site supervision and monitoring.
Health allocated public health funds for syphilis testing and treatment services.
Through a situation analysis, the local health facilities were mapped, evaluated for capacity and then categorized as sites for syphilis testing, diagnosis and treatment or sites for syphilis testing only. These were primary-care centres or community and township hospitals. A total of 363 sites across Yunnan province, including all the 130 antenatal clinics, were officially designated as testing, diagnosis and treatment sites by the provincial authority to ensure that each of 129 districts or counties had at least one such site. An additional 307 testing-only sites were established by equipping existing facilities with treponemal point-ofcare test kits (immunochromatographic strips for finger-prick blood).
In 2012, 436 (81.0%) of the 538 sites in place could provide both treponemal testing (Treponema pallidum particle agglutination, enzyme immunoassay or immunochromatographic assay) and non-treponemal testing (toluidine red unheated serum test or rapid plasma reagin test). By 2015 the number of sites had increased to 670, of which 635 (94.8%) were equipped with both type of tests. Outreach teams from communitybased organizations were also equipped to conduct point-of-care tests. The cost to patients of a syphilis test is normally 20 Chinese yuan or about 3 United States dollars (US$; 6.8 Chinese yuan = 1 US$ in 2017), but the programme provided testing free-of-charge in all the designated antenatal care settings.
To encourage people to seek syphilis screening, health promotion efforts were integrated into the ongoing HIV health education programme, via leaflets, posters and AIDS Day health promotion activities. An opt-out screening for syphilis was offered to people attending sexually transmitted disease clinics, voluntary counselling and testing sites, and methadone maintenance treatment clinics. For people testing positive at the designated testing, diagnosis and treatment sites, treatment was started immediately with intramuscular injection of benzathine benzylpenicillin 2.4 million units (MU) weekly for 2-3 weeks. For those testing positive at testing-only sites or at outreach services, staff gave patients a referral card with the address, telephone number and contact person at the nearest site where the diagnosis could be confirmed and treatment provided. Pregnant women were routinely screened for syphilis at their first visit to an antenatal clinic and, if positive, treated for infection at the same clinic.
Training and re-training of local staff on how to perform point-of-care testing or on health promotion was a mandate of designated local centres for disease control. Approximately 4000 people annually were trained or re-trained in 1-2 day training courses at provincial, district and county levels. The trainers were disease control spe-  Lessons from the field Syphilis screening and treatment in China Wanyue Zhang et al.

cialists, doctors, nurses and outreach paramedical workers.
To improve implementation of the testing, referral and treatment services, a pay-for-performance scheme was introduced in 2011. The scheme consisted of two mechanisms. The first was a purchase mechanism, by which public health subsidies were provided through an outsourcing contract to compensate sites for the services provided. Specifically, health-care providers at testingonly sites or outreach teams were paid 20 yuan for successful referral of a person positive for syphilis. Providers at testing, diagnosis and treatment sites were paid 20 yuan (US$ 3.03) for treating a referred patient with the recommended regimen. The second mechanism was an assessment by the local health authority of the performance of the sites in delivering these services. Advice and recommendations were provided after the site assessment, and payment was made if performance met the requirements.

Relevant changes
The programme's data collection and reporting system showed that over the  (Table 1 and Fig. 2).
Data from sentinel surveillance indicated a decline in syphilis prevalence The mean cost for the additional investment in pay-for-performance was around US$ 39 000 annually (range: US$ 35 000-70 000).

Lessons learnt
A specific effort in screening and treatment of syphilis in Yunnan has resulted in an increased uptake of syphilis testing and corresponding increase in treatment of infected cases. In addition to health promotion efforts which have been active for some time, two factors may have contributed to the increases. First, there was a province-wide HIV prevention and control programme in place in which the syphilis intervention services could be easily integrated to increase the uptake of syphilis testing. Second, the pay-for-performance scheme appeared to motivate health-care professionals to undertake syphilis intervention services.
The main lessons learnt are summarized in Box 1. Introduction of point-of-care tests for syphilis served as a facilitator for scaling-up of testing for syphilis, 13,14 thereby creating a testing network covering 670 sites across Yunnan province. Furthermore, integrating syphilis testing into the existing services in government health facilities as well as the outreach services of communitybased organizations resulted in an increased proportion of people tested and treated for syphilis. One of these strategies, pay-for-performance has been widely implemented in many countries, with varying levels of success. 15,16 Despite the successes, several challenges remain. Although the costs are not high in relation to the provincial government budget for sexually transmitted disease control (more than US$ 2.5 million), the sustainability of local investments in pay-for-performance is a challenge. Treatment for chlamydia or other sexually transmitted infections did not benefit from the pay-for-performance scheme and may have been neglected. We therefore need to determine whether the benefits of

Box 1. Summary of main lessons learnt
• Syphilis screening and treatment services were integrated into the existing human immunodeficiency virus programme as public health interventions in Yunnan province. • Establishing a network of testing-only and testing, diagnosis and treatment sites across the province facilitated people's access to syphilis screening and treatment services. • Introduction and implementation of a pay-for-performance scheme appeared to motivate providers to increase the provision of syphilis testing, referral and treatment services. We also need to know whether implementation of pay-for-performance compromises the voluntary nature of testing.
In summary, introduction of financial incentives to providers could be linked to increased uptake of syphilis testing and treatment in the study area. These increases reinforce the need to collect further information on the feasibility, acceptability and cost-effectiveness of introducing pay-for-performance within the national or provincial health services and to translate evidence to policy for responding to the syphilis epidemic in China. ■ Leçons tirées La stratégie a permis d'accroître considérablement le recours au dépistage et au traitement de la syphilis par les personnes vulnérables. L'utilisation de tests de dépistage de la syphilis sur les lieux des soins a permis d'augmenter le nombre de bénéficiaires des services de dépistage. La mise en place d'un système de rémunération aux résultats a semblé inciter les prestataires de soins de santé à pratiquer des interventions ciblant la syphilis.

Incentivos monetarios para la provisión de pruebas de detección de la sífilis, Yunnan, China
Situación La detección temprana de las personas infectadas por la sífilis seguida de un tratamiento efectivo es esencial para la prevención y el control de la enfermedad. Enfoque Desde 2010, la autoridad sanitaria local de la provincia de Yunnan, China, desarrolló una red de 670 puntos de servicio para llevar a cabo las pruebas, el diagnóstico y el tratamiento de la sífilis o solo para llevar a cabo las pruebas con derivación a diagnóstico y tratamiento posteriores. Las pruebas en el punto de atención para la sífilis y sus intervenciones se integraron en el programa de prevención y control del virus de la inmunodeficiencia humana (VIH) existente. Para mejorar los servicios relativos a la sífilis, se introdujo un programa de pago por desempeño en el que los profesionales recibían un pago por hacer pruebas y tratar a pacientes. Marco regional La provincia de Yunnan es la región más afectada por la infección por VIH y una cantidad desproporcionada de casos de sífilis en China.