Integrated prevention of mother-to-child transmission for human immunodeficiency virus, syphilis and hepatitis B virus in China

Abstract Problem China continues to face challenges in eliminating mother-to-child transmission of human immunodeficiency virus (HIV), syphilis and hepatitis B virus (HBV). Approach In 2010, a programme that integrated and standardized prevention of mother-to-child transmission (PMTCT) efforts for HIV, syphilis and HBV was implemented in 1156 counties. At participating antenatal care clinics, pregnant women were offered all three tests concurrently and free of charge. Further interventions such as free treatment, prophylaxis and testing for mothers and their children were provided for HIV and syphilis. Local setting China’s national PMTCT HIV programme started in 2003, at which time there were no national programmes for perinatal syphilis and HBV. In 2009, the rate of maternal-to-child transmission of HIV was 8.1% (57/702). Reported congenital syphilis was 60.8 per 100 000 live births. HBV infection was 7.2% of the overall population infected. Relevant changes Between 2010 and 2013 the number of pregnant women attending antenatal care clinics with integrated PMTCT services increased from 5.5 million to 13.1 million. In 2013, 12.7 million pregnant women were tested for HIV, 12.6 million for syphilis and 12.7 million for HBV. Mother-to-child transmission of HIV fell to 6.7% in 2013. Data on syphilis transmission are not yet available. Lessons learnt Integrated PMTCT services proved to be feasible and effective, and they are now part of the routine maternal and child health services provided to infected women. The services are provided through a collaboration between maternal and child health clinics, the national and local Centers for Disease Control and Prevention, and general hospitals.


Introduction
The World Health Organization (WHO) has called for integrated action to eliminate new paediatric human immunodeficiency virus (HIV) infection and congenital syphilis by 2015. 1,2 However, in 2009, mother-to-child transmission of these diseases was still high in China. At the end of 2009, the HIV prevalence in China was 0.057% (range: 0.042-0.071), with an estimated 740 000 people (range: 560 000-920 000) living with HIV. 3 Before the antiretroviral therapy era, the mother-to-child transmission rate was estimated to be 34.8%. 4 In 2009, this rate fell to 8.1% after widespread HIV screening of pregnant women, and HIV infected mothers were offered free antiretroviral prophylaxis for HIV and replacement feeding to avoid breast feeding their children.
Syphilis, caused by a spirochete bacterium, was seldom reported in the Chinese population two decades ago, however the incidence has increased to 24.7 cases per 100 000 people in 2009. 5 Reported congenital syphilis has increased from 25.5 per 100 000 live births in 2005 to 60.8 per 100 000 live births in 2009. 5 In addition, hepatitis B virus (HBV) is a public health problem. In 2006, 7.2% of the Chinese population aged 1-59 years were hepatitis B surface antigen positive. 6 In 2010, China's Ministry of Health began to integrate and standardize prevention of mother-to-child transmission (PMTCT) efforts for HIV, syphilis and HBV. Subsequently, the ministry initiated comprehensive services nationwide. In this report, we describe China's implementation of these integrated PMTCT services.

Local setting
Supported by the Government of China, the national PMTCT programme for HIV was initiated in 2003 and covered 453 counties, cities and districts by 2009. At the participating antenatal care clinics, free HIV screening was offered for pregnant women. The interventions for HIV-infected mothers included HIV-tailored midwifery services, free antiretroviral therapy or prophylaxis and practical guidance on infant feeding. Exposed infants received free antiretroviral medicines, HIV antibody testing at 12 and 18 months of age and developmental monitoring. In 2003 there were no nationwide programmes designed to prevent maternal transmission of syphilis and HBV.

Approach
To meet the WHO goals for elimination of paediatric HIV infection and congenital syphilis by 2015, China faced many national challenges. In the second half of 2010, the Government of China incorporated a nationwide PMTCT programme for HIV, syphilis and HBV into the existing maternal and child health-care system.
In February 2011, the Ministry of Health issued the Protocol for prevention of mother-to-child transmission of HIV, syphilis and hepatitis B, which contained the govern-Lessons from the field Prevention of mother-to-child transmission in China Ai-Ling Wang et al. ment's response strategy, intervention measures, and requirements regarding organization and management. 7 The protocol provided guidance to all regions for implementation of integrated PMTCT efforts for HIV, syphilis and hepatitis B. It also reiterated the official policy of strengthening government leadership, ensuring that all departments fulfil their respective responsibilities, promoting full social mobilization and broad participation, integrating service resources, improving intervention quality, expanding coverage and promoting standardization. 7 From 2010 to 2013, the central government allocated over 3.4 billion Yuan (573 million United States dollars), to implement these services.
For PMTCT, testing and counselling are the first intervention steps within the antenatal care environment. In 2010, health-care facilities providing midwifery and antenatal care services that participated in the programme at provincial, prefecture, county and township levels started to offer free HIV, syphilis and hepatitis B counselling and testing for pregnant women. Free PMTCT interventions were provided to all infected mothers and their children throughout the nation.
The interventions for HIV were identical to interventions in the original national PMTCT programme for HIV, except that the current programme offered early HIV diagnosis for exposed infants at 6-8 weeks of age.
Mothers infected with syphilis were provided free treatment with 2.5 million units of intramuscular benzathine penicillin once a week for three weeks and appropriate midwifery services to prevent transmission during labour. Exposed infants were provided with free prophylaxis with benzathine penicillin and offered testing for syphilis every three months up to 18 months of age. For infected infants, free treatment was offered.
Children born to women testing positive for hepatitis B surface antigen were provided with free hepatitis B immunoglobulin (100 IU) within 24 hours after birth and three hepatitis B vaccinations within 24 hours of birth, at 1 month and 6 months of age, in accordance with national guidelines. 8 Testing and treatment of children were not covered by the programme.
The programme supported training of health-care providers. Between 2010 and 2012 training-of-trainers was provided yearly at national and provincial level on the elements of the PMTCT care cascade. The training lasted for approximately three days. Subsequently, at provincial and prefectural level, the instructors held yearly training sessions, that normally lasted for 1-3 days, for local health-care providers to improve programme capacity. Health-care providers were trained on implementation of integrated PMTCT interventions and management of infected pregnant women and their children. They were also trained in data collection. Staff were trained in data management and analysis. The National Center for Women and Children's Health incorporated all PMTCT data on HIV, syphilis and HBV into the pre-existing management information system of the national PMTCT programme.

Relevant changes
By 2013 the programme covered 41% (1156/2853) of counties, cities and districts within 31 provinces, autonomous regions and municipalities in China. In six provinces, autonomous regions and municipalities with the most serious epidemics, all counties were covered.
The PMTCT programme reached 13.1 million pregnant women in 2013, 8.7 million more than in 2009. Of these, 12.7 million were tested for HIV antibodies, representing an increase in testing rates from 85.4% in 2009 to 97.3% in 2013. There was a 63.1% increase in pregnant women diagnosed with HIV, from 3662 cases in 2009 to 5973 cases in 2013. Mother-to-child transmission of HIV fell from 8.1% (57/702) in 2009 to 6.7% (145/2180) in 2013. In the same year, 12.6 million pregnant women in the programme were also tested for syphilis, covering 96.4% of women reached by the integrated programme. We commenced data collection on mother-to-child transmission of syphilis in the latter half of 2012. To be able to exclude transmission, syphilis-infected

Lessons learnt
Integrated prevention of three verticallytransmitted diseases -HIV, syphilis and HBV -proved to be feasible and effective at a large scale in China.
Pregnant women were offered all three tests concurrently, free of charge. The programme was fully nested within the existing maternal and child health-care system in China at county, township, and village levels. Pregnant women infected with HIV, syphilis or HBV were immediately enrolled for integrated PMTCT programme services as a part of their routine antenatal, postnatal, and children's care. Maternal and child health clinics, the national and local Centers for Disease Control and Prevention, and general hospitals collaborated well, which led to a successful implementation of the programme (Box 1). The integrated PMTCT programme has helped China meet the WHO goal. Implementing the integrated programme involved challenges including shortage of human resources, quality of services, and suboptimal availability of services in some areas. To address the concerns about availability, the Government of China has expanded the integrated PMTCT programme to 1638 counties in August 2014, using the same strategy that had been deployed in 2010. This expansion will allow more pregnant women to access free integrated PMTCT services. Improving the capacity of health-care staff and quality-associated monitoring and evaluation through further training will be our future focus.
In conclusion, the expansion of the integrated PMTCT programme both in content and coverage can significantly contribute towards achieving the dual goal of eliminating paediatric HIV infection and congenital syphilis, as well as addressing the ongoing burden of perinatal HBV transmission. Our experience took place in a large population with high disease burdens. The Chinese model may be of interest to other nations that seek to better integrate HIV, syphilis and HBV services into the broader maternal and child health context. ■ Funding: All funding was provided by the National Health and Family Planning Commission, China.
Funding: SHV's engagement was supported by an NIH Fogarty training grant, D43 TW001035 and R01AI094562.
Competing interests: None declared. Lessons from the field Prevention of mother-to-child transmission in China Ai-Ling Wang et al.

Prevention of mother-to-child transmission in China
Ai-Ling Wang et al.