The increase of sexually transmitted infections calls for simultaneous preventive intervention for more effectively containing HIV epidemics in China

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1 DOI: / Original article The increase of sexually transmitted infections calls for simultaneous preventive intervention for more effectively containing HIV epidemics in China N Zheng, a,b, * Y Guo, a,b, * S Padmadas, c B Wang, d ZWu a,b a Centre for Public Health Research, b State Key Laboratory of Analytical Chemistry for Life Science, Nanjing University, Nanjing, China c Division of Social Statistics, Southampton Statistical Sciences Research Institute, University of Southampton, Southampton, UK d Institute of Sexually Transmitted Diseases, Chinese Academy of Medicines, Nanjing, China Correspondence: Z Wu, Centre for Public Health Research, Nanjing University, 22 Hankou Road, Nanjing , China. wzhw@nju.edu.cn Accepted 19 June Objective To identify the priority public health challenges with respect to the development of multipurpose prevention technologies in China. Design Review of published literature, databases of state and local disease control agencies and unpublished data relating to HIV and other sexually transmitted infections (STIs). Setting China. Population General and migrant populations. Methods Review of published data, government reports and databases of China Disease Control agencies, and our unpublished studies. Main outcome measures Reported STI incidence, particularly HIV, syphilis, chlamydia and genital herpes, and the migrant population with respect to disease transmission. Results We found that the reported STI incidence increases along with that of HIV and showed significant geographic overlap with HIV. Economic migrant workers may facilitate the spread of STIs, including HIV. Conclusions To more effectively contain the HIV epidemic, it is imperative to develop preventive measures to simultaneously target HIV and other STIs. We recommend that the development of multipurpose prevention technologies in China should target HIV and STIs. Keywords HIV/AIDS, mobile population, multipurpose prevention technology strategies, sexually transmitted infections. Please cite this paper as: Zheng N, Guo Y, Padmadas S, Wang B, Wu Z. The increase of sexually transmitted infections calls for simultaneous preventive intervention for more effectively containing HIV epidemics in China. BJOG 2014; 121 (Suppl. 5): Introduction HIV epidemics have undergone dramatic changes in China, from dominantly blood-borne transmission in the early 1980s through the 1990s to predominantly sexually mediated transmission at the start of the 21st century. 1,2 Epidemiological studies have shown that sexual transmission accounted for more than 80% of new HIV infections in 2012 and this trend of increase is expected to continue. One hallmark of the increased role of sexual transmission in the HIV *These authors contributed equally. epidemic is the dramatically increased number of new infections in men who have sex with men (MSM) since the beginning of the epidemic. The number of females remains disproportionately high among the newly infected cases 3 in the context of their proportion of the population. The HIV epidemic also exhibits distinct geographic characteristics with respect to the routes of transmission. 2,4 Once almost completely eliminated, other sexually transmitted infections (STIs), such as syphilis and chlamydia, are on the rise again. 5 Studies show that the number of annually reported cases of STIs increased to in the early 21st century from about in ,7 Regional mapping of STIs indicated ª 2014 Royal College of Obstetricians and Gynaecologists 35

2 Zheng et al. geographic overlap with HIV-1, suggesting possible correlation of the infections. As China undergoes sustained economic development and urbanisation, an unprecedented number of migrants move from economically less developed regions to better developed urban areas for employment, creating an enormous mobile population (migrant workers). Data from the sixth state population census ( showed that in 2010 the mobile population of China was million. Compared with the fifth state population census data obtained in 2000 ( the mobile population increased 81% during that decade and this trend is predicted to continue over the next 20 years. Most of the mobile population comes from rural China, are adolescents with only primary or secondary education, and work in the low-wage industries or service sectors. 8 Therefore, this demographic poses one of the major public health challenges with respect to communicable diseases. In addition, increasingly open attitudes towards sexuality 9 and unprotected sexual intercourse 10 demand easily accessible technologies for preventing HIV-1 infection and other STIs. 8 Multipurpose prevention technologies (MPTs) are products designed to simultaneously protect women from unintended pregnancy, HIV and other STIs. The implementation of MPT strategies requires the identification of key regional public health priorities and the design of MPT approaches to best meet the needs of the target population. HIV/AIDS prevention has been a national priority in China and an integrated policy has been implemented to reduce new infections. However, as STI incidence continues to increase, a single-focus preventive approach targeting HIV alone will not be sufficient. It is imperative to develop a technological platform dealing simultaneously with preventing HIV and sexually transmitted infections for more effective containment of new HIV infections and other STIs in China. Methods We reviewed published data as well as data from state and local disease control agencies with respect to HIV and STI epidemics in China. Our analysis emphasised the geographical distribution of STI incidence and the potential relationship to economic migration. HIV, STIs, syphilis, gonorrhoea, incidence and prevalence of STIs and HIV were used as keywords to collect published data. As a complement to the data collected from English publications, data taken directly from the official reports of Nationwide STD surveillance system of China, published in Chinese as National Center for STD Control (NCSTD) reports ( were also included in the analysis. In addition, the fifth and sixth state population census data (published in Chinese) were collected from the National Bureau of Statistics of PRC ( Both NCSTD reports and state population census reports comprise the respective data from each of 31 provinces in mainland China. The Statistical Package for the Social Sciences (SPSS) package was used for statistic analysis (SPSS Inc., Chicago, IL, USA). MS EXCEL and CHINA DATA MAP PLUG-IN ( were used in the geographical analysis and illustration. Results Changing face of China s HIV epidemics The Chinese Ministry of Health estimated that the number of people living with HIV increased to in Infections through sexual contacts have increased from 9.8% in 2005 to 81.6% in 2011 (UNAIDS, 2005, 2011). 3,11 As the HIV epidemic started through blood-borne transmission in many other countries, the Chinese HIV-1 epidemic started in certain blood-borne high-risk groups such as intravenous drug users and, uniquely, former blood and plasma donors in geographically disparate rural areas. However, heterosexual and homosexual transmission of HIV have rapidly increased since 2006 and are now the dominant routes for new infection (Figure 1). In particular, new infections have increased rapidly among MSM and among female sex workers (FSWs). Although the overall prevalence of HIV in China is low because of the large base population of the country, there are a number of high-prevalence geographic areas. In 2009, there were six provinces with high prevalence ranging from 1 to 7%; these provinces Yunnan, Guangxi, Henan, Sichuan, Xinjiang and Guangdong accounted for 77.1% of the total cases. In contrast to the global AIDS epidemics in many settings where the hardest hit regions tend to be the economically disadvantaged, the economically well-developed Guangdong Province is one of the provinces with the highest prevalence in China. Experts have even termed it the Guangdong phenomenon as it exemplifies the many social and economic factors in China facilitating the sexual transmission of HIV. These factors include emergence and/or re-emergence of STIs, inadequate social welfare and public health infrastructure and the presence of a large migrant population that tends to concentrate in economically well-developed regions. Increasingly open attitudes towards sexuality also facilitate the spread of STIs as casual sex and having multiple sexual partners are becoming common. A recent study found that casual sex is an important risk factor for the acquisition of STIs in China, 9 and sexual intercourse among adolescents is increasingly common. According to the results of a Chinese Youth Risk Behaviour Survey carried out in high-school students and college students (age range years) in 18 provinces in 36 ª 2014 Royal College of Obstetricians and Gynaecologists

3 STI prevention and HIV epidemic in China Annual transmission cons tute of reported (%) Heterosexual Homosexual IDU Blood MTCT Unknown Figure 1. Percentage of transmission routes of reported HIV cases in China from 1985 to 2011 (2012 China AIDS Response Progress Report, UNAIDS). China, 4.8% of high school students and 11.3% of college students reported that they had experienced sexual intercourse. Notably, 50.3% of the college students reported that they had engaged in high-risk sexual behaviour without using condoms. Moreover, 24% of the college students who had experienced sexual intercourse reported an unintended pregnancy. 10 In view of China s growing HIV epidemic through sexual transmission, more effective preventive measures are urgently needed. Emergence and re-emergence of STIs Since the 1980s, STIs have shown dramatic increases. Available data show that annually reported STI cases increased from in 1986 to in 2000, a more than 36-fold increase in 15 years. (China CDC, unpubl data). As only syphilis and gonorrhoea are STIs for which national registration is mandatory, it is likely that the numbers of reported STI cases are underestimates of the real prevalence of the infections. In 1991, national statistics showed that gonorrhoea was the dominant STI, accounting for 65% of total cases, while genital warts were second at 25%. Syphilis accounted for only 1.08% of the total cases. In 2005, nongonococcal urethritis became the dominant STI (37% of all STIs) and gonorrhea and genital warts decreased to 24% and 18.85%, respectively. 11 However, the prevalence of drug-resistant Neisseria gonorrhoeae increased during this time. According to a study carried out in Guangzhou, the prevalence of N. gonorrhoeae isolates resistant to penicillin, tetracycline and ciprofloxacin remains high from 85%, 85% and 78% in 2001 to 81.9%, 100% and 98.4% in 2011, respectively. 12 On the other hand, although the overall prevalence of gonorrhoea in the general population was low, 0.02% for men and 0.08% for women, 13 gonorrhoea is highly prevalent in high-risk groups, particularly among FSWs In the same period, syphilis increased to 16%, an almost 16-fold increase. By 2008, syphilis showed a further increase to account for 37.5% of the total cases of STIs, more than double the cases in 2005, as shown in Figure 2. Syphilis has shown a dramatic comeback from almost no reported cases in 1979 to more than reported cases in FSWs and MSM are at the highest risk of Treponema pallidum infection, which causes syphilis. A review study found that the prevalence of syphilis was 12.5% in imprisoned FSWs, 3.0% in FSW clients, 6.8% in intravenous drug users and 14.6% in MSM. 17 Studies indicated that FSWs from low-tier venues (such as street FSWs) had extremely high syphilis prevalence of 10 38%. 18 A detailed study of syphilis and HIV-1 infections among FSWs found that overall, FSWs were at high risk of being infected by both HIV-1 and syphilis, and those working at the lower end of the business (e.g. roadside call girl, FSWs in rental apartments) had significantly higher risk of becoming HIV or T. pallidum (syphilis) infected (Table 1). 11 Available data also showed that peasants and herdsman had among the highest incidences of new T. pallidum infections in 2012, and peasants accounted for 38.13% and 31.38% of new syphilis and gonorrhea cases, respectively. 11 Peasants and herdsmen tend to have lower incomes and limited medical coverage, and herdsmen resemble migrants in that they migrate seasonally. Although Chlamydia trachomatis infection is not a mandatorily reportable STI in the national STI surveillance programme in China, it is believed to be the most prevalent bacterial STI in China. A population-based study in 1999 found a prevalence of 2.1% among men and 2.6% among women. 13 FSWs have the highest prevalence of chlamydia infection. 11 A study of the MSM population in Shenzhen found that a much higher prevalence for anorectal chlamydia infection (24.4%) than urethral infection (5.3%). 19 ª 2014 Royal College of Obstetricians and Gynaecologists 37

4 Zheng et al. Syphilis 1.08% NGU 5.64% Genital herpes 0.34% Others 2.60% Genital warts 25.12% Ratio of STIs in China in 1991 Gonorrhea 65.22% Syphilis 16.17% Genital herpes 3.94% Others 0.13% NGU 36.78% Genital warts 18.85% Gonorrhea 24.14% Ratio of STIs in China in 2005 Gonorrhea 17.70% Genital herpes 5.30% Syphilis 37.50% Genital warts 18.80% Ratio of STIs in China in 2008 Chlamydia 20.69% Figure 2. Composition of annually reported STIs in China in 1991, 2005 and 2008 (NCSTD: Epidemiologic Reports of Syphilis and Gonorrhea Case Reports in China [ Herpes simplex virus type 2 (HSV-2) infection is the main cause of genital herpes. HSV-2 infection was also high among FSWs (30 70% seroprevalence) 14,20,21 and MSM (8 30% seroprevalence). 22,23 Together, the data suggest that there is a significantly higher incidence of STIs in individuals engaging in high-risk sex and using commercial sex workers. Geographic distribution of HIV-1 and syphilis cases Most of the nearly one million people living with HIV in China, live in six of China s 33 provinces: Yunnan, Guangxi, Henan, Sichuan, Xinjiang and Guangdong. These coastal provinces reported the highest number of HIV and AIDS cases, representing approximately 70 80% of the 38 ª 2014 Royal College of Obstetricians and Gynaecologists

5 STI prevention and HIV epidemic in China Table 1. Correlation of syphilis and HIV infection in China Location Syphilis infection HIV-1 infection No. of people % No. of people A B C Total Chi-square P < P < A: karaoke, disco, teahouse, star-rated hotel; B: hair salon, massage parlour, beauty salon, foot massage, roadside guesthouse etc.; C: roadside call girl, rental apartment. national total. 3 The geographic distribution of syphilis and gonorrhoea incidence in 2012 exhibited an overlap with that of HIV-1, with Guanxi, Guangdong and Xinjiang having the highest number of cases of both infections (Figure 3). The coastal provinces, such as Fujian, Zhejiang and Jiangsu, and Beijing and Tianjing municipalities, also have high syphilis and gonorrhoea incidence rates, as shown in Figure 3(A). 11 These coastal provinces and municipalities are among the most economically developed regions with the largest mobile populations, consistent with a study that found a greater number of reported syphilis cases in counties with a higher standard of living. 24 In a 2006 study in India, the elevated risk of HIV-1 infection that was observed among participants with incident syphilis supports the hypothesis that syphilis may enhance the sexual transmission of HIV-1 and highlights the importance of early diagnosis and treatment of syphilis. 25 Recent findings that concordant syphilis and HIV infections increased in China require new public health strategies, such as providing simultaneous HIV screening and consultation to people with STIs and their sexual partners. Many key behavioural and partnership risk factors for syphilis are also risk behaviours for HIV transmission and point to the need for integrated strategies that tackle prevention of both HIV and syphilis. Simplified procedures for syphilis screening should be available in genito-urinary medicine settings, along with targeted community outreach prevention interventions. 4,26 Migrant workers are susceptible to STIs and may contribute to the spread of HIV-1 National census data showed that in 2009 China had a migrant population of 211 million, accounting for 16.5% of the total population. The mean age of migrants was 27.3 years, with the vast majority (78.7%) from the countryside and from agriculturally registered households (Hu Kou). Migrants generally have little education; fewer than 20% % have any skill training. Most of the migrants do not have adequate health insurance and 52% do not have any health insurance policy. Many migrants do not use medical facilities, at least partly for economic reasons. They mostly work in manufacturing, retail and service industries, and are concentrated in low-paying and high-risk jobs. The state census predicted that the trend of population mobility will continue in the next 20 years. 8 In some municipalities, the migrant population constitutes a significant proportion of the overall population. The general trend of population mobility and urbanisation centres in China are shown in Figure 4 and Table 2, based on the fifth (2000) and sixth (2010) state population census data (National Bureau of Statistics of China, For example, a majority of the population in Shenzheng and Dongguan of Guangdong province are migrants (4.06 million out of a total 5.57 million, and 4.4 million out of 6 million, respectively). 8 Both cities are important economic centres in China. In Guangdong, more than 50% of new cases of HIV/AIDS were identified in migrant workers. In Dongguan, over 90% of new HIV cases were in the migrant population. A number of studies have investigated sexual behaviours, prevalence of HIV-1 and STI incidence in the migrant population. Migrants were more likely to engage in STI-associated risk behaviours than nonmigrants (e.g. receiving money for sex). Data from another study conducted in two major economic centres in 2002/03, 27 Beijing and Nanjing, showed that about 70% of the migrants surveyed had more than one sexual partner, and only small numbers often (10%) or always (8%) used condoms during sex. The same study also found that mobility was associated significantly with increased STI risk across both sexes. Among migrants, women were more likely than men to have STIs, including HIV. The high STI prevalence among migrants highlights an urgent need to implement comprehensive prevention and intervention programmes targeting the cultural, social and structural needs of migrants in the city, especially migrant women. 14,15 In addition, the imbalance of sexes may also increase the risks of STIs. China has seen persistent imbalance of sexes for cultural, social and economic reasons. The data from the sixth national census in 2010 showed that the ratio of boys to girls was at 117.7/100 and the cumulative impact of years of imbalance can have a huge impact on various aspects of social life. Previous findings suggest that an imbalance of opposite-sex partners will increase the risk of early, frequent, and multi-partner sex, thereby increasing risk of sexually transmitted infection. 28 Discussion Main findings This review of the data on HIV and other STI epidemics in China notes that HIV transmission shifted from mainly ª 2014 Royal College of Obstetricians and Gynaecologists 39

6 Zheng et al. A B Figure 3. (A) Incidence of total mandatorily reportable STIs (syphilis and gonorrhoea) in 2012 by province, Data source: Nationwide STI surveillance system. (B) Geographical distribution of cumulative HIV/AIDS cases (as of 31 December 2011) (2012 China AIDS Response Progress Report, UNAIDS). 40 ª 2014 Royal College of Obstetricians and Gynaecologists

7 STI prevention and HIV epidemic in China A B Figure 4. (A) China population growth by province, figures based on the fifth and sixth state population census data (National Bureau of Statistics of China, [ (B) China s Urbanisation Centres, figures based on the sixth state population census data (National Bureau of Statistics of China, ª 2014 Royal College of Obstetricians and Gynaecologists 41

8 Zheng et al. Table 2. Cities with mobile population more than in 2003 in China ( ) City Total population ( ) Registration population ( ) Mobile population ( ) Dongguan Shenzhen Beijing Shanghai Guangzhou Foshan Hangzhou Wenzhou Wuhan Zhongshan Nanjing Ningbo Suzhou Tianjin Wuxi Xiamen Zhanjiang Shenyang Xi an Chengdu Changzhou Jinan Qingdao Dalian Kunming Chongqing blood-borne transmission early in the epidemic to the current epidemic where the main mode of transmission is sexual. Parallel with this shifting HIV epidemic is the dramatic emergence and re-emergence of STIs, including a rapid increase in the prevalence and incidence of syphilis. The epidemics of HIV and syphilis show some geographic overlap and a number of economically well-developed regions have high incidence rates of both HIV and syphilis. These regions also have high migrant populations, in some settings comprising some 70% of the total population. Strengths and limitations The recorded incidence of STIs may be biased by China s rules on reportable STIs in that data for mandatorily reportable STIs (syphilis and gonorrhoea) are likely to be more reliable than that for those STIs (nongonococcal urethritis, genital herpes) that do not have mandatory reporting requirements, and therefore may be underestimated. The reported incidence of all STIs can be affected by availability of regional sentinel sites, health infrastructure and detection methods used. Interpretation Since the first cases among local recipients of contaminated blood products in the mid-1980s, HIV-1 has spread to all parts of mainland China. The major route for HIV transmission has shifted from the blood-borne to sexual transmission, suggesting that China s HIV/AIDS epidemic has moved from more confined high-risk groups to the general population. To address the challenge of this changing epidemic, a state-sanctioned research and development programme aimed at reducing HIV-related death and new infections, including sexually mediated transmission, was implemented in Although the coordinated efforts have mitigated the effects of the epidemics, the spread of HIV through sexual contact remains a huge challenge, as the new statistics in 2012 showed that sexual transmission now accounts for more than 80% of newly acquired HIV infection in China. 3 The advent of the HIV/AIDS epidemic in China was accompanied by a rapid increase in incidence and prevalence of other STIs. Syphilis, chlamydia and genital herpes, all highly contagious, which have steadily increased since the 1980s. 3,6,14,29,30 However, it is of interest that the epidemiological profiles of these STIs undergo dramatic changes from the early 1990s to the late 2000s, with syphilis and chlamydia becoming dominant in 2008 in contrast to the dominance of gonorrhoea in The dramatic increase in reported incidence of syphilis can be attributed to a widely performed blood test for syphilis diagnosis in usual medical practice and the routine blood test before surgical operations widely performed in recent years in China. National STI survey data from 2011 indicate that 72.7% of all reported syphilis cases are asymptomatic. This fact implies that the shifting of mostly prevalent STI from gonorrhoea to syphilis might be a result of the improved finding and reporting system. 30 Other STIs may be just as common but underdiagnosed or underreported, further indicating the severity of the STI problem. Traditional STIs (syphilis, gonorrhoea, genital herpes, genital chlamydia infection) have emerged as a major public health concern, both as diseases and as risk factors for HIV. Many of the STIs are known to have significant overlaps with HIV in the affected population because of the same route of transmission and because they potentiate risk of HIV. Epidemiological studies have demonstrated that STIs such as genital herpes and syphilis will facilitate HIV acquisition. Genital herpes infection not only increases the risk of HIV-1 acquisition 31 but may also facilitate HIV-1 transmission by HIV-positive individuals A person is more likely to become infected by HIV if exposed when syphilis sores are present. 25 China s huge migrant population may facilitate the spread of HIV and other STIs and a number of national policies make developing solutions to this especially 42 ª 2014 Royal College of Obstetricians and Gynaecologists

9 STI prevention and HIV epidemic in China challenging. The existing household registration system in China makes it difficult for people to move from rural to urban residence permanently, most of the ruralto-urban migrants work in the city for a period of time and return to their home village, or they travel back and forth seasonally. 8 Without a permanent urban household registration, the migrants become marginalised and cannot access the social welfare benefits available to urban residents, such as subsidised housing, education and long-term employment contracts. 8 This household registration system also hinders the effective management of public health challenges and disease prevention. The current public health infrastructure and medical services to identify, monitor and intervene are largely tailored to serve the registered households. For example, many of the migrant workers are not covered by health insurance provided by their employers and the household registration system often hinders medical re-imbursement when a migrant worker receives medical services in a different province from where his/her Hu Kou is registered. This insufficient healthcare coverage and social welfare further deters the migrants, who are mostly lower income, from seeking medical services. The scope of the STI increase and the concomitant development of economic migrants, urbanisation and social transformation require an integrated public health approach for controlling the spread of STIs. Strong evidence has supported biological mechanisms through which STIs, particularly ulcerative STIs, can facilitate HIV transmission by increasing both HIV infectiousness and HIV susceptibility. To more effectively tackle the changing face of the HIV/AIDS epidemic, the Chinese government implemented an integrated national policy in 2008 to reduce new HIV infections and AIDS deaths. 3 HIV prevention is an important component of the national public health strategy. However, prevention programmes against HIV alone may not be optimal and could be undermined by the surging rates of STIs, many of which cause inflammation and mucosal damage, hence facilitating HIV transmission. From both biological and epidemiological points of view, prevention may work more effectively and cost-efficiently when interventions are targeted simultaneously against the most prevalent and co-transmitted pathogens. To be effective, HIV/AIDS prevention intervention programmes need to address the specific needs, vulnerabilities and empowerment of the high-risk groups and adolescents. Much greater efforts are needed to promote safer sex, and programmes for the control of syphilis need to be tailored for migrant workers in China. 35 A user-friendly, easily accessible and effective MPT should play important roles in reducing STIs, including HIV, in the changing face of China s epidemics. We suggest that the priority of MPTs in China should be focused on HIV and STIs, as those are the major public health challenges that require immediate attention, and are the focus of key public health concerns. Conclusion The rapid increase of STIs, such as syphilis, chlamydia and genital herpes, may facilitate the transmission and acquisition of HIV through sexual contacts. The high prevalence of STIs elevates the risk of sexual transmission of HIV-1 and may mitigate the efforts and progress made by HIV-1 control in China, particularly in high-risk groups and adolescents. The country s huge migrant population may further exacerbate the spread of all STIs (syphilis, gonorrhoea, HIV, genital herpes) through complex social and economic factors within current Chinese society. Therefore, MPTs that are easily accessible, acceptable and effective could play an important role in simultaneously preventing the spread of HIV and other STIs. The simultaneous intervention of STIs and HIV may bring synergistic effects in disease control and public health benefits because some of the STIs exacerbate the infection and transmission of HIV. MPTs targeting multiple pathogens will provide a powerful tool for the control of STIs and HIV. The anti-sti feature of an MPT may even attract more users and wider acceptance. Since HIV/AIDS is a priority of China s national infectious disease control targets, an integrated approach to develop and make available MPTs targeting HIV and specific STIs will help to achieve China s goal of reducing new HIV infection. Disclosure of interests The authors declared no financial relationships or conflicts of interest regarding the content herein. Contribution to authorship ZWW planned and wrote the initial manuscript. NZ, YPG and BXW performed data collections, analysis and figure preparations. SP and ZWW provided critical comments and revised the manuscript. Details of ethics approval No human or animal experiments were involved in this research. Therefore, ethics approval was not required. Funding The work was supported by the Major Research and Development Project from the Ministry of Health (Grant No. 2012ZX and 2013ZX ). Acknowledgement The authors thank Xin Gong for her secretarial work. & ª 2014 Royal College of Obstetricians and Gynaecologists 43

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