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Meta-analyses of Schistosoma japonicum infections in wild rodents across China over time indicates a potential challenge to the 2030 elimination targets

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  • Hui-Ying Zou
  • Qiu-Fu Yu
  • Chen Qiu
  • Joanne P Webster
  • Da-Bing Lu

Abstract

China once suffered greatly from schistosomiasis japonica, a major zoonotic disease. Nearly 70 years of multidisciplinary efforts have achieved great progress in disease control, with infections in both humans and bovines significantly reduced to very low levels. However, reaching for the target of complete interruption of transmission at the country level by 2030 still faces great challenges, with areas of ongoing endemicity and/or re-emergence within previously ‘eliminated’ regions. The objectives of this study were, by using meta-analytical methods, to estimate the overall prevalence of Schistosoma japonicum infections in abundant commensal rodent species in mainland China after the introduction of praziquantel for schistosomiasis treatment in humans and bovines in 1980s. In doing so we thereby aimed to further assess the role of wild rodents as potential reservoirs in ongoing schistosome transmission. Published studies on infection prevalence of S. japonicum in wild rodents in mainland China since 1980 were searched across five electronic bibliographic databases and lists of article references. Eligible studies were selected based on inclusion and exclusion criteria. Risks of within and across study biases, and the variations in prevalence estimates attributable to heterogeneities were assessed. The pooled infection prevalence and its 95% confidence intervals (CIs) were calculated with the Freeman-Tukey double arcsine transformation. We identified a total of 37 relevant articles involving 61 field studies which contained eligible data on 8,795 wild rodents across mainland China. The overall pooled infection prevalence was 3.86% (95% CI: 2.16–5.93%). No significant change in the overall pooled prevalence was observed between 1980–2003 (n = 23 studies) and 2004-current (n = 38 studies). However, whilst the estimated prevalence decreased over time in the marshland and lake regions, there was an apparent increase in prevalence within hilly and mountainous regions. Among seven provinces, a significant prevalence reduction was only seen in Jiangsu where most endemic settings are classified as the marshland and lakes. These estimates changed over season, ranging from 0.58% in spring to 22.39% in winter, in association with increases in rodent density. This study systematically analyzed S. japonicum infections in wild rodents from the published literature over the last forty years after the introduction of praziquantel for schistosomiasis treatment in humans and bovines in 1980s. Although numbers of schistosomiasis cases in humans and bovines have been greatly reduced, no such comparable overall change of infection prevalence in rodents was detected. Furthermore, there appeared to be an increase in S. japonicum prevalence in rodents over time within hilly and mountainous regions. Rodents have been projected to become the dominant wildlife in human-driven environments and the main reservoir of zoonotic diseases in general within tropical zones. Our findings thus suggest that it is now necessary to include monitoring and evaluation of potential schistosome infection within rodents, particularly in hilly and mountainous regions, if we are ever to reach the new 2030 elimination goals and to maximize the impact of future public, and indeed One Health, interventions across, regional, national and international scales.Author summary: Consistent with the revised WHO Global Goals, China has set the target of complete interruption of transmission (elimination) of zoonotic Schistosoma japonicum by 2030 at the entire country level. Much remains to be known, however, regarding the complex multi-host disease dynamics of schistosomiasis. Multi-disciplinary disease control programs within China, including mass treatment with praziquantel for over 40 years, have successfully targeted human and bovine definitive hosts, significantly reducing infection prevalence to extremely low levels. However, S. japonicum has at least 40 species of potential definitive host reservoirs. Most notably, and perhaps most challenging in terms of targeted control, high prevalence of S. japonicum has been detected in rodent wildlife within recent years, particularly in hilly and mountainous regions of China. Molecular/phylogenetic studies have revealed matched S. japonicum genotypes indicative of shared transmission between rodents and humans. Similarly, mathematical models, incorporating parasitological and molecular data, have indicated that rodents may be sufficient to maintain ongoing transmission of schistosomiasis within some Chinese regions, most notably that of hilly and mountainous habitats. In order to help elucidate further the potential association between prevalence of S. japonicum in humans with rodent wildlife across China, and to assess whether this balance may be changing following the introduction of mass drug administration with praziquantel to humans (and bovines) in the 1980s, we performed a meta-analyses aimed to estimate the overall prevalence of S. japonicum infections in commensal species rodents in China over this period. Published studies on S. japonicum infections in wild rodents in China since 1980 were searched for across five electronic bibliographic databases, together with lists of cited articles. We identified a total of 37 relevant articles involving 61 studies with eligible data on 8795 rodents. The pooled prevalence level was 3.86% (95% CI: 2.16–5.93%). No significant change in overall pooled prevalence levels within rodents was observed between 1980–2003 and 2004-current, despite the integrated control strategies performed across China within the latter period. However, whilst the prevalence estimates did decrease within marshland and lake regions since 2004, in the hilly and mountainous regions, in contrast, there was a significant increase in the rodent infection prevalence. The estimate increased from the smallest 0.58% in spring to the highest 22.39% in winter. It also increased with the density of rodents. Therefore, we suggest that future systematic monitoring of schistosome infection levels within potential wildlife reservoirs, particularly within hilly and mountainous regions within China and/or areas aiming for verification of interruption of transmission, should be incorporated in order to reliably evaluate impact, risk and ultimately help ensure the sustainability of elimination interventions across, regional, national and international scales.

Suggested Citation

  • Hui-Ying Zou & Qiu-Fu Yu & Chen Qiu & Joanne P Webster & Da-Bing Lu, 2020. "Meta-analyses of Schistosoma japonicum infections in wild rodents across China over time indicates a potential challenge to the 2030 elimination targets," PLOS Neglected Tropical Diseases, Public Library of Science, vol. 14(9), pages 1-21, September.
  • Handle: RePEc:plo:pntd00:0008652
    DOI: 10.1371/journal.pntd.0008652
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    References listed on IDEAS

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    1. Darren J Gray & Gail M Williams & Yuesheng Li & Honggen Chen & Simon J Forsyth & Robert S Li & Adrian G Barnett & Jiagang Guo & Allen G Ross & Zheng Feng & Donald P McManus, 2009. "A Cluster-Randomised Intervention Trial against Schistosoma japonicum in the Peoples' Republic of China: Bovine and Human Transmission," PLOS ONE, Public Library of Science, vol. 4(6), pages 1-7, June.
    2. David Moher & Alessandro Liberati & Jennifer Tetzlaff & Douglas G Altman & The PRISMA Group, 2009. "Preferred Reporting Items for Systematic Reviews and Meta-Analyses: The PRISMA Statement," PLOS Medicine, Public Library of Science, vol. 6(7), pages 1-6, July.
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