Population Biology of Schistosoma Mating, Aggregation, and Transmission Breakpoints: More Reliable Model Analysis for the End-Game in Communities at Risk

Mathematical modeling is widely used for predictive analysis of control options for infectious agents. Challenging problems arise for modeling host-parasite systems having complex life-cycles and transmission environments. Macroparasites, like Schistosoma, inhabit highly fragmented habitats that shape their reproductive success and distribution. Overdispersion and mating success are important factors to consider in modeling control options for such systems. Simpler models based on mean worm burden (MWB) formulations do not take these into account and overestimate transmission. Proposed MWB revisions have employed prescribed distributions and mating factor corrections to derive modified MWB models that have qualitatively different equilibria, including ‘breakpoints’ below which the parasite goes to extinction, suggesting the possibility of elimination via long-term mass-treatment control. Despite common use, no one has attempted to validate the scope and hypotheses underlying such MWB approaches. We conducted a systematic analysis of both the classical MWB and more recent “stratified worm burden” (SWB) modeling that accounts for mating and reproductive hurdles (Allee effect). Our analysis reveals some similarities, including breakpoints, between MWB and SWB, but also significant differences between the two types of model. We show the classic MWB has inherent inconsistencies, and propose SWB as a reliable alternative for projection of long-term control outcomes.

数学建模被广泛应用于病原体防控方案的预测分析。针对具有复杂生活史与传播环境的宿主-寄生虫系统开展建模，往往会面临诸多挑战性难题。诸如血吸虫（Schistosoma）这类大型寄生虫，栖息于高度破碎化的生境中，此类生境会决定其繁殖成功率与种群分布格局。在对此类系统的防控方案进行建模时，聚集分布（Overdispersion）与交配成功率是需要重点考量的关键因素。基于平均蠕虫负荷（mean worm burden, MWB）的简化模型并未纳入上述两类要素，因而会高估寄生虫的传播能力。此前提出的MWB修正模型通过预设分布形式与交配因子校正，推导得到了改进版MWB模型，该模型具备定性迥异的平衡点，其中包含“临界点”——当防控措施维持于该临界点以下时，寄生虫种群将走向灭绝，这提示可通过长期大规模治疗防控实现寄生虫的根除。尽管此类MWB方法已得到普遍应用，但目前尚无研究对其背后的适用范围与核心假设开展系统性验证。我们针对经典MWB模型以及近年提出的、可考量交配与繁殖障碍（阿利效应（Allee effect））的“分层蠕虫负荷（stratified worm burden, SWB）”模型展开了系统性分析。分析结果显示，两类模型既存在临界点这类相似特征，同时也存在显著差异。我们证实经典MWB模型存在内在不一致性，并提出SWB模型可作为预测长期防控效果的可靠替代方案。