Meta-analysis of cyathostomin species-specific prevalence and relative abundance in domestic horses from 1975–2020: emphasis on geographical region and specimen collection method

(2020) 13:509 Bellaw and Nielsen Parasites Vectors https://doi.org/10.1186/s13071-020-04396-5 Parasites & Vectors Open Access RESEARCH Meta‑analysis of cyathostomin species‑specific prevalence and relative abundance in domestic horses from 1975–2020: emphasis on geographical region and specimen collection method Jennifer L. Bellaw and Martin K. Nielsen* Abstract Background: Cyathostomins infect virtually all horses, and concomitant infections with 10 or more species per horse is standard. Species-specific knowledge is limited, despite potential species bias in development of disease and anthelmintic resistance. This is the first meta-analysis to examine effects of geographical region and cyathostomin collection method on reported composition of cyathostomin communities. Methods: Thirty-seven articles published in English in 1975 or later, in which adults of individual species were systematically enumerated, were included. Seven regions; North America, South America, eastern Europe, western Europe, northern Europe, southern Africa, and Oceania, and three cyathostomin collection methods; (i) standard necropsy recovery from the large intestine, (ii) critical test collection from post-treatment feces and necropsy, and (iii) diagnostic deworming recovery solely from post-treatment feces, were considered. Generalized mixed linear models analyzed the effects of region and collection method on species-specific prevalence and relative abundance. Species richness was analyzed by mixed linear models. Results: Definitively, the most prevalent and relatively abundant species were Cylicocyclus nassatus (prevalence = 93%, relative abundance = 20%), Cylicostephanus (Cys.) longibursatus (93%, 20%), and Cyathostomum catinatum (90%, 16%). A bias toward horses with high infection intensities and cyathostomin collection from feces resulted in North American critical tests and eastern European diagnostic deworming overestimating the species-specific prevalence and underestimating the relative abundance of rare/uncommon species compared to respective intraregional standard necropsies. North American critical tests underestimated species richness due partially to identification key errors. Inter-regional standard necropsy comparisons yielded some species-specific regional differences, including a significantly higher Cys. longibursatus prevalence and relative abundance in North America (92%, 33%) than in eastern Europe (51%, 7%) (P > 0.0001). Localization of critical tests to North America and diagnostic deworming to Eastern Europe precluded expansive ‘region by collection method’ interaction analyses. Conclusion: We provide substantial data to inform study design, e.g. effect and study size, for cyathostomin research and highlight necessity for method standardization and raw data accessibility for optimal post-factum comparisons. *Correspondence: M. H. Gluck Equine Research Center, Department of Veterinary Science, University of Kentucky, Lexington, KY, USA © The Author(s) 2020. This article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons licence, and indicate if changes were made. The images or other third party material in this article are included in the article’s Creative Commons licence, unless indicated otherwise in a credit line to the material. If material is not included in the article’s Creative Commons licence and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this licence, visit http://creativecommons.org/licenses/by/4.0/. The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated in a credit line to the data. Bellaw and Nielsen Parasites Vectors (2020) 13:509 Page 2 of 15 Keywords: Cyathostomin, Prevalence, Relative abundance, Critical test, Diagnostic deworming, Necropsy Background Strongylid parasites of horses (Nematoda: Strongylidae) comprise a vast complex of 50 currently recognized species [1]. Cyathostomins, referring collectively to 40 Cyathostominae and seven non-migratory Strongylinae species, infect virtually all grazing horses with prevalence frequently approaching 100% [2–5]. Concomitant infection with 10 or more cyathostomin species per individual horse is the norm, rendering infections inherently complex [6–8]. Historically, the Strongylinae, most particularly Strongylus vulgaris, were regarded the most pathogenic gastrointestinal nematodes infecting equines, but species of this subfamily were observed to decline dramatically during the 1980s, and cyathostomins have since then been recognized as prominent parasitic pathogens of horses [9, 10]. Cyathostomins cause the rare but often fatal clinical syndrome, larval cyathostominosis [11, 12], and exhibit emerging or widespread resistance to all currently available anthelmintic drug classes [13]. Cyathostomins are thusly the most important gastrointestinal parasites of horses weaning age and older [14, 15]. Despite this, species-specific research on basic cyathostomin biology and ecology or on population and epidemiological dynamics involved in clinical disease and anthelmintic resistance is wanting. The major cause of this is limitations of available diagnostic tools [16, 17]. Only adult stage specimens can be morphologically identified to species, albeit with significant training and expertise [1]. In equine cyathostomin research, adult specimens are primarily collected via post-mortem methods. Standard necropsies are the most common and are often opportunistic, utilizing euthanized horses from veterinary hospital cases and abattoirs [2, 18, 19]. Therein, cyathostomin adults are recovered from digesta within the large intestine. Standard necropsies generally accommodate larger sample sizes than methods specific to anthelmintic efficacy trials and reduce ethical concerns of maintaining horses for this sole purpose. However, standard necropsies are not adequate for anthelmintic trials in which enumeration of specimens both expelled within feces and remaining in the horse are important [20]. In the critical test method, horses are first anthelmintically treated, and expelled adults are collected from feces during a post-treatment interval. After which, horses are necropsied and adults collected from digesta as above [21]. Critical tests are labor intensive and require maintenance of horses for this specific purpose, resulting in few and small-scale studies. A third post-mortem method, the controlled test, entails systematic necropsy and parasite collection from matched treatment and control groups after a post-treatmen (...truncated)