Preplanned Studies: Niche Analysis of Spatial Distribution and Host Selection of Global Echinococcus Species — Worldwide, up to June 30, 2024

Objective: Echinococcosis is a fatal parasitic disease caused by infection with the larval stages of Echinococcus spp.. This study explored the spatial distribution characteristics and the host selection patterns of global Echinococcus species based on niche analysis, to provide scientific insights for the prevention and control of echinococcosis.

Methods: Relevant literature was retrieved from Web of Science, PubMed, ScienceDirect, and CNKI (China National Knowledge Infrastructure) databases. Data on the host information and geographic locations for all Echinococcus species worldwide were extracted. The spatial distribution characteristics of Echinococcus were summarized, and the host frequency heatmaps were generated using the SRplot platform. Niche indices were calculated and visualized using R language packages and the Hiplot Pro platform.

Results: The ten existing Echinococcus species were documented across 1,770 provincial-level administrative divisions in 113 countries, involving 188 species of host animals. Significant heterogeneity with varying degrees of overlap and differentiation was observed in spatial and host niches among Echinococcus species. The overall spatial distribution among Echinococcus species showed a significantly negative correlation (VR=0.85, W=1,502.79<χ² 0.951770), while host selection patterns revealed no significant correlation (VR=0.90, χ² 0.95187<W=167.70<χ² 0.05187). Echinococcus granulosus and Echinococcus multilocularis exhibited the broadest spatial niche (B_Eg=7.34) and host niche (B_Em=3.07), respectively.

Conclusion: The spatial distribution and host selection among Echinococcus species exhibit complex heterogeneity and correlations, requiring the development of targeted strategies for the prevention, control, and surveillance of echinococcosis.

Echinococcosis is a deadly infectious disease caused by Echinococcus larvae infection (1). Understanding the ecological niche of Echinococcus is crucial for exploring echinococcosis epidemiology. This study retrieved infection events and investigations of all 10 Echinococcus species from databases and found that Echinococcus spp. are currently distributed in at least 1,770 provincial regions across 113 countries, with 188 mammalian host species globally. Significant heterogeneity exists in the geographical distribution and host selection among different Echinococcus species. The niche overlap and separation of Echinococcus species contribute to the complexity, diversification, and endemicity of echinococcosis. These findings suggest that current surveillance approaches should be reconsidered and that differences among Echinococcus species must be fully accounted for in echinococcosis control. Specific host surveillance, targeted control strategies, and precise epidemiological investigations should be tailored to different types of endemic areas.

Echinococcosis causes approximately 19,300 deaths and 871,000 disability-adjusted life years, and costs more than 3 billion United States Dollars (USD) worldwide per year (2). Recent studies have recognized 10 valid natural species of Echinococcus worldwide: Echinococcus granulosus (Eg), E. equinus (Ee), E. ortleppi (Eor), E. intermedius (Ei), E. canadensis (Ec), E. felidis (Ef), E. multilocularis (Em), E. shiquicus (Es), E. vogeli (Ev), and E. oligarthra (Eol) (1). Host suitability and geographical distribution vary significantly among these Echinococcus species; however, detailed information remains limited due to a lack of systematic molecular data (3).

In this study, researchers conducted a comprehensive literature search from the Web of Science (https://webofscience.clarivate.cn), PubMed (https://pubmed.ncbi.nlm.nih.gov), ScienceDirect (https://www.sciencedirect.com/), and the China National Knowledge Infrastructure (https://www.cnki.net/) databases using the search terms “Echinococcus,” “echinococcosis,” “hydatid disease,” and “hydatidosis.” The final search was completed on June 30, 2024. This study’s authors performed full-text reviews and included articles with detailed investigation locations and clear identification of Echinococcus species/genotypes or echinococcosis types. Data on Echinococcus species, host species, and discovery locations (provincial-level administrative divisions, PLADs) were then extracted for subsequent analyses. The heat map of host occurrence frequencies was generated using the SRplot platform (https://www.bioinformatics.com.cn). Four ecological indices were calculated and visualized using the spaa package in R version 4.1.3 (R Core Team, Vienna, Austria) and Hiplot Pro platform (https://hiplot.com.cn): Shannon’s niche width (breadth) index (B_i), Levin’s niche overlap index (O_i-k), the overall interspecific association quantified by the variance ratio (VR) and tested for significance using the statistic W, and interspecific association coefficient (AC).

According to globally available data from 285 formal publications, 10 Echinococcus species have been reported in 1,770 provincial administrations across 113 countries (34 in Asia, 41 in Europe, 21 in Africa, 5 in North America, 11 in South America, and 1 in Oceania) (Supplementary Material). Echinococcus spp. have been observed or detected in 188 host species from 25 families, comprising 157 species (94 rodents, 34 ungulates, 18 marsupials, 7 primates, and 4 insectivores) serving as intermediate hosts (IHs) and 30 species (17 canids, 12 felids, and 1 quoll) acting as definitive hosts (DHs). Humans are considered accidental hosts and play a dead-end role in the life cycle of Echinococcus spp. (Figure 1).

Figure 1. 

The heatmap for host occurrence frequencies of 10 Echinococcus species.

Note: A separate information pool was created for each Echinococcus species, encompassing all reported host species within each provincial district (with each host species recorded only once per PLAD). The statistics for intermediate hosts, definitive hosts, and humans within each information pool were treated independently. Occurrence frequency = (the number of occurrences of the species/the total number of occurrences of all species recorded in the information pool) × 100%. RA3: L. europaeus, L. oiostolus, Sylvilagus floridanus; PI4: Ochotona dauurica, O. pallasii, O. rufescens, O. curzoniae; HA4: Cricetulus barabensis, C. kamensis, C. migratorius, C. longicaudatus; LE3: Lemmus lemmus, L. sibiricus, Dicrostonyx torquatus; MV2: Ellobius talpinus, E. tancrei; MV3: Alticola argentatus, A. olchonensis, A. strelzovi; RB4: Myodes rutilus, M. rex, M. rufocanus, Clethrionomys gapperi; SV2: Chionomys nivalis, C. roberti; VO21: Alexandromys limnophilus, A. middendorffii, A. oeconomus, Blanfordimys juldaschi, Lagurus lagurus, Lasiopodomys brandtii, L. gregalis, Microtus agrestis, M. arvalis, M. guentheri, M. ilaeus, M. irani, M. mystacinus, M. pennsylvanicus, M. socialis, M. subterraneus, M. transcaspicus, Myodes glareolus, Neodon irene, N. leucurus, N. fuscus; AG4: Dasyprocta leporina, D. azarae, D. punctata, D. fuliginosa; JE2: Pygeretmus pumilio, Scarturus elater; SR3: Proechimys guyannensis, P. trinitatus, P. semispinosus; DO2: Dryomys nitedula, Eliomys quercinus; FM5: Apodemus agrarius, A. argenteus, A. sylvaticus, A. uralensis, A. witherbyi; GE5: Meriones libycus, M. meridianus, M. persicus, M. unguiculatus, Rhombomys opimus; HM4: Mus macedonicus, M. musculus, Nesokia indica, Rattus norvegicus; GS6: Spermophilus alashanicus, S. erythrogenys, S. pygmaeus, S. relictus, Urocitellus undulates. MA4: Marmota baibacina, M. bobak, M. caudata, M. marmota; ZO2: Eospalax fontanierii, Myospalax myospalax. SH3: Sorex unguiculatus, S. jacksoni, Crocidura suaveolens; KA5: Macropus giganteus, M. rufogriseus, M. fuliginosus, M. dorsalis, Dendrolagus lumholtzi; WA11: Macropus parryi, Notamacropus dorsalis, N. parryi, N. rufogriseus, Onychogalea fraenata, Osphranter robustus, Petrogale godmani, P. mareeba, P. penicillata, P. persephone, Wallabia bicolor; AN3: Addax nasomaculatus, Gazella gazelle, Oryx gazelle; CA3: Bos taurus, B. indicus, B. frontalis; CA2: Camelus dromedaries, C. bactrianus; MO3: Cercopithecus ascanius, Pygathrix nemaeus, Macaca sylvanus; LE2: Lemur catta, Varecia rubra.

Among the 10 Echinococcus species, Eg was the most extensively documented across 93 countries (Asia, Europe, Africa, Oceania and the Americas), with dogs serving as the primary DHs (95.52% of all DH occurrences) and Bovidae animals as the predominant IHs (89.81% of all IH occurrences). Em was identified in 58 countries (Asia, Europe and North America), with foxes (47.26%) and dogs (35.98%) as the main DHs, and rodents as the principal IHs (93.83%). Ei was reported in 52 countries (Asia, Europe, Africa and South America), with dogs (61.29%) as the primary DHs, and camels (26.12%) and pigs (22.39%) as the main IHs. Eor was found in 35 countries (Asia, Europe, Africa and Latin America), with dogs (75.00%) as the predominant DHs, and cattle (57.89%) and pigs (11.58%) as the main IHs. Ec was identified in 10 countries in northern Asia, Europe and North America, with wolves (78.95%) and coyotes (21.05%) as DHs and Cervidae animals (96.43%) as IHs. Ee was recorded in 17 countries (western and southern Europe, western and central Asia, eastern and southern Africa), with dogs (60.00%) as the main DHs and Equidae animals (75.76%) as the principal IHs. Ev was documented in 10 countries in northern South America, with Speothos venaticus (85.71%) and Cuniculus paca (63.64%) being the main DH and IH, respectively. Eol was recorded in 8 countries in Latin America, with agouties (54.55%) as the main IHs and Puma concolor (33.33%) and other American Feline animals as the DHs. Ef was found in 5 countries (Kenya, Namibia, Uganda, Zambia and South Africa) in Sub-Saharan Africa, with lions (73.33%) being the preferred DHs, and warthogs and hippopotamuses as the few documented IHs. Es is currently considered endemic to the Tibetan Plateau in China, with Ochotona curzoniae (66.67%) and Vulpes ferrilata (42.86%) being the main IH and DH, respectively. Additionally, the most frequent cause of human echinococcosis was Eg (69.45%), followed by Em (10.24%), Ei (9.04%), Eor (4.78%), Ev (3.75%), Eol (1.19%), Ec (0.85%), and Ee (0.68%), whereas Es and Ef have not yet been recorded in humans (Figure 1 and Supplementary Material).

In terms of the spatial niche, Eg exhibited the largest niche width (B_Eg=7.34), with niche overlap with nearly all other species (mean O_Eg-others=0.12±0.28), particularly with Em (O_Eg-Em=0.86). Conversely, the niche overlaps between Ev and other species were the lowest (O_mean-Ev=0.02±0.06), and Es showed the smallest niche width (B_Es=1.39). For the host (excluding humans) niche, Em had the largest niche width (B_Em=3.07), whereas Ef had the smallest niche width (B_Ef=0.03). The group comprising Eg, Eor, and Ei (mean O_Eg-Eor-Ei=0.64±0.04) and that comprising Em and Es (O_Em-Es=0.56) exhibited higher niche overlaps. The overall interspecific association of spatial distribution among Echinococcus species (VR=0.85, W=1,502.79) showed significant negative associations, with 14 (AC>0) and 31 (AC<0) pairs of positive and negative correlations, respectively, in all interspecific correlations. The overall interspecific association of host selection (VR=0.90, W=167.70) showed no significant associations, with 16 positive and 29 negative pairs (Figure 2).

Figure 2. 

The spatial and host niche indexes of 10 Echinococcus species. (A) the spatial niche indexes; (B) the host niche indexes.

Note: Shannon’s niche width (breadth) index (B_i)=$ -\sum _{j=1}^{N}{(P}_{ij}\times \mathrm{L}\mathrm{n}{P}_{ij}) $; Levin’s niche overlap index (O_ik)=$ \dfrac{\sum _{j=1}^{N}\left({P}_{ij}\times {P}_{kj}\right)}{\sum _{j=1}^{N}{\left({P}_{ij}\right)}^{2}} $; variance ratio (VR)=$ \dfrac{1/N\sum _{j=1}^{N}{({T}_{j}-t)}^{2}}{\sum _{i=1}^{s}\left[{(n}_{i}/N\left)\times \right(1-{n}_{i}/N)\right]} $; Statistic W=VR*N; interspecific association coefficient (AC)=$ \dfrac{a\times d-b\times c}{\left(a+b\right)\times (b+d)} $ (if a*d ≥ b*c ) or $ \dfrac{a\times d-b\times c}{\left(a+b\right)\times (a+c)} $ (if a*d < b*c and a ≤ d) or $ \dfrac{a\times d-b\times c}{\left(b+d\right)\times (d+c)} $ (if a*d < b*c and a > d); i and k represents the Echinococcus species (i) and (k), respectively; j represents the space (PLAD) (j) or host species (j); N represents the number of spaces (PLADs) or host species; P_ij and P_kj represents abundance of species (i) and (k) for (j), respectively; S represents the number of Echinococcus species; n_i represents the number of spaces (PLADs) or host species that (i) appears; T_j represents the number of Echinococcus species for (j); t represents the mean number of Echinococcus species for all spaces (PLADs) or host species; a represents the number of spaces (PLADs) or host species occupied both by (i) and (k); b represents the number of spaces (PLADs) or host species occupied only by (i); c represents the number of spaces (PLADs) or host species only have (k); d represents the number of spaces (PLADs) or host species without (i) or (k); B_i represents the niche width of species (i), with a higher value indicating a wider niche; O_ik denotes the index of niche overlap between Echinococcus species of (i) and (k), with a higher value indicating more niche overlap; VR refers variance ratio of the number to the relative frequency of Echinococcus species, with a value >1 indicating a positive overall interspecific association and a value <1 indicating negative association; W is used in comparison with chi square (χ²) threshold with N, with a value >χ² (P=0.05) or χ² (P=0.95) indicating a significant overall interspecific association and a value <χ² (P=0.05) and >χ² (P=0.95) indicating an insignificant association; AC represents interspecific association between each pair of species, with a value >1 indicating a positive association and a value <1 indicating negative association.

Abbreviation: PLAD=provincial-level administrative division.

To date, human echinococcosis caused by Eg, Em, Ei, Ec, and Eor has been identified in China. These findings will facilitate the development of targeted, differentiated, and localized control and surveillance strategies to address the complex epidemiology of echinococcosis.