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. 2022 Sep 9;8(6):2785–2805. doi: 10.1002/vms3.932

The global prevalence of Spirometra parasites in snakes, frogs, dogs, and cats: A systematic review and meta‐analysis

Milad Badri 1,7, Meysam Olfatifar 2,✉, Amir KarimiPourSaryazdi 3, Leila Zaki 3, Luis Manuel Madeira de Carvalho 4, Majid Fasihi Harandi 5, Fatemeh Barikbin 6, Parisa Madani 7, Aida Vafae Eslahi 1,✉
PMCID: PMC9677416  PMID: 36084292

Abstract

Background

Spirometra infection is aneglected food‐ and waterborne disease with worldwide distribution.

Objectives

The present study aims to estimate the global prevalence of Spirometra species in snakes, frogs, dogs and cats.

Methods

Multiple databases (PubMed, Scopus, ProQuest, Web of Science and Google Scholar) were searched for relevant literatures published up to March 2022.

Results

Among 131 data sets (including 113 articles) that met the inclusion, 15 investigations reported Spirometra infection in snakes, 23 in frogs, 41 in dogs and 52 in cats. The pooled prevalence (95% confidence interval) in intermediate hosts and definitive hosts was found to be 0.313% and 0.089%, respectively. Based on continent, the infection was most prevalent in Asia for studies on snakes (0.696%) and frogs (0.181%), while Africa (0.224%) and Oceania (0.203%) were the regions with the highest pooled prevalence rates of the infection in dogs and cats, respectively. Among different diagnostic methods, the highest pooled prevalence was related to morphological method for studies on snakes, frog and cats with rate of 0.665%, 0.189% and 0.104%, respectively. Regarding studies on dogs, the highest pooled prevalence was observed for molecular technique (0.101%).

Conclusions

The results presented here revealed the importance of establishing a prevention and control measure focused on protection of aquaculture systems from being contaminated with faeces of dogs and cats, and raising awareness of parasitic zoonotic diseases to decrease the transmission risk.

Keywords: amphibians, canine, feline, reptiles, Spirometra, zoonosis

Spirometra species have been considered as neglected helminths in snakes, frogs, dogs and cats with a more recent growing interest in understanding its prevalence, means for prevention and better treatment, and the phylogenetic relationship of Spirometra in its various hosts. To build on our understanding of the epidemiology of Spirometra. The review and meta‐analysis in the submitted manuscript will contribute to filling this gap in knowledge.

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1. INTRODUCTION

The worldwide‐distributed pseudophyllidean tapeworms of the genus Spirometra inhabit the intestine of canids, felids and other mammals (Kavana et al., 2015, 2014; Le et al., 2017). The life‐cycle involves the crustaceans from Cyclops genus as the first intermediate host, amphibians and reptiles, birds and mammals as the second intermediate hosts, carnivores such as dogs and cats as the final hosts and humans as accidental hosts (Kavana et al., 2014). The procercoid larvae develop in Cyclops sp., and the plerocercoids develop in amphibians or reptiles (Wiwanitkit, 2005; Yudhana et al., 2019). These plerocercoid larvae (sparganum) are the causative agents of human larval migrans syndromes called sparganosis (spirometrosis), a food and waterborne zoonotic disease, which was firstly described by Manson in 1882 (Anantaphruti et al., 2011; Li et al., 2011; Wang et al., 2014). The disease is endemic in East Asian countries, and has also been reported in populations from Europe, America, Africa and Australia (Wang et al., 2014). So far, there are more than 2000 cases of sparganosis that have been reported in humans worldwide (Kuchta et al., 2015, 2021). However, the number of human cases reported from Eastern and Southeastern Asia is outstanding (Zhang et al., 2020). Humans acquire the infection through drinking water containing procercoid larvae in copepods, consuming raw or undercooked flesh of frogs, snakes, birds and mammals (e.g. pigs) as well as using flesh of frogs or snakes with plerocercoids as poultices on the eyes or open wounds (Li et al., 2011; Q. Liu et al., 2015). The research on sparganosis concentrated more in Asia, where the raw flesh of snake or frog is consumed as a remedy due to the traditional misbelieve and the infection is a serious hazard for humans (MARTA Kołodziej‐Sobocińska et al., 2018; Kuchta et al., 2015). Plerocercoid larvae mostly affect the subcutaneous connective tissues, causing nodules. However, occasionally they invade muscles, the abdominal cavity, eyes, central nervous system, liver, lungs, heart and urinary system (Cui et al., 2011; Kim et al., 2020; Kuchta et al., 2015; Nithiuthai et al., 2004). The migration and proliferation of larvae may result in paralysis, and even death following serious pathologic damages (Oda et al., 2016). There are more than 64 nominal species of Spirometra tapeworms (Kuchta et al., 2021). However, only four of them including S. erinaceieuropaei, S. mansonoides, S. pretoriensis and S. theileri are recognised as valid species (Kuchta et al., 2021; Yamasaki et al., 2021). Epidemiological data are critical for successful application of preventive and control programs against Spirometra infection in animals and raises the awareness of the public health hazard caused by these helminthic parasites. In this regard, the present review and meta‐analysis was designed to estimate the pooled prevalence of Spirometra tapeworms in snakes, frogs, dogs, and cats in different geographic locations of the world through evaluating available scientific reports.

2. MATERIALS AND METHODS

2.1. Search strategy

This systematic review and meta‐analysis followed the Preferred Reporting Items for Systematic reviews and Meta‐Analyses (PRISMA) guidelines (Page et al., 2021). Relevant published articles on the prevalence of Spirometra in snakes, frogs, dogs, and cats were searched in the following electronic bibliographic databases: PubMed, Scopus, ProQuest, Web of Science and Google Scholar. A systematic search was carried out using the keywords described as follows: Spirometra, Sparganosis, Foodborne parasites, Foodborne Diseases, Intestinal helminth, worm, snakes, frogs, dogs, cats, prevalence, frequency, global, worldwide using AND and/or OR Boolean operators. The searching process, evaluation of titles and abstracts and review of the full‐texts were conducted by two independent authors. After removing duplicates and irrelevant records, the reference lists of obtained articles were screened for further studies that were not found in the database search.

2.2. Inclusion and exclusion criteria

Full‐text literatures were evaluated for eligibility, if they met the inclusion criteria described below: (1) peer‐reviewed original papers, (2) cross‐sectional studies reporting the prevalence of Spirometra in snakes, frogs, dogs, and cats, (3) having accessible full‐text and abstract in English, (4) having total sample size and exact number of positive cases and (5) articles published in English language up to March 2022. Review articles, case reports, case series, publications with non‐original data, letters, editorials and papers with unclear/undetermined results, as well as papers written in other languages were excluded. Moreover, those articles that reported Spirometra infection in humans and in animals other than dogs, cats, snakes and frogs were excluded from the analyses of the current study. A Microsoft Excel® version 2016 was used to separately collect the following information that was retrieved from each of the included articles: first author's name, publication year, country where the study was conducted, continent, country‐level income, sample size, number of positive samples, climate, average temperature, annual rainfall, humidity, diagnostic methods including morphological detection and molecular techniques and species of Spirometra (Table 1, Table 2).

TABLE 1.

. Main characteristics of the included studies reporting the prevalence of Spirometra in cats, dogs, frog and snakes

No Reference Publication year Country Continent Total samples positive samples Detection method
Cats
1 Read 1948 United States North America 14 2 Morphological detection
2 Olsen et al. 1976 United States North America 82 8 Morphological detection
3 Ryan et al. 1976 Australia Oceania 146 89 Morphological detection
4 Gregory et al. 1976 Australia Oceania 107 61 Morphological detection
5 Coman et al. 1981 Australia Oceania 327 107 Morphological detection
6 Fujinami et al. 1983 Japan Asia 171 55 Morphological detection
7 Poglayen et al. 1985 Italy Europe 116 1 Morphological detection
8 Oikawa et al. 1991 Japan Asia 1064 166 Morphological detection
9 Meloni et al. 1993 Australia Oceania 33 5 Morphological detection
10 Huh et al. 1993 South Korea Asia 41 17 Morphological detection
11 Milstein et al. 1997 Australia Oceania 39 3 Morphological detection
12 Hata et al. 2000 Japan Asia 326 44 Morphological detection
13 Mcglade et al. 2003 Australia Oceania 418 2 Morphological detection
14 Scholz et al. 2003 Lao PDR Asia 55 7 Morphological detection
15 Sohn and Chai 2005 South Korea Asia 438 181 Morphological detection
16 Zibaei et al. 2007 Iran Asia 114 4 Morphological detection
17 Palmer et al. 2008 Australia Oceania 1063 29 Morphological detection
18 Yamamoto et al. 2009 Japan Asia 1079 90 Morphological detection
19 Castro et al. 2009 Uruguay South America 4 3 Morphological detection
20 Shin et al. 2009 South Korea Asia 4 4 Morphological detection
21 Lucio‐Forster and Bowman 2011 United States North America 1322 5 Morphological detection
22 Headley et al. 2012 British West Indies North America 55 10 Morphological detection
23 Spada et al. 2012 Italy Europe 139 2 Morphological detection
24 Al‐Obaidi 2012 Iraq Asia 55 13 Morphological detection
25 Sabshin et al. 2012 United States North America 100 1 Morphological detection
26 Borkataki et al. 2013 India Asia 100 8 Morphological detection
27 Ramos et al. 2013 Brazil South America 146 6 Morphological detection
28 Hoopes et al. 2013 Canada North America 635 1 Morphological detection
29 Ngui et al. 2014 Malaysia Asia 105 2 Morphological detection
30 Rojekittikhun et al. 2014 Thailand Asia 300 12 Morphological detection
31 Zanzani et al. 2014 Italy Europe 156 2 Morphological detection
32 Tun et al. 2015 Malaysia Asia 152 14 Morphological detection
33 Fang et al. 2015 China Asia 39 13 Morphological detection
34 Zanzani et al. 2015 Italy Europe 103 1 Morphological detection
35 Rojekittikhun et al. 2015 Thailand Asia 100 7 Morphological detection
36 Hong et al. 2016 China Asia 116 47 Morphological detection
37 Pumidonming et al. 2016 Thailand Asia 180 36 Morphological detection
38 Eslahi et al. 2017 Iran Asia 12 3 Morphological detection
39 Marques et al. 2017 Brazil South America 339 1 Morphological detection
40 Blasco et al. 2017 Spain Europe 423 1 Morphological detection
41 Wyrosdick et al. 2017 United States North America 76 6 Morphological detection
42 Sedionoto and Anamnart 2018 Thailand Asia 23 3 Morphological detection
43 Salman et al. 2018 Japan Asia 351 1 Morphological detection
44 Amoei et al. 2018 Iran Asia 42 1 Morphological detection
45 Andersen et al. 2018 United States North America 482 16 Morphological detection
46 Loftin et al. 2019 United States North America 56 5 Morphological detection
47 Hoggard et al. 2019 United States North America 103 3 Morphological detection
48 Traversa et al. 2019 Italy Europe 1000 3 Morphological detection
49 Nagamori et al. 2020 United States North America 2586 2 Morphological detection
50 Jitsamai et al. 2021 Thailand Asia 509 8 Morphological detection
51 Tong et al. 2021 China Asia 135 1 Morphological detection
52 Nath et al. 2022 Bangladesh Asia 50 19 Morphological detection
Dogs
1 Olsen et al. 1976 United States North America 2 2 Morphological detection
2 Cho et al. 1981 South Korea Asia 102 2 Morphological detection
3 Dalimi and Mobedi 1992 Iran Asia 35 2 Morphological detection
4 Meloni et al. 1993 Australia Oceania 182 4 Morphological detection
5 Saeki et al. 1997 Japan Asia 916 1 Morphological detection
6 Hee et al. 1998 South Korea Asia 304 1 Morphological detection
7 Traub et al. 2002 India Asia 101 28 Morphological detection
8 Asano et al. 2004 Japan Asia 772 8 Morphological detection
9 Inpankaew et al. 2007 Thailand Asia 229 7 Morphological detection
10 Palmer et al. 2008 Australia Oceania 1400 140 Morphological detection
11 Yamamoto et al. 2009 Japan Asia 906 9 Morphological detection
12 Lin et al. 2010 China Asia 31 6 Morphological detection
13 Itoh et al. 2011 Japan Asia 2365 1 Morphological detection
14 Cardoso et al. 2013 Portugal Europe 301 1 Morphological detection
15 Schar et al. 2014 Cambodia Asia 94 20 Morphological detection
16 Ngui et al. 2014 Malaysia Asia 105 8 Morphological detection
17 Rojekittikhun et al. 2014 Thailand Asia 500 3 Morphological detection
18 Tun et al. 2015 Malaysia Asia 227 8 Morphological detection
19 Itoh et al. 2015 Japan Asia 573 2 Morphological detection
20 Kavana et al. 2015 Tanzania Africa 59 17 Morphological detection
21 Fang et al. 2015 China Asia 40 4 Morphological detection
22 Bang et al. 2015 Vietnam Asia 414 28 Morphological detection
23 Inpankaew et al. 2015 Cambodia Asia 50 9 Morphological detection
24 Binod et al. 2015 India Asia 223 98 Morphological detection
25 Hong et al. 2016 China Asia 229 63 Morphological detection
26 Pumidonming et al. 2016 Thailand Asia 197 30 Morphological detection
27 Harriott 2016 Australia Oceania 201 72 Morphological detection
28 Eslahi et al. 2017 Iran Asia 27 2 Morphological detection
29 Sato et al. 2017 Lao PDR Asia 34 15 Molecular detection
30 Gillespie and Bradbury 2017 Australia Oceania 300 4 Morphological detection
31 Binod et al. 2018 India Asia 223 1 Morphological detection
32 Amouei et al. 2018 Iran Asia 42 1 Morphological detection
33 Beiromvand et al. 2018 Iran Asia 167 1 Molecular detection
34 Rusdi et al. 2018 Australia Oceania 141 5 Molecular detection
35 Little et al. 2019 United States North America 1202 1 Morphological detection
36 Nagamori et al. 2020 United States North America 7409 7 Morphological detection
37 Stafford et al. 2020 United States North America 3006 2 Morphological detection
38 Tong et al. 2021 China Asia 135 1 Morphological detection
39 Mulinge et al. 2021 Kenya Africa 65 11 Morphological detection
40 Sobotyk et al. 2021 United States North America 4692 2 Morphological detection
41 Nath et al. 2022 Bangladesh Asia 100 62 Morphological detection
Frogs
1 Ooi et al. 2000 Taiwan Asia 176 18 Morphological detection
2 Berger et al. 2009 Australia Oceania 243 12 Molecular detection
3 Mao et al. 2009 China Asia 818 131 Morphological detection
4 WeiMin et al. 2009 China Asia 671 209 Morphological detection
5 Liu et al. 2010 China Asia 292 59 Molecular detection
6 Lin et al. 2010 China Asia 446 75 Morphological detection
7 Young et al. 2012 China Asia 877 218 Morphological detection
8 Deng et al. 2012 China Asia 1149 306 Morphological detection
9 Zhang et al. 2014 China Asia 214 65 Molecular detection
10 Nelli et al. 2014 Armenia Europe 22 4 Morphological detection
11 Ruijia et al. 2015 China Asia 153 31 Morphological detection
12 Wei et al. 2015 China Asia 3482 565 Molecular detection
13 Borteiro et al. 2015 Uruguay South America 139 2 Morphological detection
14 Hong et al. 2016 China Asia 1949 229 Morphological detection
15 Zhang et al. 2016 China Asia 276 55 Molecular detection
16 Wang et al. 2018 China Asia 511 50 Molecular detection
17 Zhang et al. 2020 China Asia 386 19 Molecular detection
18 Yudhana et al. 2020 Indonesia Asia 185 17 Molecular detection
19 Chai et al. 2020 Myanmar Asia 20 15 Morphological detection
20 Fu et al. 2020 China Asia 1556 201 Morphological detection
21 Zhang et al. 2020 China Asia 4078 447 Molecular detection
22 Zhang et al. 2020 China Asia 386 19 Molecular detection
23 Fu et al. 2022 China Asia 1556 201 Morphological detection
Snakes
1 WeiMin et al. 2009 China Asia 3 3 Morphological detection
2 Wang et al. 2011 China Asia 1160 345 Morphological detection
3 Zhang et al. 2014 China Asia 6 3 Molecular detection
4 Wang et al. 2014 China Asia 456 251 Morphological detection
5 Sargsyan et al. 2014 Armenia Europe 22 2 Morphological detection
6 Pranashinta et al. 2017 Indonesia Asia 60 41 Morphological detection
7 Kondzior et al. 2018 Poland Europe 59 2 Molecular detection
8 Wang et al. 2018 China Asia 346 141 Molecular detection
9 Lu et al. 2018 China Asia 30 26 Molecular detection
10 Xiao et al. 2019 China Asia 149 55 Molecular detection
11 Yudhana et al. 2019 Indonesia Asia 378 192 Morphological detection
12 Liu et al. 2020 China Asia 375 344 Molecular detection
13 Yudhana et al. 2020 Indonesia Asia 43 43 Morphological detection
14 Yudhana et al. 2020 Indonesia Asia 37 21 Morphological detection
15 Yudhana et al. 2021 Indonesia Asia 55 51 Morphological detection
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TABLE 2.

Sub‐group analysis of the prevalence of Spirometra based on included studies diagnostic method, country‐level income level, genus and species, climate, average temperature, annual rainfall, humidity and continent

Heterogeneity**
Number of studies Sample size Number infected Pooled prevalence (%) (95% CI) I 2 τ 2 p Value*
Variable (cat)
Diagnostic method
Morphological detection 52 15,631 1131 0.104 (0.061 to 0.155) 98 0.074 <0.001
Income level
High income 36 13,349 987 0.115 (0.055 to 0.193) 98 0.099 <0.001
Upper‐middle income 9 1854 89 0.051 (0.017 to 0.104) 92 0.014 <0.001
Lower‐middle income 7 428 55 0.134 (0.039 to 0.273) 87 0.030 <0.001
Genus and species
Spirometra erinaceieuropaei 15 5295 866 0.268 (0.123 to 0.445) 98 0.110 <0.001
Spirometra mansoni 5 733 75 0.094 (0 to 0.314) 96 0.049 <0.001
Spirometra mansonoides 5 886 39 0.051 (0.001 to 0.164) 84 0.020 <0.001
Spirometra spp. 27 8717 151 0.049 (0.020 to 0.089) 93 0.039 <0.001
Climate
Humid continental climate 15 5594 311 0.142 (0.033 to 0.309) 98 0.131 <0.001
Tropical savanna climate 11 4153 441 0.113 (0.046 to 0.204) 96 0.032 <0.001
Semi‐desert climate 3 168 8 0.065 (0 to 0.433) 63 0.026 0.070
Tropical marine climate 1 55 10 0.181 (0.092 to 0.293) NA NA NA
Subarctic climate 1 635 1 0.001 (0 to 0.006) NA NA NA
Tropical monsoon climate 2 155 15 0.097(0 to 0.513) 0 0 0.350
Humid subtropical climate 9 2426 20 0.024 (0 to 0.114) 73 0.064 <0.001
Oceanic climate 8 2188 309 0.203 (0.026 to 0.487) 99 0.105 <0.001
Tropical rainforest climate 2 257 16 0.050 (0 to 0.930) 86 0.011 0.007
Average temperature
>20°C 14 2169 146 0.091 (0.043 to 0.154) 92 0.025 <0.001
10–20°C 37 12,827 984 0.115 (0.057 to 0.190) 98 0.096 <0.001
<10 1 635 1 0.001 (0 to 0.006) NA NA NA
Annual rainfall
>1500 mm 3 307 35 0.128 (0 to 0.733) 94 0.066 <0.001
1001–1500 mm 26 10,002 696 0.101 (0.045 to 0.174) 98 0.071 <0.001
401–1000 mm 19 5099 379 0.105 (0.030 to 0.217) 98 0.099 <0.001
<400 mm 4 223 21 0.103 (0 to 0.357) 85 0.031 <0.001
Humidity
>75 4 742 23 0.030 (0 to 0.115) 89 0.010 <0.001
40–75 44 14,666 1087 0.113 (0.063 to 0.175) 98 0.083 <0.001
<40 4 223 21 0.103 (0 to 0.357) 85 0.031 <0.001
Continent
Asia 25 5561 756 0.154 (0.081 to 0.244) 96 0.075 <0.001
Europe 6 1937 10 0.005 (0.001 to 0.011) 0 0 0.44
North America 11 5511 59 0.037 (0.009 to 0.081) 92 0.017 <0.001
Oceania 7 2133 296 0.203(0.026 to 0.487) 99 0.105 <0.001
South America 3 489 10 0.144 (0 to 1.000) 91 0.235 <0.001
Variable (dog)
Diagnostic method
Morphological detection 38 27,759 668 0.070 (0.032 to 0.120) 98 0.070 <0.001
Molecular detection 3 342 21 0.101 (0 to 0.854) 95 0.112 <0.001
Income level
High income 20 25,138 328 0.029 (0.002 to 0.087) 98 0.081 <0.001
Upper‐middle income 7 1329 60 0.065 (0.018 to 0.138) 92 0.015 <0.001
Lower‐middle income 13 1575 278 0.159 (0.061 to 0.291) 97 0.066 <0.001
Low income 1 59 17 0.288 (0.180 to 0.409) NA NA NA
Genus and species
Spirometra erinaceieuropaei 13 7997 266 0.045 (0.006 to 0.116) 98 0.048 <0.001
Spirometra mansoni 7 1413 105 0.141 (0 to 0.519) 96 0.201 <0.001
Spirometra spp. 21 18,691 318 0.080 (0.029 to 0.154) 98 0.062 <0.001
Climate
Humid continental climate 14 17,710 148 0.070 (0.006 to 0.195) 97 0.111 <0.001
Tropical savannah climate 10 6623 134 0.050(0 to 0.169) 97 0.075 <0.001
Semi‐desert climate 4 271 6 0.026 (0 to 0.092) 49 0.004 0.11
Tropical monsoon climate 5 640 159 0.250 (0.034 to 0.577) 98 0.070 <0.001
Humid subtropical climate 1 301 1 0.003 (0 to 0.013) NA NA NA
Oceanic climate 5 2224 225 0.078 (0 to 0.273) 97 0.044 <0.001
Tropical rainforest climate 2 332 16 0.050 (0 to 0.510) 57 0.002 0.12
Average temperature
>20°C 15 2621 345 0.162 (0.074 to 0.275) 97 0.059 <0.001
10–20°C 26 25,480 344 0.034 (0.008 to 0.077) 97 0.061 <0.001
Annual rainfall
>1500 mm 4 846 106 0.157 (0 to 0.650) 98 0.108 <0.001
1001–1500 mm 19 23,654 123 0.037 (0.002 to 0.109) 94 0.094 <0.001
401–1000 mm 14 3330 454 0.129 (0.055 to 0.227) 97 0.047 <0.001
<400 mm 4 271 6 0.026 (0 to 0.092) 49 0.004 0.11
Humidity
>75 3 746 44 0.057 (0.015 to 0.123) 48 0.001 0.14
40–75 33 27,019 628 0.078 (0.031 to 0.143) 98 0.088 <0.001
<40 5 336 17 0.051 (0.003 to 0.152) 83 0.013 <0.001
Continent
Asia 28 9141 421 0.076 (0.034 to 0.133) 97 0.055 <0.001
Europe 1 301 1 0.003 (0 to 0.013) NA NA NA
North America 5 16,311 14 0.071 (0 to 0.755) 80 0.377 <0.001
Oceania 5 2224 225 0.078 (0 to 0.273) 97 0.044 <0.001
Africa 2 124 28 0.224 (0 to 0.971) 60 0.005 0.11
Variable (frog)
Diagnostic method
Morphological detection 13 9532 1640 0.189 (0.105 to 0.290) 96 0.037 <0.001
Molecular detection 10 10,053 1308 0.121 (0.070 to 0.183) 95 0.014 <0.001
Income level
High income 20 19,358 2912 0.143 (0.104 to 0.187) 96 0.015 <0.001
Upper‐middle income 1 22 4 0.181 (0.052 to 0.365) NA NA NA
Lower‐middle income 2 205 32 0.385 (0 to 1.000) 97 0.260 <0.001
Genus and species
Spirometra erinaceieuropaei 14 13,077 1777 0.130 (0.089 to 0.177) 95 0.011 <0.001
Spirometra mansoni 6 4793 953 0.202 (0.135 to 0.280) 96 0.006 <0.001
Spirometra spp. 3 1715 218 0.232 (0 to 1.000) 97 0.218 <0.001
Climate
Humid continental climate 18 18,822 2884 0.163 (0.125 to 0.204) 96 0.010 <0.001
Tropical monsoon climate 1 20 15 0.750 (0.542 to 0.910) NA NA NA
Humid subtropical climate 2 315 20 0.049 (0 to 0.998) 92 0.018 <0.001
Oceanic climate 1 243 12 0.049 (0.025 to 0.080) NA NA NA
Tropical rainforest climate 1 185 17 0.091 (0.054 to 0.137) NA NA NA
Average temperature
>20°C 3 381 50 0.273 (0 to 1.000) 95 0.165 <0.001
10–20°C 20 19,204 2898 0.146 (0.107 to 0.190) 96 0.015 <0.001
Annual rainfall
>1500 mm 2 361 35 0.096 (0.041 to 0.172) 0 <0 0.74
401–1000 mm 20 19,202 2909 0.162 (0.105 to 0.229) 96 0.031 <0.001
<400 mm 1 22 4 0.181 (0.052 to 0.365) NA NA NA
Humidity
40–75 23 19,585 2948 0.156 (0.107 to 0.213) 96 0.027 <0.001
Continent
Asia 20 19,181 2930 0.181 (0.052 to 0.365) 96 0.025 <0.001
Europe 1 22 4 0.172 (0.119 to 0.232) NA NA NA
Oceania 1 243 12 0.049 (0.025 to 0.080) NA NA NA
South America 1 139 2 0.014 (0.001 to 0.040) NA NA NA
Variable (snake)
Diagnostic method
Morphological detection 9 2214 949 0.665 (0.349 to 0.915) 97 0.165 <0.001
Molecular detection 6 965 571 0.513 (0.132 to 0.884) 98 0.155 <0.001
Income level
High income 9 2584 1170 0.550 (0.252 to 0.830) 98 0.150 <0.001
Upper‐middle income 1 22 2 0.090 (0.009 to 0.242) NA NA NA
Lower‐middle income 5 573 348 0.790 (0.402 to 0.995) 96 0.102 <0.001
Genus and species
Spirometra erinaceieuropaei 8 2147 918 0.424 (0.142 to 0.736) 98 0.141 <0.001
Spirometra mansoni 1 3 3 1.000 (0.712 to 1.000) NA NA NA
Spirometra spp. 6 1029 599 0.752 (0.438 to 0.963) 96 0.092 <0.001
Climate
Humid continental climate 9 2547 1170 0.565 (0.284 to 0.824) 98 0.129 <0.001
Oceanic climate 1 59 2 0.033 (0.003 to 0.094) NA NA NA
Tropical rainforest climate 5 573 348 0.790(0.402 to 0.995) 96 0.102 <0.001
Average temperature
>20°C 5 573 348 0.790 (0.402 to 0.995) 96 0.102 <0.001
10–20°C 9 2547 1170 0.565 (0.284 to 0.824) 98 0.129 <0.001
<10°C 1 59 2 0.033 (0.003 to 0.094) NA NA NA
Annual rainfall
>1500 mm 5 573 348 0.790 (0.402 to 0.995) 96 0.102 <0.001
401–1000 mm 9 2584 1170 0.550 (0.252 to 0.830) 98 0.150 <0.001
<400 mm 1 22 2 0.090 (0.009 to 0.242) NA NA NA
Humidity
>75 1 59 2 0.033 (0.003 to 0.094) NA NA NA
40–75 14 3120 1518 0.653 (0.444 to 0.835) 98 0.125 <0.001
Continent
Asia 13 3098 1516 0.696 (0.502 to 0.859) 98 0.100 <0.001
Europe 2 81 4 0.049 (0 to 0.656) 0 0.002 0.33
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*

Data analysis was conducted using chi‐square tests.

**

Heterogeneity between studies was evaluated using Cochrane's Q test and the I2 statistic.

2.3. Quality assessment

A Newcastle–Ottawa Scale was implemented for quality assessment of the included studies (Supplementary Table S1) (Modesti et al., 2016). Scoring was based on three following items: selection (maximum of 5 stars), comparability (maximum of 2 stars) and outcome (maximum of 3 stars) (Badri et al., 2022; Eslahi et al., 2021; Eslahi et al., 2022; Mirzadeh et al., 2021)

2.4. Data synthesis and statistical analysis

The pooled prevalence of Spirometra in snakes, frogs, dogs and cats reported globally was calculated with 95% confidence interval. Meta‐regression analysis was conducted to evaluate the impact of average temperature, and year of publication on prevalence. Egger's test and Begg's test were applied to specify the possible publication bias. Moreover, publication bias was assessed by the Luis Furuya‐Kanamori (LFK) index and Doi plot (Barendregt & Doi, 2016). An LFK index within the range of ±1, ±2 and outside ±2 was inferred as symmetrical, slightly/minor asymmetrical and significantly/major asymmetrical, respectively, where symmetrical index indicates the absence of publication bias. Freeman‐Tukey double arcsine transformation for the random‐effects model (based on the inverse variance approach for measuring weight) was used to compute the pooled prevalence estimates. Cochrane's Q test and inconsistency index (I 2 statistics) was used to assess the magnitude of heterogeneity among included studies, with I 2 values of <25%, 25–75% and >75% were taken as low, moderate and high heterogeneity, respectively. A p‐value less than 0.05 was set as statistically significant. All statistical analyses were conducted using the meta‐package of R (version 3.6.1, R Foundation for Statistical Computing, Vienna, Austria) (Team, 2020).

3. RESULTS

3.1. Search results and study selection

The initial database search identified 1248 articles including 46 from PubMed, 87 from Scopus, 59 from ProQuest, 21 from Web of Science and 1035 from Google Scholar, of which 59 duplicates were removed. Of 976 records screened, 740 articles excluded, as they did not meet the inclusion criteria. Of 236 full‐text articles assessed for eligibility, 125 articles were excluded with the following reasons: papers without sufficient data (n = 11), multiple studies with overlapping data (n = 7), case report or case series (n = 66), studies with no original data including reviews, letters, theses or workshops (n = 39). Finally, 113 articles (including 131 data sets) were included in the current systematic review and meta‐analysis (Figure 1).

FIGURE 1.

FIGURE 1

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Flow diagram of the study design process

3.2. Prevalence in intermediate hosts (snakes and frogs)

For snake hosts, a total of 15 studies (3179 cases) were analysed, of which 1520 harboured Spirometra parasites spargana (Table 2). Global pooled prevalence rate for snakes was 0.6048% (95%CI: 0.3819–0.8068%) (Figure 2). According to the species of the parasite, the estimated pooled prevalence was as follows: 1.000% (95%CI: 0.712–1.000%) for S. mansoni, 0.752% (95%CI: 0.438–0.963%) for Spirometra spp. and 0.424% (95%CI: 0.142–0.736%) for S. erinaceieuropaei (Table 2). The highest prevalence was found in Asia (0.696, 95%CI: 0.502–0.859). The analyses based on different climates and climatic parameters revealed that the infection was most prevalent in regions with tropical rainforest climate (0.790, 95%CI: 0.402–0.995), average temperature of >20°C (0.790, 95%CI: 0.402–0.995), annual rainfall of >1500 mm (0.790, 95%CI: 0.402–0.995) and humidity of 40–75% (0.653, 95%CI: 0.444–0.835). The pooled prevalence rate with regard to the income level was the highest for lower‐middle income countries (0.790, 95%CI: 0.402–0.995) (Table 2).

FIGURE 2.

FIGURE 2

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Forest plots for random‐effects meta‐analysis of Spirometra in snakes

For frog hosts, a total of 23 studies (19,585 cases) were analysed, of which 2948 found to be infected with Spirometra parasites spargana, giving a global pooled prevalence of 0.1565% (95%CI: 0.1072–0.2131%) (Table 2 and Figure 3). Regarding the species of the parasite, the estimated pooled prevalence was as follows: 0.232% (95%CI: 0–1.000%) for Spirometra spp., 0.202% (95%CI: 0.135–0.280%) for S. mansoni and 0.130% (95%CI: 0.089–0.177) for S. erinaceieuropaei (Table 2). The highest prevalence rate was related to Asia (0.181, 95%CI: 0.052–0.365). The analyses based on different climates and climatic parameters revealed that the infection was most prevalent in regions with Tropical monsoon climate (0.750, 95%CI: 0.542–0.910), average temperature of >20°C (0.273, 95%CI: 0–1.000), annual rainfall of <400 mm (0.181, 95%CI: 0.052–0.365) and humidity of 40–75% (0.156, 95%CI: 0.107–0.213). The pooled prevalence rate with regard to the income level was highest for lower‐middle income countries (0.385, 95%CI: 0–1.000) (Table 2).

FIGURE 3.

FIGURE 3

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 Forest plots for random‐effects meta‐analysis of Spirometra in frogs

3.3. Prevalence in definitive hosts (dogs and cats)

For dog hosts, a total of 41 studies (28,101 cases) were analysed, of which 689 harboured Spirometra parasites, giving a pooled prevalence of 0.0723% (95%CI: 0.0351–0.1215%) (Table 2 and Figure 4). Regarding the species of the parasite, the estimated pooled prevalence was as follows: 0.141% (95%CI: 0–0.519%) for S. mansoni, 0.080% (95%CI: 0.029–0.154%) for Spirometra spp. and 0.045% (95%CI: 0.006–0.116%) for S. erinaceieuropaei (Table 2). The highest prevalence rate was related to Africa (0.224%, 95%CI: 0–0.971%). The analyses based on different climates and climatic parameters revealed that the infection was most prevalent in regions with Tropical monsoon climate (0.250%, 95%CI: 0.034–0.577%), average temperature of >20°C (0.162%, 95%CI: 0.074–0.275%), annual rainfall of >1500 mm (0.157%, 95%CI: 0–0.650%) and humidity of 40–75% (0.078%, 95%CI: 0.031–0.143%). The pooled prevalence rate with regard to the income level was highest for low‐income countries (0.288%, 95%CI: 0.180–0.409%) (Table 2).

FIGURE 4.

FIGURE 4

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 Forest plots for random‐effects meta‐analysis of Spirometra in dogs

For cat hosts, a total of 52 studies (15,631 cases) were analysed, of which 1131 were infected with Spirometra parasites, giving a pooled prevalence of 0.1040% (95%CI: 0.0619–0.1555%) (Table 2 and Figure 5). Based on the species of the parasite, the estimated pooled prevalence was as follows: 0.268% (95%CI: 0.123–0.445%) for S. erinaceieuropaei, 0.094% (95%CI: 0–0.314%) for S. mansoni, 0.051% (95%CI: 0.001–0.164%) for S. mansonoides, 0.049% (95%CI: 0.020–0.089%) for Spirometra spp. (Table 2). The highest prevalence rate was related to Oceania (0.203%, 95%CI: 0.026–0.487%). The analyses with regard to different climates and climatic parameters revealed that the infection was most prevalent in regions with Oceanic climate (0.203%, 95%CI: 0.026–0.487%), average temperature of 10–20°C (0.115%, 95%CI: 0.057–0.190%), annual rainfall of >1500 mm (0.128%, 95%CI: 0–0.733%) and humidity of 40–75% (0.113%, 95%CI: 0.063–0.175%). The pooled prevalence rate with regard to the income level was highest for lower‐middle income countries (0.134%, 95%CI: 0.039–0.273%) (Table 2).

FIGURE 5.

FIGURE 5

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 Forest plots for random‐effects meta‐analysis of Spirometra in cats

3.4. Prevalence based on diagnostic methods

There were two diagnostic procedures used for the detection of adult and spargana of Spirometra spp. in included studies (Table 2). All studies on intermediate hosts (snakes and frogs) were conducted on carcasses, while studies on definitive hosts (dogs and cats) were performed on stool specimens or carcasses. Totally 112 studies used morphological detection method and 19 studies used molecular detection method. According to the diagnostic method, the highest pooled prevalence was related to morphological method for studies on snakes, frog and cats with rate of 0.665% (95%CI: 0.349–0.915%), 0.189% (95%CI: 0.105–0.290%) and 0.104% (95%CI: 0.061–0.155%), respectively. However, all studies on cats were performed via morphological method (Table 2). Regarding studies on dogs, the highest pooled prevalence was observed for molecular technique (0.101%, 95%CI: 0–0.854%) (Table 2).

3.5. Meta regression analysis

Heterogeneity was noted for the year of publication and average temperature. Accordingly, the results of the test were significant for the year of publication for studies on cats (slop = 0.0069, p < 0.0062), and average temperature for studies on dogs (slop = 0.0149, p < 0.0172) (Supplementary Figure S1).

3.6. Publication bias

Asymmetry of the funnel plot indicates that publication bias was present in studies on cats (Egger's test: t = 3.31, p = 0.0017, and Begg's test: p = 0.0043) and dogs (Egger's test: t = 5.30, p = 0.0001, and Begg's test: p = 0.0003). There was no statistical publication bias for studies in snakes and frogs (Supplementary Figure S2A1–B4). Furthermore, asymmetrical Doi plots suggest presence of publication bias for prevalence in snakes, dogs and cats. Accordingly, there was major asymmetry for snakes (LFK index  = 2.93), dogs (LFK index  = 5.32) and cats (LFK index  =  3.57). In contrast, there was no asymmetry for prevalence in frogs (LFK index =  0.92) (Supplementary Figure S2C1–C4).

A QGIS3 software (version 3.1) was used to provide a map representing the global prevalence of Spirometra in snakes, frogs, dogs and cats in different geographical regions of the world based on included studies (Figure 6)

FIGURE 6.

FIGURE 6

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 Prevalence of Spirometra in (a) snakes, (b) frogs, (c) dogs and (d) cats in different geographical regions of the world based on the included studies

4. DISCUSSION

The current systematic review and meta‐analysis aims to estimate the global prevalence of Spirometra infection in snakes, frogs, dogs and cats. The overall prevalence of Spirometra in intermediate hosts and definitive hosts was found to be 0.313% and 0.089%, respectively. Among intermediate hosts analysed in this study, Spirometra infection was more prevalent in Asia with higher rate in snakes (0.6048%) than in frogs. Occurrence of infection with plerocercoid in snakes is more probably caused by ingestion of infected frogs than acquisition of the procercoid (Oda et al., 2016). In reptile hosts subcutaneous tissues and muscles are the frequent sites involved with infective larvae of the parasite (Mendoza‐Roldan et al., 2020). Snakes are the most common reptiles to be an intermediate host for Spirometra, a best‐known reptile‐borne zoonotic tapeworm. The raw or undercooked snakes meat for consumption or for purposes such as zootherapeutic remedies are regarded as a rout for transmission of sparganosis (Magnino et al., 2009; Mendoza‐Roldan et al., 2020).

One of the causes for the growth in reports of foodborne diseases in recent years has been the rising demand for animal protein, as well as, exotic and raw foods resulted in the expansion of some farming systems (wildlife farming) in emerging or underdeveloped nations where health monitoring may be inadequately managed (Broglia & Kapel, 2011; Xiao et al., 2021).

The complex life cycle of Spirometra parasites gives them the opportunity to be acquired not only via consumption of raw wild animal products (e.g. snakes and frogs infected with plerocercoids), but also by drinking contaminated water containing infected copepods (water‐borne route) (Yudhana et al., 2021).

It has been documented that the consumption of wild meat (bushmeat) has a direct relationship with poverty and low‐income communities, where is a lack of sanitary drinking water sources, sanitation and hygiene (Badri et al., 2022; Eslahi et al., 2021; Kouassi et al., 2019; Maleki et al., 2020; Prüss‐Ustün et al., 2014; Van Velden et al., 2020). Also, water hygienic interventions in low‐ and low‐middle‐income settings, which place less emphasis on limiting animal faeces exposure in water sources, help to maintain parasitic remains and provide the water‐borne cycle (Delahoy et al., 2018).

In Southeast Asian countries over the last decades, there has been a growing interest in snakes, and despite the negative impact on wildlife, snake farming and the international trade of snakes have emerged as significant phenomena. It is mostly visible in the Chinese population relative to the involvement of snakes in their dietary habits (Aust et al., 2017; Xiao et al., 2019).

Furthermore, sushi and sashimi as popular dishes prepared from the meat of frogs and snakes are the major sources of human sparganosis in Southeast Asia, where there is still a lack of awareness relating to the risk of this infection (Nawa et al., 2005).

Among the definitive hosts we analysed in the current study, cats have a higher infection rate (0.1040%) than dogs. This finding suggests that cats are the potential sources of maintenance for tapeworms of the genus Spirometra. They have a significant role in environmental contamination, transmission of many microbial pathogens and can serve as reservoirs for several parasites of both public and wildlife health importance (Hernandez et al., 2018; Jeon et al., 2018; Taghipour et al., 2021). Cats are predators of a broad variety of prey, including amphibians and reptiles. Thus, it is believed that the prevalence of Spirometra parasites is impacted by host diets and the access of definitive hosts to infected intermediate hosts (Hernandez et al., 2018).

The identification of both larval stage and adults of Spirometra species is through morphological and molecular approaches (Jeon et al., 2018). The morphological identification of Spirometra tapeworms to the species level is based on taxonomic differences (Badri et al., 2017). Recent advances of molecular techniques promote species identification for both adults and larvae. These techniques that rely on DNA sequencing of the whole mitochondrial COI (cytochrome c oxidase subunit I) gene are considered as the only approach to precisely specify the species (Kuchta et al., 2021). However, it is dependent on the availability of gene sequences and the accuracy of data, especially in the case that parasites are lacerated in the host's cadaver due to the road‐killing incidences (Eslahi et al., 2021; Tang et al., 2017).

Asia was the most prevalent region for Spirometra infection in snakes and frogs, whereas Africa and Oceania had been shown to have the highest pooled prevalence rates in dogs and cats, respectively. The geographical variation found for the prevalence emphasises that the infection risk is different in each region. Spirometra tapeworms have a broad host spectrum and they have been reported in domesticated and wild animals from different geographical regions all over the world (except Antarctica) (Bagrade et al., 2021). Although, this infection is mostly observed in tropical and sub‐tropical areas with the highest prevalence in South‐east Asia and East Africa (Farrar et al., 2013; L. N. Liu et al., 2015). This statement is in consistent with our analyses suggesting that oceanic and tropical climates present the highest prevalence for the infection.

The persistence of the heteroxenous life cycle and survival of Spirometra are affected by environmental factors including physiochemical conditions (pH, pCO2, O2, viscosity) and temperature (Muller & Wakelin, 2002). Moreover, humid areas with abundant river networks offer an optimal condition for development of Spirometra parasites (Marta Kołodziej‐Sobocińska et al., 2019). However, plerocercoids are able to tolerate stress conditions, such as diverse range of pH. As well, they have ability to survive in various vertebrate hosts even cold‐blooded ones, except fish (Kavana, 2015; Muller & Wakelin, 2002).

Given that the information on distinct morphological traits of both adults and plerocercoids are limited and there were lack of molecular diagnostics at the time of the study, most reports cannot identify Spirometra to the species level. Regardless of the fact that several species of the parasite have been identified, the taxonomy of Spirometra tapeworms is still unclear and needs to be more clarified (Bagrade et al., 2021).

The results of the present systematic review and meta‐analysis should be interpreted cautiously referring to some of the limitations. First, our analyses may have been affected by publication bias, as the result of absence or the low number of published studies from some geographic regions. Second, there were several single case reports of Spirometra species other than those included in the current study. Another point is the fact that this study was limited to publications in English. Finally, there were small‐study effects in some studies we included in our analyses attributable to (1) small sample size, (2) sampling bias relating to the nature of sample collection from wildlife over several years and (3) lack of a sensitive diagnostic technique. Despite these limitations, this study provides the most comprehensive estimates of the prevalence of Spirometra infection in snakes, frogs, dogs and cats from a global perspective.

5. CONCLUSION

The findings of the current systematic review and meta‐analysis indicate the relatively significant burden and current status of Spirometra infection in snakes, frogs, dogs and cats in different parts of the world and highlight the importance of conducting investigations in more geographical regions. Furthermore, our results showed that this infection may represent a significant risk for public health, especially in low‐ and lower‐middle‐income countries and in regions with oceanic and tropical climates. Paying attention to preventive strategies such as protection of aquaculture systems from being contaminated with faeces of dogs and cats, development of precise diagnostic approaches for foodborne parasitic infection during preparation, distribution, and selling stages, improving public education regarding the hazard of consuming reptile and amphibian products. Moreover, breaking the life cycle of the parasites and decreasing the burden of infective larvae in the aquatic environment play a key role in a large‐scale control measure in endemic regions.

AUTHOR CONTRIBUTIONS

MB, LMMDC, MFH, and AVE contributed to study design. AK, LZ, FB and PM searched for primary publications, screened and appraised primary studies. MB and AVE extracted the data and wrote the study manuscript. MO contributed to data analysis. All authors read the manuscript and participated in the preparation of the final version of the manuscript.

CONFLICT OF INTEREST

The authors declare that there are no conflicts of interests.

ETHICAL APPROVAL

None required.

PEER REVIEW

The peer review history for this article is available at https://publons.com/publon/10.1002/vms3.932.

Supporting information

Supporting Information

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Supporting Information

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Supporting Information

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ACKNOWLEDGEMENTS

We thank members of the Metabolic Diseases Research Center, Research Institute for Prevention of Non‐Communicable Diseases, Qazvin, Iran for their assistance with this project. This work was supported by Metabolic Diseases Research Center, Research Institute for Prevention of Non‐Communicable Diseases, Qazvin, Iran under the contract no. IR.QUMS.REC.1401.043.

Badri, M. , Olfatifar, M. , KarimiPourSaryazdi, A. , Zaki, L. , Madeira de Carvalho, L. M. , Fasihi Harandi, M. , Barikbin, F. , Madani, P. , & Vafae Eslahi, A. (2022). The global prevalence of Spirometra parasites in snakes, frogs, dogs, and cats: A systematic review and meta‐analysis. Veterinary Medicine and Science, 8, 2785–2805. 10.1002/vms3.932

Milad Badri and Leila Zaki contributed equally to this work.

Contributor Information

Meysam Olfatifar, Email: Ol.meysam92@gmail.com.

Aida Vafae Eslahi, Email: Vafaeeslahia@yahoo.com.

DATA AVAILABILITY STATEMENT

The authors confirm that the data supporting the findings of this study are available within the article and its supplementary material.

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