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Parasitology Research

, Volume 113, Issue 2, pp 619–640 | Cite as

An overview of the host spectrum and distribution of Calodium hepaticum (syn. Capillaria hepatica): part 1—Muroidea

  • Hans-Peter FuehrerEmail author
Open Access
Original Paper

Abstract

Calodium hepaticum (syn. Capillaria hepatica) is a worldwide-distributed species of zoonotic nematodes with a high affinity to the liver. Several rodent species of the superfamily Muroidea serve as main hosts for this pathogen. C. hepaticum has been found in Muroidean hosts in more than 60 countries in Europe; North, Central, and South America; Asia; Africa; and Oceania. C. hepaticum was documented in more than 90 Muroidean rodent species (Murinae, Deomyinae, Arvicolinae, Neotominae, Cricetinae, Sigmodontinae, Gerbillinae, and Cricetomyinae). Globally, the Norway rat (Rattus norvegicus) seems to be the main host species for this nematode. However, locally high prevalences (above 50 %) have also been observed in several other synanthropic (commensal and non-commensal) Muroidea species (e.g., Rattus tanezumi, Ondatra zibethicus, Apodemus sylvaticus). This review gives an overview of the distribution and host spectrum of C. hepaticum in Muroidea host species.

Keywords

Bank Vole Rodent Species Main Host Apodemus Sylvaticus Host Spectrum 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.

Introduction

Calodium hepaticum (syn. Capillaria hepatica) is a zoonotic nematode parasite distributed worldwide. Adults of this nematode parasitize the liver of mammals and lay their eggs into the liver parenchyma causing hepatic capillariasis. The eggs are only released into the environment with the death of the host. The main hosts of this parasite are rodents of the superfamily Muroidea (Schmidt 2001). Furthermore, this parasite has been documented in numerous other mammalian species including more than 70 human cases (reviewed in Fuehrer et al. 2011; Fuehrer 2013). Hepatic capillariasis is diagnosed through necroscopy or biopsy only, because with hepatic infections eggs are not shed into the environment with the feces.

This review focuses on the Muroidea host spectrum and its geographic distribution in those hosts only. Information about the pathogenesis, ecology, and host spectrum in humans and other mammalians is given elsewhere (e.g., Fuehrer et al. 2011; Fuehrer 2013; Schmidt 2001).

For data evaluation, the systematic search was based on electronic databases (Scopus, PubMed, Google Scholar) and previous summaries (e.g., Schmidt 2001). The search terms Capillaria hepatica, Calodium hepaticum, Hepaticola hepatica, Trichocephalus hepaticus, and hepatic capillariasis were used. An attempt was made to include only those studies where the scientific names of the host and parasite were given clearly. Furthermore, spurious infections (= pseudoparasitism) were differentiated as far as possible from hepatic capillariasis. A short overview of spurious C. hepaticum infections in animals is given in Fuehrer (2013).

Taxonomy

C. hepaticum is a nematode out of the family Capillaridae (order Trichocephalida). Moravec (1982) categorized C. hepaticum in the genus Calodium. However, the name C. hepaticum is rarely used, and most researchers use the term Capillaria hepatica. Further synonyms are Trichocephalus hepaticus (Bancroft, 1893) and Hepaticola hepatica (Hall 1916) (Fuehrer et al. 2011).

The taxonomy of the family Capillaridae is disputed and pending. In the past, most species were included in the genus Capillaria. Recently, a molecular phylogenetic study revealed that Capillaridae can be clearly separated from Trichuridae (Guardone et al. 2013). However, the former genus Capillaria consists of a complex group of parasites including several parasites of carnivores and rodents of the genera Calodium, Eucoleus, Capillaria, Paracapillaria, Pearsonema, and Aonchotheca (Guardone et al. 2013). Three species are of zoonotic importance, namely Paracapillaria philippinensis (syn. Capillaria philippinensis), Eucoleus aerophila (syn. Capillaria aerophila), and C. hepaticum (syn. C. hepatica).

Life cycle

The life cycle of C. hepaticum is a direct one with a high affinity to the liver. After the ingestion of embryonated eggs, larvae hatch in the area of the caecum and invade the liver via the portal vein system. Adult worms parasitize in the liver of its mammalian hosts where the females lay eggs into the liver parenchyma after mating. The life span of adult worms is short (18–60 days post infection in mice) (Juncker-Voss et al. 2000; Schmidt 2001). The eggs develop in the host's liver to the eight-cell stage only. Unembryonated eggs are only released into the environment with the death of the host only (decay of host; excretion in feces of carnivores and omnivores or after cannibalism). Depending on the environmental conditions (e.g., humidity, temperature), eggs embryonate within 5–8 weeks. Laboratory studies revealed that embryonated eggs are viable for 25 months (reviewed in Juncker-Voss et al. 2000). The life cycle is closed when embryonated eggs are ingested from a mammalian host. The ingestion of non-embryonated eggs leads to pseudoparasitosis (= spurious infections) where the non-embryonated eggs are re-released with the feces and lead to mild symptoms only (reviewed in Fuehrer et al. 2011).

Muroidea host spectrum

The mammalian superfamily Muroidea consists of rodents with a worldwide distribution (with the exception of Antarctica) including animals like rats, true mice, gerbils, and hamsters. Recent molecular phylogenetic studies classified the superfamily into 6 families, 19 subfamilies, around 280 genera, and over 1,300 species (e.g., Steppan et al. 2004).

The host spectrum of C. hepaticum in Muroidea hosts (and in other mammals) indicates very low host specificity. More than 90 species of at least 44 genera of the superfamily Muroidea (Murinae, Arvicolinae, Neotominae, Cricetinae, Sigmodontinae, Gerbilinae, and Cricetomyinae) are known as hosts of this parasite (Table 1). Of these, more than 55 species are rodents of the subfamily Murinae including the Norway rat (Rattus norvegicus), Black rat (Rattus rattus), and house mouse (Mus musculus). Prevalences above 50 % are regularly documented in Norway rats (R. norvegicus) and Tanezumi rats (R. tanezumi), and rarely in house mice (M. musculus), long-tailed field mice (Apodemus sylvaticus), muskrats (Ondatra zibethicus), and bank voles (Myodes glareolus). All of these species are known as (commensal or non-commensal) synanthropic species. Human hepatic capillariosis cases are associated with poor hygienic conditions and the presence of rodents (e.g., rats) (Fuehrer et al. 2011). Davis (1951) reported that C. hepaticum is significantly less prevalent in decreasing rat populations than in stationary or increasing populations. A study conducted in Michigan (USA) with deer mice revealed that parasite prevalences are correlated negatively with heterozygosity when the effects of population density were held constant (Meagher 1998). Meagher further hypothesizes that inbred populations are more susceptible to parasite infestations. Differences in the prevalences of C. hepaticum in different rodent host species are thought to be associated with different living and nutritional habits (Schmidt et al. 1998). Several authors report that C. hepaticum occurs in localized foci of the examined study areas (e.g., Reperant and Deplazes 2005; Stojčević et al. 2002). Furthermore, cannibalism may be an important egg-releasing mechanism and is an important source of infection in burrows. On the other hand, predation seems to be responsible for scattered foci of infection (Farhang-Azad 1977a, b; Stojčević et al. 2002). Decomposition is thought to be a less important egg-releasing mechanism. Environmental conditions (humidity and temperature) are also associated with the distribution of these pathogens (e.g., Resendes et al. 2009). The pathogenicity of C. hepaticum in Muroidea hosts is considered low, although experimental infections of rats and mice have been demonstrated to lead to hepatic failure and the death of the host (the host survival rate is reduced by 5–10 %) (Singleton and Chambers 1996). However, individual variations of the host's inflammatory reaction to the parasite have been reported. Furthermore, hypersensitivity is associated with repeated infections (Borucinska and Nielsen 1993).
Table 1

Calodium hepaticum in Muroidea

Classification

Species

Prevalence (%)

Country/region

References

Muridae

Murinae

Norway rat (Rattus norvegicus)

 

USA

Childs et al. (1988); Shorb (1931); Wantland et al. (1956)

  

82 % (of 86)

USA (Connecticut)

Conlogue et al. (1979)

  

75 % (of 845)

USA (Maryland—Baltimore area and zoo)

Farhang-Azad (1977a)

  

75 % (of 845)

USA (Maryland—Baltimore Zoo)

Farhang-Azad (1977b)

  

87.9 % (176/201)

USA (Maryland, Baltimore)

Easterbrook et al. (2007)

   

USA (New York)

Herman (1939)

  

85.6 %

USA (Maryland)

Luttermoser (1936)

  

94.1 % (of 1,460)

USA (Maryland)

Davis (1951)

   

USA (North Carolina)

Harkema (1936)

   

USA (District of Columbia)

Price and Chitwood (1931); Cram (1928)

   

USA (Pennsylvania and Rhode Island)

Winfield (1933)

   

USA (California)

Hall (1916)

  

Spurious infection 6 % (of 150)

Canada (Quebec)

Firlotte (1948)

   

Puerto Rico

Leon de (1964)

   

Venezuela

Vogelsang and Espin (1949)

  

20.1 % (51/254)

Colombia

Duque et al. (2012)

   

Brazil

Araújo (1967); Galvão (1981); Chieffi et al. (1981); Ferreira and Andrade (1993)

   

Brazil (Bahia)

Ferreira and Andrade (1993)

  

54.1 % (13/24)

Brazil (Belém)

Moreira et al. (2013)

  

30 %

Argentina (Buenos Aires)

Hancke (2011)

  

33.3 % (5/15)

Chile

Torres and Gonzáles (1972); Rojas et al. (1971)

  

1 case

England

Simmons and Walkey (1971)

  

1 case

England (zoo)

Redrobe and Patterson-Kane (2005)

  

A: 90.4 % (38/42)

B + C: none of 38

England

Owen (1976)

  

23 % (n = 44)

England

Webster and MacDonald (1995)

  

60 % (of 29)

Portugal (Azores)

Roque (1989)

  

20 % (of 20)

Portugal (Azores)

Cruz (2006)

  

62.5 % (of 73)

Portugal

Roque et al. (1984)

  

42 % (21/50)

Portugal Lisbon Zoo

Crespo (2012)

  

20 %

Spain

Mascato et al. (1993); Feliu et al. (1985); Castro (1944); Gallego Berenguer (1959)

   

France

Davoust et al. (1997)

   

Italy

Perugia (1893)

  

80 % (of 28)

Italy

Vanni (1938); Vanni (1947)

  

30 % (of 100)

Italy (Pisa)

Ghelardoni (1966)

  

30 % (of 50)

Italy

Casarosa and Ghelardoni (1965)

  

36 % (17/49)

Italy (Milano)

Ceruti et al. (2001)

  

54.55 % (of 143)

Italy (Sicily)

Milazzo et al. (2010b)

  

74.6 %

Austria

Rydlo (1966)

  

1 case

Austria

Frank (1977)

   

Switzerland

Hörning (1966)

  

16.4 % (of 864)

Belgium

Cotteleer et al. (1982)

   

Former CSSR

Mituch (1960)

  

100 % (26/26)

Hungary (zoo)

Mészáros and Kemenes (1973)

  

1.95 % (6/307)

Croatia

Stojčević et al. (2002)

  

10.9 % (of 147)

Serbia (Belgrad)

Kataranovski et al. (2010)

   

Turkey

Merdivenci (1970)

   

Kazakhstan

Pleščëv and Kozlov (1978)

   

Japan

Shimatani (1961); Sato and Shimatani (1960); Iwaki et al. (1993); Ito et al. (1996); Yagisawa (1978)

  

52.7 % (1,272/2,222)

Japan (Osaka)

Momma (1930)

  

90 %

Philippines

Tubangui (1931)

  

60/138 (42 %)

Thailand

Chaiyabutr (1979)

  

12.5 % (of 16)

Thailand

Namue and Wongsawad (1997)

   

Malaysia

Liat et al. (1977); Sinniah et al. (1979)

   

China

Lagrange (1924)

  

30.4 %

China (Soochow)

Wu (1930)

  

7.1 %

China (Canton)

Chen (1933)

  

61.9 %

China (Hubei Province)

Zhou et al. (1991)

  

66.7 %

China (Yunnan Province)

Zhou et al. (1998)

  

1 case

China (Yunnan Province)

Xiong et al. (1999)

  

77 %

China (Yunnan Province)

Shen et al. (2003)

  

66.7 %

China (Fujian Province)

Yuan et al. (2000)

  

12.3 %

China (Fujian Province)

Xue et al. (1998)

  

46.2 %

China (Fujian Province)

Zhang et al. (2003)

  

25.8 %

China (Henan Province)

Lin et al. (2007)

  

25.83 % (109/422)

China (Henan)

Wang et al. (2013)

  

36.7 %

Taiwan

Yang and Lu (2000)

  

54.9 %

Taiwan

Tung et al. (2009)

  

62.5 % (20/32)

Taiwan

Tung et al. (2013)

  

36 %

South Korea (Seoul)

Nakamura and Kobashi (1935)

  

88 % (286/235)

South Korea (Seoul)

Seo et al. (1964)

  

38.1 % (of 1,000)

South Korea (Seoul)

Min (1979)

  

12.1 % (of 33)

South Korea (Pochun and Chungpyong)

Seo et al. (1968)

  

23.6 % (21/89)

South Korea (Gangwon Province)

Yi et al. (2010)

  

25.9 % (11/43)

South Korea (Chunchon)

Seong et al. (1995)

  

13.04 % (of 23)

Iran

Pakdel et al. (2013)

  

28 %

Australia (Queensland)

Singleton et al. (1991)

   

Egypt

El-Nassery et al. (1991)

   

Tunisia

Mishra and Gonzalez (1975)

 

Black rat (Rattus rattus)

 

New Zealand

Roberts (1990)

  

5 %

Australia (Queensland)

Singleton et al. (1991)

  

25–30 %

Federated States of Micronesia (Pohnpei)

Storer (1962)

   

Bangladesh

Bhuiyan et al. (1995)

   

India

Chahota et al. (1997); Kumar et al. (1985); Somvanshi et al. (1995); Chahota et al. (1997); Bhattacharya et al. (1998)

  

29.54 % (of 88)

India

Malsawmtluangi and Tandon (2009)

  

2.32 % (1/43)

Spurious infection

India

Sharma et al. (2012)

  

88.3 %

India

Patel et al. (2004)

  

7.3 % (of 3,190)

Pakistan

Ahmad et al. (2011)

  

20 % (1/5)

Iran

Pakdel et al. (2013)

  

7.4 % (2/27)

Thailand

Chaiyabutr (1979)

  

4.54 % (of 22)

Thailand

Namue and Wongsawad (1997)

  

28.6 %

Taiwan

Tung et al. (2009)

  

18.2 % (2/11)

Taiwan

Tung et al. (2013)

   

Japan

Sato and Shimatani (1960); Shimatani (1961)

   

Turkey

Merdivenci (1970)

  

3.1 % (2/65)

Israel

Wilamowski et al. (2002)

   

Spain

Feliu et al. (1985); Castro (1944); Gallego Berenguer (1959)

   

Portugal (Azores)

Casanova et al. (1996); Roque (1989)

   

France

Davoust et al. (1997)

  

34.2 % (of 37)

Italy (Sicily)

Milazzo et al. (2010a)

   

Switzerland

Hörning (1966)

   

USA

Layne (1970)

   

Brazil

Chieffi et al. 1981

   

Brazil (Bahia)

Ferreira and Andrade (1993)

  

69.8 % (30/43)

Brazil (São Paulo)

Almeida-Silva et al. (2011)

  

38.4 % (10/26)

Brazil (Belém)

Moreira et al. (2013)

   

Egypt

El-Nassery et al. (1991)

  

6.2 % (19/308)

Ethiopia

Farhang-Azad and Schlitter (1978)

   

Democratic Republic of the Congo

Dubois (1933)

  

5.8 % (6/103)

Nigeria

Onyenwe et al. (2009)

 

Rattus spp. (R. norvegicus and/or R. rattus)

100 % (of 12)

Philippines

Claveira et al. (2005)

  

34 %

Japan (Southern Anami Islands)

Kamiya et al. (1968)

  

44 % (of 82)

France

Davoust et al. (1997)

 

Rattus spp. (Rattus rattus diardii, R. norvegicus, and R. exulans)

21.6 %

Malaysia

Paramasvaran et al. (2009)

 

Rattus sp.

11.9 %

France—Lyon Zoo

Apéry (2012)

  

13 %

France—Vincennes Zoo

Apéry (2012)

 

Rattus rattus sladerni

38.8 %

China (Yunnan Province)

Shen et al. (2003)

  

33 % (1/3)

China (Yunnan Province)

Xiong et al. (1999)

 

Polynesian rat (Rattus exulans)

 

New Zealand

Roberts (1990)

   

Indonesia

Brown et al. (1975b)

   

Malaysia

Liat et al. (1977); Sinniah et al. (1979)

  

37.5 %

Malaysia

Syad-Arnez and Mohd Zain (2006)

 

Sikkim rat (Rattus andamanensis)

8.3 % (1/12)

Bangladesh

Fuehrer et al. (2012)

 

Rice-field rat (Rattus argentiventer)

 

Indonesia

Brown et al. (1975b)

   

Malaysia

Mulkit and Cheong (1971); Liat et al. (1977); Sinniah et al. (1979)

 

Lesser rice-field rat (Rattus losea)

5.4 %

Taiwan

Yang and Lu (2000)

  

38.9 %

China (Fujian Province)

Yuan et al. (2000)

 

Hoffmann's rat (Rattus hoffmanni)

 

Indonesia

Brown et al. (1975b)

 

Opossum rat (Rattus marmosurus)

 

Indonesia

Brown et al. (1975b)

 

Tanezumi rat (Rattus tanezumi)

 

Indonesia

Brown et al. (1975b); Wiroreno (1978)

   

Malaysia

Liat et al. (1977); Sinniah et al. (1979)

 

Rattus flavipectus (syn. for Rattus tanezumi)

12.9 % (20/155)

China (Henan)

Wang et al. (2013)

  

12.9 %

China (Henan Province)

Lin et al. (2007)

  

61.9 %

China (Hubei Province)

Zhou et al. (1991)

  

65.1 %

China (Yunnan Province)

Zhou et al. (1998)

  

49.4 % (of 881)

China (Yunnan Province)

Xiong et al. (1999)

  

77.5 %

China (Yunnan Province)

Shen et al. (2003)

  

44.3 %

China (Fujian Province)

Yuan et al. (2000)

  

13.1 %

China (Fujian Province)

Xue et al. (1998)

  

66.7 %

China (Fujian Province)

Zhang et al. (2003)

 

Malayan field rat (Rattus tiomanicus)

 

Malaysia

Mulkit and Cheong (1971); Liat et al. (1977); Sinniah et al. (1979)

  

44.4 %

Malaysia

Syad-Arnez and Mohd Zain (2006)

 

Annandale's rat (Rattus annandalei)

 

Malaysia

Liat et al. (1977); Sinniah et al. (1979)

 

Himalayan field rat (Rattus nitidus)

40.1 %

India

Malsawmtluangi and Tandon (2009)

 

Bush rat (Rattus fuscipes)

 

Australia

Singleton et al. (1991); Spratt and Singleton (1986)

 

Müller's giant Sunda rat (Sundamys muelleri)

 

Malaysia

Liat et al. (1977)

  

33.3 %

Malaysia

Syad-Arnez and Mohd Zain (2006)

 

Greater bandicoot rat (Bandicota indica)

 

Malaysia

Liat et al. (1977)

  

11.5 %

Taiwan

Yang and Lu (2000)

   

Sri Lanka

Dissanaike and Paramananthan (1961)

 

Lesser bandicoot rat (Bandicota bengalensis)

 

Bangladesh

Bhuiyan et al. (1995)

   

India

Pasricha et al. (1941)

  

33.3 % (6/18)

India

Singla et al. (2013)

 

Bower's white-toothed rat (Berylmys bowersi)

 

Malaysia

Liat et al. (1977)

  

16.6 %

India

Malsawmtluangi and Tandon (2009)

 

Kenneth's white-toothed rat (Berylmys mackenziei)

31.8 %

India

Malsawmtluangi and Tandon (2009)

 

Gray tree rat (Lenothrix canus)

 

Malaysia

Liat et al. (1977)

 

White-bellied rat (Niviventer niviventer)

 

Indonesia

Brown et al. (1975b)

 

Chestnut white-bellied rat (Niviventer fulvescens)

 

Malaysia

Liat et al. (1977)

  

40 %

India

Malsawmtluangi and Tandon (2009)

  

55.6 %

China (Fujian Province)

Yuan et al. (2000)

 

Dark-tailed tree rat (Niviventer cremoriventer)

 

Malaysia

Mulkit and Cheong (1971)

 

Chinese white-bellied rat (Niviventer confucianus)

30 %

China (Fujian Province)

Yuan et al. (2000)

 

Rattus nivivente (sug. syn. for Niviventer sp.)

6.12 % (3/49)

China (Henan)

Wang et al. (2013)

 

Edwards's long-tailed giant rat (Leopoldamys edwardsi)

 

Indonesia

Brown et al. (1975b)

   

Malaysia

Liat et al. (1977)

 

Long-tailed giant rat (Leopoldamys sabanus)

 

Indonesia

Brown et al. (1975b)

   

Malaysia

Mulkit and Cheong (1971); Liat et al. (1977)

 

Bartels's spiny rat (Maxomys bartelsii)

 

Indonesia

Brown et al. (1975b); Wiroreno (1978)

 

Hellwald's spiny rat (Maxomys hellwaldii)

 

Indonesia

Brown et al. (1975b)

 

Rajah spiny rat (Maxomys rajah)

 

Malaysia

Mulkit and Cheong (1971); Liat et al. (1977)

  

30.6 %

Malaysia

Syed-Arnez and Mohd Zain 2006

 

Musschenbroek's spiny rat (Maxomys musschenbroekii)

 

Indonesia

Brown et al. (1975b)

 

Whitehead's spiny rat (Maxomys whiteheadi)

 

Malaysia

Mulkit and Cheong (1971); Liat et al. (1977)

  

25 %

Malaysia

Syed-Arnez and Mohd Zain 2006

 

Red spiny rat (Maxomys surifer)

 

Malaysia

Liat et al. (1977)

  

30.4 %

Malaysia

(Syed-Arnez and Mohd Zain 2006)

 

Fawn-footed mosaic-tailed rat (Melomys cervinipes)

 

Australia

Singleton et al. (1991); Spratt and Singleton (1986)

 

Giant white-tailed rat (Uromys caudimaculatus)

24 %

Australia

Singleton et al. (1991)

 

Kaiser's rock rat (Aethomys kaiseri)

 

Rwanda

Fain (1955)

 

Hinde's rock rat (Aethomys hindei)

 

Democratic Republic of the Congo

Fain (1953)

 

Peters's striped mouse (Hybomys univittatus)

 

Democratic Republic of the Congo

Schwetz (1956)

 

African grass rat (Arvicanthis niloticus)

 

Democratic Republic of the Congo

Fain (1953)

 

African marsh rat (Dasymys incomtus)

 

Democratic Republic of the Congo

Fain (1953); Schwetz (1956)

 

House mouse (Mus musculus)

6.2 %

Spain

Mascato et al. (1993); Feliu et al. (1985); Castro (1944); Gallego Berenguer (1959)

  

2.6 % (1/39)

Israel

Wilamowski et al. (2002)

  

9.1 % (of 22)

Russia

Romašov (1983)

   

Russia

Romašov (1996)

   

Kazakhstan

Pleščëv and Kozlov (1978)

   

Turkey

Merdivenci (1970)

  

47.4 %

Austria

Juncker et al. (1998)

  

42.7 % (of 166)

Austria (Vienna—zoo)

Juncker-Voss et al. (2000)

   

Switzerland

Hörning (1966)

  

80 % (of 5)

Italy

Vanni (1947)

  

5.5 % (of 37)

Italy (Sicily)

Milazzo et al. (2010a)

  

21.2 % (of 52)

Portugal (Azores)

Casanova et al. (1996)

  

19.6 % (10/51)

Portugal (Azores)

Resendes et al. (2009)

  

40.2 % (of 92)

Portugal (Azores)

Pereira (2009)

  

22 % (11/50)

Portugal Lisbon Zoo

Crespo (2012)

   

USA

Childs et al. (1988)

   

USA (Maryland)

Luttermoser (1938)

   

USA (Pennsylvania)

Doran (1955)

  

0.9 % (of 110)

Iran

Pakdel et al. (2013)

  

4.6 % (of 410)

Pakistan

Ahmad et al. (2011)

  

2.1 % (1/47)

Bangladesh

Fuehrer et al. (2012)

   

Bangladesh

Bhuiyan et al. (1995)

  

19.1 %

China (Hubei Province)

Zhou et al. (1991)

  

21.1 %

China (Yunnan Province)

Zhou et al. (1998)

  

4.6 %

China (Fujian Province)

Xue et al. (1998)

  

10 %

China (Henan Province)

Lin et al. (2007)

  

10 % (13/130)

China (Henan)

Wang et al. (2013)

   

Australia (Queensland)

Singleton et al. (1991)

   

Australia release study

Singleton and Chambers (1996)

 

Long-tailed field mouse (Apodemus sylvaticus)

2/17

Austria

Frank (1977)

   

Switzerland

Hörning (1966)

  

7 % (of 99)

Switzerland (Geneva Canton)

Reperant and Deplazes (2005)

   

Belgium

Bernard (1961)

   

Former UDSSR

Pavlov (1955)

   

Spain

Feliu et al. (1984, 1985, 1987); Mas-Coma and Feliu (1977); Prokopič and Tenora (1975)

   

England

Baylis (1931)

  

75 % (of 58)

England

Canning et al. (1973)

  

100 %

St. Kilda, UK

Berry and Tricker (1969)

  

18 % (2/11)

UK Shetland Islands

Wilson et al. (1998)

   

Wales

Lewis (1968)

   

Slovakia

Mituch (1966/1970)

   

Bulgaria

Genov (1984); Prokopič and Genov (1974)

   

Russia

Romašov (1996)

   

Georgia

Kirschenblat (1948)

   

Armenia

Kirakosjan et al. (1963)

   

Middle Asia

Tokobaev (1976)

 

Yellow-necked mouse (Apodemus flavicollis)

 

Russia

Romašov (1978, 1996)

  

5.93 % (of 135)

Russia

Romašov (1983)

   

Bulgaria

Genov (1984); Prokopič and Genov (1974)

  

2 cases

Serbia

Ĉabrilo et al. (2013)

   

Slovakia

Mituch (1960); Mituch (1966/1970)

   

Former CSSR

Erhardová (1956); Erhardová and Ryšavy (1955); Prokopič and Genov (1974); Tenora (1963)

  

8.5 % (24/284)

Germany (Saxony-Anhalt)

Schmidt (2001)

  

6 cases

Denmark

Tenora et al. (1991)

 

Apodemus spp.

1.5 % (of 96)

France (forested area near Dijon)

Scandola et al. (2013)

   

Iran

Mobedi and Arfaa (1971)

 

Broad-toothed field mouse (Apodemus mystacinus)

 

Georgia

Kirschenblat (1948)

 

Striped field mouse (Apodemus agrarius)

 

Russia

Romašov (1978)

  

3.37 % (of 297)

Russia

Romašov (1983)

  

0.2 %

Russia (Southern West Siberia)

Chechulin et al. (2011)

   

Former UDSSR

Pavlov (1955)

   

Russia (Novosibirsk Region)

Koval'chuk and Bonina (1981)

  

4.27 % (5/117)

China (Henan)

Wang et al. (2013)

 

Small Japanese field mouse (Apodemus argenteus)

 

Japan

Chabaud et al. (1963); Ishimoto (1974); Iwaki et al. (1993)

 

Korean field mouse (Apodemus peninsulae)

 

Japan

Iwaki et al. (1993)

 

Large Japanese field mouse (Apodemus speciosus)

 

Japan

Iwaki et al. (1993)

 

Typical striped grass mouse (Lemniscomys striatus)

 

Democratic Republic of the Congo

Fain (1953)

 

Southern multimammate mouse (Mastomys coucha)

 

Democratic Republic of the Congo

Fain (1953); Schwetz (1956)

 

Natal multimammate mouse (Mastomys natalensis)

 

Ghana

Paperna et al. (1970)

   

South Africa

Cochrane et al. (1957)

 

Jackson's soft-furred mouse (Praomys jacksoni)

 

Democratic Republic of the Congo

Fain (1953)

 

Tropical Vlei rat (Otomys tropicalis)

 

Democratic Republic of the Congo

Fain (1953)

 

Creek groove-toothed swamp rat (Pelomys fallax)

 

Democratic Republic of the Congo

Schwetz (1956)

 

Bell groove-toothed swamp rat (Pelomys campanae)

 

Guinea

Joyeux et al. (1928)

 

Target rat (Stochomys longicaudatus)

 

Democratic Republic of the Congo

Schwetz (1956)

 

Ethiopian white-footed mouse (Stenocephalemys albipes)

0.5 % (1/212)

Ethiopia

Farhang-Azad and Schlitter (1978)

Deomyinae

Yellow-spotted brush-furred rat (Lophuromys flavopunctatus)

 

Democratic Republic of the Congo

Schwetz (1956)

 

Southern African spiny mouse (Acomys spinosissimus)

 

Zimbabwe

Sandground (1933)

Cricetidae

    

Arvicolinae

    
 

Bank vole (Myodes glareolus)

 

Russia

Romašov (1978, 1996)

  

37.36 % (of 1,159)

Russia

Romašov (1983)

  

1.4 %

Russia (Southern West Siberia)

Chechulin et al. (2011)

   

Former UDSSR

Pavlov (1955)

  

75 % (of 57)

England

Canning et al. (1973)

  

27.6 % (of 29)

France (forested area near Dijon)

Scandola et al. (2013)

  

15.1 % (22/146)

Germany (Saxony-Anhalt)

Schmidt et al. (1998); Schmidt (2001)

  

5.2 % (of 58)

Switzerland (Geneva Canton)

Reperant and Deplazes (2005)

   

Slovakia

Mituch (1960)

  

5.4 % (of 115)

Czech Republic

Rupeš (1964)

 

Northern red-backed vole (Myodes rutilus)

 

Former UDSSR

Pavlov (1955)

  

1 %

Russia (Southern West Siberia)

Chechulin et al. (2011)

 

Southern red-backed vole (Myodes gapperi)

 

USA

Fisher (1963)

  

9.5 % (28/294)

USA

Solomon and Handley (1971)

  

2.8 %

Canada (Alonquin Park)

Freeman and Wright (1960)

 

Grey red-backed vole (Myodes rufocanus)

 

Japan

Chabaud et al. (1963); Ishimoto (1974); Iwaki et al. (1993)

 

Northern mole vole (Ellobius talpinus)

 

Former UDSSR

Pavlov (1955)

 

Zaisan mole vole (Ellobius tancrei)

 

???

Mentioned in Tinnin et al. (2011)

 

Siberian brown lemming (Lemmus sibiricus)

 

Former UDSSR

Morozow (1956)

   

USA

Rausch (1961)

 

Southern bog lemming (Synaptomys cooperi)

 

Canada (Alonquin Park)

Freeman and Wright (1960)

 

Muskrat (Ondatra zibethicus)

 

Canada (Alonquin Park)

Freeman and Wright (1960)

   

Canada (Ontario)

Price (1931)

  

Laboratory infection studies

USA

Borucinska et al. (1997)

  

77 % (184/270)

USA (Pennsylvania and Connecticut)

Borucinska et al. (1993)

   

USA (Louisiana)

Penn (1952)

  

17 % (of 104)

USA (Maine)

Meyers and Reilly (1950)

   

USA (Michigan)

Ameel (1942)

   

Russia

Romašov (1995, 1996)

   

Former CSSR

Tenora and Zavadil (1967)

  

4.21 % (of 1,140)

Belgium

Cotteleer et al. (1982)

  

1 case (of 440)

Great Britain

Warwick (1937)

 

Field vole (Microtus agrestis)

3 cases (of 5)

Austria

Frank (1977)

  

16.67 % (of 6)

Russia

Romašov (1983)

   

Russia

Romašov (1978, 1996)

  

4.5 %

Russia (Southern West Siberia)

Chechulin et al. (2011)

 

Common vole (Microtus arvalis)

0.9 % (3/318)

Austria

Fuehrer et al. (2010)

  

4 cases (of 4)

Austria

Frank (1977)

  

20.69 % (of 29)

Russia

Romašov (1983)

   

Russia

Romašov (1996)

 

Rock vole (Microtus chrotorrhinus)

 

USA

Fisher (1963)

   

Canada

Freeman and Wright (1960); Lubinsky et al. (1971)

 

Meadow vole (Microtus pennsylvanicus)

 

Canada

Lubinsky et al. (1971)

  

9.4 % (of 769)

Canada (Alonquin Park)

Freeman and Wright (1960)

 

Tundra vole (Microtus oeconomus)

 

Former UDSSR

Morozow (1956)

  

3.4 %

Russia (Southern West Siberia)

Chechulin et al. (2011)

   

Canada

Freeman and Wright (1960)

 

Narrow-headed vole (Microtus gregalis)

 

Kyrgyzstan

Tokobaev (1960)

 

Günther's vole (Microtus guentheri)

1 case

England (zoo)

Redrobe and Patterson-Kane (2005)

 

Water vole (Arvicola terrestris)

1.1 % (1/98)

Austria

Fuehrer et al. (2010)

   

Russia

(Chechulin 1989); Romašov (1978, 1996)

  

10.4 %

Russia (Southern West Siberia)

Chechulin et al. (2011)

  

28.57 % (of 42)

Russia

Romašov (1983)

   

Switzerland

Hörning (1966)

  

0.2 % (of 466)

Switzerland (Geneva Canton)

Reperant and Deplazes (2005)

  

2 cases

England (zoo)

Redrobe and Patterson-Kane (2005)

 

European snow vole (Chionomys nivalis)

 

Former UDDSR

Pavlov (1955)

   

Former UDDSR

Kirschenblatt (1938)

 

Brandt's vole (Lasiopodomys brandtii)

 

China (Inner Mongolia)

Wan et al. (2007a)

Neotominae

Eastern wood rat (Neotoma floridana)

47.1 % (16/34)

USA

Solomon and Handley (1971)

 

Bushy-tailed woodrat (Neotoma cinerea)

 

USA

Rausch (1961)

 

Cotton mouse (Peromyscus gossypinus)

 

USA

Layne (1968, 1970); Layne and Winegarner (1971)

 

White-footed mouse (Peromyscus leucopus)

2.9 % (7/239)

USA

Solomon and Handley (1971)

 

Deer mouse (Peromyscus maniculatus)

10.2 % (73/713)

USA

Solomon and Handley (1971)

   

USA (lab experiments)

Meagher (1998)

   

Canada

Lubinsky (1957); Lubinsky et al. (1971); Freeman and Wright (1960); Freeman (1958); Wright (1961); Herman (1981)

   

Canada (Alberta)

Lubinsky (1956)

 

Florida mouse (Podomys floridanus)

 

USA

Rausch (1961); Layne (1968, 1970); Layne and Winegarner (1971)

  

12.7 % (21/723)

USA (Florida)

Layne and Griffo Jr (1961)

 

Reithrodontomys sp.

 

USA

King and Stanton (1974)

Cricetinae

Gray dwarf hamster (Cricetulus migratorius)

 

Former UDSSR

Pavlov (1955)

 

European hamster (Cricetus cricetus)

 

Austria

Frank (1977)

 

Greater long-tailed hamster (Tscherskia triton)

 

China (Henan)

Wang et al. (2013)

 

Campbell's dwarf hamster (Phodopus campbelli)

 

China (Inner Mongolia)

Wan et al. (2007a, b)

Sigmodontinae

Northern grass mouse (Necromys urichi)

 

Venezuela

Vogelsang and Espin (1949)

 

Hispid cotton rat (Sigmodon hispidus)

 

USA

Luttermoser (1937); Layne (1968, 1970)

   

USA (Texas)

Read (1949)

  

Freshwater marshes: 30 % (43/142); salt water marshes 12 % (4/34); upland habitats 5 % (1/22)

USA (Florida)

Kinsella (1974)

Gerbillinae

Savanna gerbil (Gerbilliscus validus)

 

Democratic Republic of the Congo

Fain (1953)

   

Democratic Republic of the Congo

Schwetz (1956)

 

Bushveld gerbil (Gerbilliscus leucogaster)

 

Democratic Republic of the Congo

Schwetz (1956)

 

Persian jird (Meriones persicus)

 

Armenia

Kirakosjan et al. (1963)

  

6.9 % (11/160)

Iran

Kia et al. (2010)

Cricetomyinae

Emin's pouched rat (Cricetomys emini)

17.7 %

Democratic Republic of the Congo

Malekani (1990), 1994)

   

Rwanda

Fain (1955)

 

Gambian pouched rat (Cricetomys gambianus)

30.8 %

Democratic Republic of the Congo

Malekani (1990), 1994)

   

Nigeria

Chineme and Ibrahim (1984)

Hepatic capillariasis—geographic distribution in Muroidea hosts

C. hepaticum has been found in Muroidean hosts in more than 60 countries in Europe; North, Central, and South America; Asia; Africa; and Oceania. R. norvegicus is the rodent species with the highest prevalences worldwide. In Europe, North America, South America, and Asia, several studies reported prevalences above 50 % in Norway rats (e.g., Easterbrook et al. 2007). Also other murid host species can present high prevalences in certain regions. In Asia, the nematode was found in prevalences above 50 % in the common species R. tanezumi and the white bellied rat (Niviventer fuloscens) (e.g., Yuan et al. 2000; Zhou et al. 1998). Furthermore, the muskrat (O. zibethicus) seems to be an important host of C. hepaticum in North America (Borucinska and Nielsen 1993). In the UK, high prevalences of this parasite were observed in long-tailed field mice (A. sylvaticus) and the bank vole (M. glareolus) (Canning et al. 1973).

Conclusions

C. hepaticum is a worldwide-distributed parasite with rodents of the superfamily Muroidea as main hosts. C. hepaticum has been described in more than 90 rodent species. Murinae and Arvicolinae are the hosts with the highest prevalences of this parasite. The Norway rat seems to be the most important host species with reported prevalences above 50 % on several continents. However, a high percentage of the studies dealt with Norway rats only, and not with less common murid rodents. Especially synanthropic (commensal and non-commensal) Murinae and Arvicolinae seem to be the most affected hosts.

However, the diagnosis of this pathogen is limited to liver biopsies and necroscopy and so the true prevalence in Muroidea and other mammals remains unclear. At spurious infections, care should be taken to exclude mix-ups with other Trichuridae and Capillaridae shedding eggs of almost similar morphology (e.g., Bork-Mimm and Rinder 2011; Di Cesare et al. 2011; Stuart et al. 2013; Traversa et al. 2011). Novel (molecular) diagnostic tools for proper (molecular) species classification are of urgent need.

Notes

Acknowledgments

I wish to thank all authors who provided personal copies of their manuscripts.

Conflict of interest

The author declares that he has no conflict of interest.

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Authors and Affiliations

  1. 1.Institute of Parasitology, Department of PathobiologyUniversity of Veterinary Medicine ViennaViennaAustria

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