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  • Travel Medicine and Infectious Disease (2014) 12, 582e591Available online at


    journal homepage: / tmidREVIEWCulinary delights and travel? A review ofzoonotic cestodiases and metacestodiases

    Akira Ito a,*, Christine M. Budke ba Department of Parasitology, NTD Research Laboratory, Asahikawa Medical University,Asahikawa 078-8510, Japanb Department of Veterinary Integrative Biosciences, College of Veterinary Medicine & BiomedicalSciences, Texas A & M University, College Station, TX 77843-4458, USAReceived 26 February 2014; received in revised form 22 June 2014; accepted 23 June 2014Available online 15 July 2014KEYWORDSFish tapeworm;Pork tapeworm;Beef tapeworm;Neurocysticercosis;Echinococcoses* Corresponding author. Tel.: 81 12429.

    E-mail address: [email protected] 2014 Elsevier Ltd. All rigSummary Due to increased globalization, food-borne parasitic infections are becoming moreprevalent worldwide, including in countries where these parasites and parasitic diseases hadpreviously been well controlled or eradicated. Improved sanitation, health education, andestablishment of appropriate food safety mechanisms can go a long way towards the controlof many these infections. However, food-borne parasitic infections are still common diseasesin developing countries, especially in rural areas. As many of todays travelers are looking toexplore more distant locations and partake in the local cuisine, they may be at greater risk ofacquiring a food-borne parasitic infection, including those caused by a number of adult andlarval tapeworms. This review discusses fish and meat-borne tapeworms and zoonotic meta-cestodiases of public health importance to both developing and developed countries, with afocus on infection prevention in travelers. 2014 Elsevier Ltd. All rights reserved.1. Introduction

    Food-borne parasitic infections can be a public health issuefor travelers partaking in local foods in endemic areas aswell as for the local inhabitants. Some tapeworms also havehumans as definitive hosts and, therefore, can be brought66 68 2686; fax: 81 166 68 (A.Ito).

    14.06.009hts reserved.from an endemic to a non-endemic region via an infectedperson. In this article, the most common food-borne tape-worm (cestode) infections are reviewed, focusing on trav-elers health issues [1].

    1.1. Fish-borne tapeworm infections

    Diphyllobothriaisis is caused by humans ingesting the larvalform of a number of species of fish tapeworms from theFamily Diphyllobothriidae. After ingesting infected under-cooked fish, humans can develop adult tapeworms in their

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  • Zoonotic cestode infections 583gastrointestinal tracts (diphyllobothriasis) (Fig. 1). Themost common cause of diphyllobothriasis from freshwaterfish is Diphyllobothrium latum, otherwise known as the fishtapeworm or the broad tapeworm. In 1976, Hunter et al. [2]indicated that D. latum was common in people living inthe Baltic countries, the western USSR, Finland, parts ofScandinavia and in certain endemic foci in the US andCanada. Since this early study, molecular analyses haverevealed that the family Diphyllobothriidae includesseveral genus and species which can infect humans via theingestion of freshwater or marine fish (Table 1) [3e11].Based on molecular evaluation, a number of parasitespreviously classified as D. latum are now considered inde-pendent species. For example, work by Yamane et al. [3] inJapan led to Diphyllobothrium nihonkaiense becoming aseparate species from D. latum [12e18].

    A review by Wicht et al. [9] described 11 species of thegenus Diphyllobothrium and one species of the genus Dip-logonoporus as being human health risks. D. latum is ac-quired from eating freshwater fish including pike, burbot,and perch. The other species of Diphyllobothrium are ac-quired from eating marine fish such as pacific salmon [10].Patients with diphyllobothriasis are frequently reportedfrom a number of Asian and Australasian countries,including Malaysia [8,19], Indonesia [20], Taiwan [5], andNew Zealand [21]. Infection with Diplogonoporus grandis isrelatively common in Japan, but is less common in othercountries [22e24]. Most infections with this parasite havebeen attributed to eating uncooked or undercooked sar-dines. Morishita [22] reviewed 40 human cases of D. grandisin Japan from 1892 to 1967. The majority of cases weremiddle-aged men. Most of the cases were not aware thatthey were parasitized until they expelled the tapewormFigure 1 Life cycle of Diphyllobothriumnaturally. It is believed that the natural definitive hosts, forthis parasite, are marine mammals, including whales, dol-phins, and porpoises [25].

    Fish tapeworm infections, especially with Diphyllo-bothrium nihonkaienze and Diphyllobothrium dendriticum,are becoming more common, including in traditionally non-endemic countries in Europe [26,27] and North America [28]where people eat raw fish that has been imported from thePacific Rim countries [10]. For example, D. latum has beenreported from non-endemic areas in Chile [29], Argentina[30], and Spain [31] and has been found in freshwater fishfrom French, Italian and Swiss Alpine lakes [9,14,31,32] aswell as in fish from Canadian freshwater lakes [33,34].Another species, Diphyllobothrium pacificum, has recentlybeen confirmed in infected patients in Chile [29].

    Due to available rapid freezing techniques, increasedspeed at which products are shipped around the world, andan increasing demand for sashimi and sushi, fish-bornetapeworm infections are likely to become more commonglobally. Human infection prevalence is dependent on theprevalence of the parasites in fish and local food safetyknowledge. While infections with fish tapeworms can beprevented through proper cooking techniques and foodsafety education, cases will likely continue to occur as longas raw fish remains a delicacy in many parts of the world[10,25].

    1.2. Meat-borne tapeworm infections

    The beef tapeworm, Taenia saginata, and the pork tape-worm, Taenia solium, are distributed globally. Humans arethe definitive hosts for both of these parasites, with cattleacting as the intermediate host of T. saginata and pigs actingspp. (from CDC, Atlanta, Georgia).

  • Table 1 Common sources of infection for human cesto-diasesa and metacestodiasesc.

    Source ofinfection

    Infection Parasite species

    Intestinal cestodiases

    Fish contaminated with metacestodes, plerocercoidsFresh water fish Diphyllobothriasisa Diphyllobothrium

    latumMarine fish Diphyllobothruasisa D. nihonkaiense,

    D. dendriticum,etc.Diplogonoporusgrandis

    Meat or viscera contaminated with metacestodes, cysticerciBeef Taeniasisa Taenia saginataPork (Dog meat) Taeniasisa T. soliumd

    Pig and cattleviscera

    Taeniasisa T. asiatica

    Chicken Sparganosisc Spirometraerinacei

    Wild foods contaminated with metacestodesSnake, frog etc. Sparganosisc S. erinacei

    Mesocestodiasisa Mesocestoideslineatus

    Beetles Hymenolepiasisa Hymenolepisnanad,H. diminuta

    Parenteral metacestodiases

    Eggs from animals or humans which infect humansDog, fox,

    wolf etc.Echinococcosesb Echinococcus spp.

    Human Cysticercosisb T. soliumd

    Hymenolepiasis H. nanad

    a Cestodiases with adult tapeworms in the intestinal lumendue to accidental ingestion of metacestodes.b Metacestodiases in parenteral tissues due to accidental

    ingestion of eggs.c Metacestodiases in parenteral tissues due to accidental

    ingestion of metacestodes (procercoid or plerocercoid) locatedin muscle of secondary intermediate or paratenic hosts. Adultworms may rarely develop in the intestines of humans.d Humans can be infected by ingesting eggs shed in the feces

    of a definitive host as well as from ingesting metacestodes inundercooked pork (T. solium) and in a beelte (H. nana).

    584 A. Ito, C.M. Budkeas the intermediate host of T. solium (Fig. 2). Humansbecome infected by ingesting cysts in undercooked infectedmeat. For T. solium, humans may also become infected withthe larval form if they ingest food contaminated with para-site eggs shed in the feces of an infected person, resulting incystic lesions in the central nervous system (neuro-cysticercosis) or other parts of the body (cysticercosis).Prevalence of these tapeworms will vary regionally due tobeef and pork preparation and consumption habits, whichmay be linked to religious observations. One study indicatedthat dogs may also be suitable intermediate hosts for T.solium, therefore, undercooked dogmeatmay also be a foodsafety hazard in endemic areas [35].

    A third species of human Taenia has been reported fromAsia (Asian Taenia) [36]. In the past, parasitologists hadbeen puzzled by the fact that T. saginata proglottids wereexpelled from people who ate pork, but not beef in thePhilippines, Indonesia, and Taiwan [36e43]. This newlydescribed parasite appears to be very similar in structure toT. saginata, but requires pigs as the intermediate hostsrather than cattle (Fig. 2) [36,41,43]. This new parasite waseventually given the name Taenia asiatica by Eom and Rim[44,45]. However, recent molecular studies, in Thailandand China, have identified tapeworms that are hybrids of T.saginata and T. asiatica [46e48], leading to the question ofwhether or not T. asiatica is truly as independent species.Furthermore, Fan [36] reported that metacestodes ofTaiwan Taenia (Z T. asiatica) were established in theliver of not only pigs but also of cattle [49]. Since both pigsand cattle may potentially be infected with T. asiatica [36],ingestion of uncooked liver from pigs or cattle could be apossible source for human infection.

    Data from rural and remote areas in Sichuan Province,China [50,51] and refugees villages in Thailand [52] suggestthat infection with T. asiatica is still quite rare. Field sur-veys using serology to detect antibody responses to anti-gens [53] have confirmed infection with T. solium (themajority of cases), Taenia hydatigena, and mixed T. soliumand T. hydatigena infections in pigs from China [50,51],Indonesia (Swastika et al. unpublished) and Thailand(Kusolsuk et al. unpublished). To date, these studies havenot identified pigs infected with T. asiatica.

    Eom et al. [54] reported that T. asiatica was present inJapan based on identification of this species from infectedJapanese citizens. However, travel histories were not takenon these patients. Indigenous T. asiatica cases, in Japan,were first confirmed in Tokyo in 2010 [55,56]. All taeniasiscases in Japan, except for those cases caused by T. asiaticain Tokyo [55,56], are believed to have been imported fromother endemic countries [57].

    Cultural and religious preferences, regarding meatpreparation and consumption, most likely play a role in thetransmission of T. solium, T. saginata, and T. asiatica [43].Taeniases caused by these three species are rather commonin remote and rural areas in countries where meat inspec-tion is limited and home slaughtering practices areroutinely conducted. However, global travel and immigra-tion can result in travelers to endemic countries becominginfected as well as travelers and immigrants from endemiccountries potentially introducing the parasites into non-endemic regions [55,58,59].

    1.3. Other miscellaneous tapeworm infections fromlocal foods

    While Taenia species result in the majority of human adulttapeworm cases globally, there are a number of othercestodes that can infect humans. For example, adulttapeworm infections may be acquired from eating back-yard chickens, snails, snakes or frogs infected with Mes-ocestoides lineatus [60e64] or Spirometra erinacei [64].While most patients infected with S. erinacei only developthe larval stage (sparganosis), a small proportion of infec-ted individuals develop adult tapeworms [65].

    The cestodes Hymenolepis nana (the dwarf tapeworm)and Hymenolepis diminuta (the rat tapeworm) are known

    AMUbeetle not beelte

  • Figure 2 Life cycle of three human taeniid tapeworms, Taenia solium, T. saginata and T. asiatica (modified from CDC, Atlanta,Georgia). Photos of ocular cysticercosis, neurocysticercosis, and massive taeniasis due to T. solium are from [117,74,114],respectively.

    Zoonotic cestode infections 585to infect humans through eating beetles containing thecysticercoid larvae of these parasites. H. nana can betransmitted via the ingestion of eggs shed in the feces of ahuman tapeworm carrier. While infected humans typicallydevelop adult tapeworms in their gastrointestinal tracts, H.nana infections may cause serious disseminated disease,especially in immuno-compromised individuals [66,67].Recently, numerous outbreaks of H. nana infections havebeen reported in children in Africa and South America[68e72], indicating that this parasite may be an emergingpublic health issue in endemic regions.

    1.4. The role of meat inspection

    Even countries with the most stringent meat hygiene re-quirements may experience occasional outbreaks of food-borne parasitic infections [56,58,59]. For example, therecent popularity of organic pork in some Europeancountries has the potential for increasing the risk of T.solium infection through allowing pigs to root and graze inareas that have been contaminated by a tapeworm carrier.This is especially true in regions with large immigrantpopulations from endemic countries who work in the agri-cultural sector [55,57e59]. Illegal meat markets have alsoresulted in taeniasis outbreaks in low endemicity areas[57]. For example, in Tokyo, Japan, an outbreak of T. asi-atica occurred in 2010 due to this practice [55e57]. Ascysticerci of T. asiatica appear as white milk spots on theliver surface and are similar in appearance to lesionscaused by the larval stage of the pig roundworm Ascarissuum [36], pigs with these liver lesions should always beinspected with extra care in areas where T. asiatica isknown to occur [55e57].1.5. Symptoms and treatment of intestinaltapeworm infections

    Intestinal cestode infections usually do not produce severeclinical signs and many tapeworm carriers do not know thatthey are infected until they start to pass tapeworm seg-ments. Individuals with very heavy infections may experi-ence abdominal pain, anorexia, nausea, diarrhea, andweight loss. Intestinal tapeworm infections are usuallytreated with antihelminthic drugs such as praziquantel,albendazole, or niclosamide. Chinese traditional medicineshave also been used by tapeworm sufferers [50,51].

    1.6. Prevention of food-borne parasite infections intravelers

    The simplest way for a traveler to avoid becoming infectedwith food-borne parasitic infections is simply not to eatuncooked or undercooked fish or meat or even unwashedfruits or vegetables but this advice is likely to fall on deafears. Recent sustainable education of local people to cookpork and viscera in Samosir Island, Indonesia has showndrastic decrease in the number of tapeworm carriers [73].However, enjoying local cuisine is viewed by many as anintegral part of the travel experience. In addition, whilenot consuming meat can prevent a person from becominginfected with certain parasitic disease, including cesto-diases and trichinosis, there are other parasites such as soiltransmitted helminthes that can be found on fresh vege-tation. Therefore, the next best way to prevent food-borneparasitic infections is to make sure that fish, meat andvegetables are appropriately cooked and reach a temper-ature high enough to kill any parasite larvae or eggs.

  • 586 A. Ito, C.M. Budke1.7. Larval cestode infections: cysticercosis,echinococcosis, sparganosis

    1.7.1. CysticercosisNeurocysticercosis, caused by invasion of the central ner-vous system by the larval stage of T. solium, is a leadingcause of epilepsy in regions where pigs are raised exten-sively with access to human fecal material and where meatinspection is lacking (Fig. 2) [74]. In addition to epilepsy,patients with neurocysticercosis may experience severechronic headaches as well as other neurological signs. Whileclinical signs associated with neurocysticercosis can be se-vere, patients may be asymptomatic for many years or forthe remainder of their lives [75].

    Since neurocysticercosis patients become infectedthrough ingestion of T. solium eggs shed in the feces of aparasite carrier, a risk factor for cysticercosis/neuro-cysticercosis is a person infected with the adult form of T.solium in the household [76,77]. Individuals with cysticer-cosis can either become infected via food contaminated bya tapeworm carrier or can be tapeworm carriers that infectthemselves due to poor hand hygiene [78,79]. However,since it can take years for symptoms to occur and for apatient to be diagnosed, the actual method of infection forindividual patients is often unknown. Molecular analysesare beginning to be used to identify the regional origin of aninfection when patients have a travel history that may haveallowed for exposure in numerous geographic locations[64,80,81].

    In addition to endemic areas in sub-Saharan Africa,South America, and many parts of Asia, cysticercosis casesare now becoming identified in regions previously believedto be free of the parasite. For example, in Bali, Indonesia,when patients were treated with the drug praziquantel forwhat was presumed to be T. saginata infections, some ofthese individuals developed seizures [43]. It was laterdetermined that these individuals were co-infected with T.saginata adult worms and the larval form of T. solium,resulting in neurocysticercosis. In non-endemic countries inEurope and North America, numerous cases of neuro-cysticercosis are also being detected in individuals whoeither emigrated from an endemic region or had a history oftravel to an endemic region [78].

    Cysticercosis is considered a worldwide emerging dis-ease due to travel and globalization [82], although theactual number of cases globally is not known. The goldstandard for the diagnosis of neurocysticercosis is neuro-imaging such as computed tomography scans and magneticresonance imaging [83]. However, there are a number ofFigure 3 Commercially available rapid serodiagnostic kits for alveCE) and cysticercosis (ADAMU-CC), (ICST Co. Ltd., Saitama, Japan).get a result within 20 min [77,101e103]. These kits will be licenseserological tests that can be used for ancillary diagnostics[53,84], such as the immunochromatographic rapid test(ADAMU-CC, ICST C. Ltd., Saitama, Japan) (Fig. 3) [77].

    1.7.2. EchinococcosesEchinococcoses are caused by accidental ingestion of eggsof several species of the genus Echinococcus (Fig. 4).Recent molecular re-evaluation of Echinococcus specieshave revealed that there are at least nine species, Echi-nococcus granulosus sensu stricto, Echinococcus equinus,Echinococcus ortleppi, Echinococcus canadensis, Echino-coccus felidis, Echinococcus multilocularis, Echinococcusshiquicus, Echinococcus vogeli and Echinococcus oligarthra[85e87]. E. granulosus sensu stricto, E. equinus, E.ortleppi, E. canadensis, and E. felidis comprise the speciesgroup E. granulosus sensu lato. All Echinococcus species areknown to be zoonotic except for E. felidis, E. shiquicus,and E. equinus. E. felidis is distributed exclusively in Africawith lions acting as definitive hosts [88]. While E. felidis isnot known to be zoonotic, human echinococcosis cases inAfrica are being evaluated using molecular methods to seeif there are, in fact, cases infected with this Echinococcusspecies. Another newly described species is E. shiquicus,which has only been found on the Tibetan plateau ofwestern China [89]. The only known definitive host, for thisspecies, is the Tibetan fox (Vulpes ferrilata). No humancases have been identified as being infected with thispathogen, but similar to E. felidis, this may be due to casesof E. shiquicus being previously attributed to another spe-cies of Echinococcus.

    Among the 9 known species of the genus Echinococcus,E. granulosus sensu stricto and E. multilocularis are themost prevalent globally and cause the most human cases.However, recent studies indicate that echinococcosis dueto E. canadensis may be more common than previouslybelieved and care should be taken to differentiate in-fections with E. granulosus sensu stricto and E. canadensis[90,91]. E granulosus sensu stricto is typically maintained ina cycle between dogs and sheep, whereas E. canadensis ismaintained in a cycle between wolves (Canis lupus) anddomestic livestock and/or wild ungulates [92]. In contrast,E. multilocularis is typically maintained between wild ca-nids such as red fox (Vulpes vulpes) and/or wolves andsmall mammals [92].

    Humans become infected after ingesting parasite eggsshed in the feces of an infected domestic or wild canid,resulting in cystic lesions that primarily develop in the liveror lungs [93]. Infection can occur from ingesting parasiteeggs that were on the hands of the food preparer or fromolar echinococcosis (ADAMU-AE), cystic echinococcosis (ADAMU-P: positive, N: negative. One drop of fresh blood is sufficient tod by the Ministry of Health, Labour and Welfare, Japan.

  • Figure 4 Life cycle of Echinococcus granulosus sensu stricto (from CDC, Atlanta, Georgia). All Echinococcus species completetheir life cycles using herbivorous or omnivorous intermediate hosts and carnivorous definitive hosts.

    Zoonotic cestode infections 587ingestion of food (e.g., vegetables or wild berries) thatwere contaminated directly from an infected dog or wildcanid. Urbanization may be, in part, responsible for thesecond infection route as wildlife, such as red foxes, areincreasingly found in urban settings in Europe [94e100].Diagnosis of echinococcoses is often made via diagnosticimaging (e.g., abdominal ultrasound, computed tomo-graphic scan, magnetic resonance imaging) in conjunctionwith serological evaluation with a test such as imunochro-matography (ADAMU-AE, ADAMU-CE, ICST Co. Ltd., Sai-tama, Japan) [101e103] (Fig. 3).

    1.7.3. SparganosisAs summarized in Table 1, adventurous eaters may be atrisk for infection with less common cestodes through theingestion of amphibians and reptiles [64,65,104e109]. Forexample, sparganosis, which is caused by the larval stage ofS. erinacei, has been associated with eating snakes in Asia,but may also be acquired through ingestion of frogs orbackyard chickens [64,65,104e108].

    1.8. Symptoms, treatment and prevention of larvalcestode infections

    Symptoms associated with larval cestode infections aredependent on the location of the larval stage of the para-site. T. solium cysticercosis has variable clinical signsdepending on the location of the cysts, with cysts located inthe central nervous system tending to cause the most se-vere disease, including epilepsy, severe chronic headachesand stroke [83,110e113]. In contrast, cysts located in otherbody systems, such as subcutaneous cysts, can be relativelybenign. Infection with Echinococcus spp. can present ashepatic disease, due to cysts in the liver, and can be mis-diagnosed as hepatic cancer by physicians in non-endemicregions that are not familiar with this parasitic zoonosis.Clinical manifestations associated with echinococcosis areoften due to the larval cysts pressing on surroundinganatomic structures, secondary bacterial infection of thecysts, or anaphylaxis caused by the rupture of a cyst.Creeping eruption, caused by S. erinacei, can result inpruritic lesions as the larval stage migrates in the subcu-taneous layer of the skin [64,65,104,105].

    Epilepsy-associated neurocysticercosis is often treatedwith anti-seizure medication. Antiparasitic drugs such aspraziquantel or albendazole are often accompanied byadministration of a corticosteroid [110e116]. Surgery forcysticercosis may be an option dependent on cyst location[117]. Active Echinococcus cysts may be treated withalbendazole, surgical intervention or a combination ofboth, while some cases can be monitored without the needfor intervention [118e120]. Sparganosis is usually treatedwith praziquantel and/or surgical intervention to removethe larvae.

    2. Conclusions

    There are numerous cestodes that can result in food-borneparasitic infections via the ingestion of infected fish andmeats or contaminated vegetation. Through globalization,travelers and immigrants are often at a greater risk foracquiring food-borne parasitic infections or bringing para-sites to new locations. In essence, parasites can beconsidered travelers as they are conveyed around in theworld in people and animals as well as via meat, fish, andcontaminated vegetation. Appropriate meat inspection and

  • 588 A. Ito, C.M. Budkefood hygiene practices can go a long way to preventingmany of these infections. However, no food can ever beguaranteed to be absolutely safe and travelers, as well asindividuals living in countries that are endemic for theseparasites, must remain ever vigilant.

    Conflict of interest



    The studies on cestode infections carried out by Ito havebeen supported by Grants-in-Aid for international collab-oration research funds from the Japan Society for thePromotion of Science (JSPS) (1994e2015) (06044089,07044243, 09044279, 10480235, 10557029, 11694259,12557024, 14256001, 17256002, 21256003, 22659083,24256002), by JSPS-Asia/Africa Scientific Platform Fund(2006e2011), the Special Coordination Fund for PromotingScience and Technology from the Ministry of Education,Culture, Sports, Science & Technology, Japan (MEXT)(2003-2005, 2010e2012), and the MEXT-TranslationalResearch Fund (2007e2011).References

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    Culinary delights and travel? A review of zoonotic cestodiases and metacestodiases1. Introduction1.1. Fish-borne tapeworm infections1.2. Meat-borne tapeworm infections1.3. Other miscellaneous tapeworm infections from local foods1.4. The role of meat inspection1.5. Symptoms and treatment of intestinal tapeworm infections1.6. Prevention of food-borne parasite infections in travelers1.7. Larval cestode infections: cysticercosis, echinococcosis, sparganosis1.7.1. Cysticercosis1.7.2. Echinococcoses1.7.3. Sparganosis

    1.8. Symptoms, treatment and prevention of larval cestode infections

    2. ConclusionsConflict of interestFundingReferences