In this light, at least to capture all cases reaching medical attention, it would be pivotal to implement a compulsory notification system, including both hospitalized patients and outpatients. However, the investigation of the epidemiology of CE in other animals, especially livestock, is surely of interest and should be envisaged as a future, complementary systematic review. Data curation, https://doi.org/10.1371/journal.pntd.0008519.s001, https://doi.org/10.1371/journal.pntd.0008519.s002, https://doi.org/10.1371/journal.pntd.0008519.s003, https://doi.org/10.1371/journal.pntd.0008519.s004, https://doi.org/10.1371/journal.pntd.0008519.s005. Although we did not perform a formal quality and bias assessment of the publications included, the results of our review highlight the presence of a paucity of human prevalence studies, the heterogeneity of data, and the patchy geographical coverage. Global Distribution of Alveolar and Cystic Echinococcosis. The tapeworm eggs are passed in the feces of the final host and are ingested by the intermediate host. Bethesda, MD 20894, Web Policies On the other hand, human CE is a chronic, disabling condition, its clinical manifestations ranging from asymptomatic infection to extremely severe disease, and costs for its treatment may be substantial. Thompson R.A. Parasite zoonoses and wildlife: One health, spillover and human activity. The life cycles of E. equinus and E. ortleppi both involve dogs as definitive hosts and horses and cattle as intermediate hosts, respectively [2]. Echinococcus multilocularis and Echinococcus shiquicus in a small mammal community on the eastern Tibetan Plateau: Host species composition, molecular prevalence, and epidemiological implications. Data curation, Fortunately, there is now widespread agreement based on morphological, molecular, and ecological criteria that Echinococcus should be split into ten species (Table 1). https://doi.org/10.1371/journal.pntd.0008519.g001. Dogs are the definitive hosts, and horses are considered intermediate hosts. This last portion of individuals with CE can only be quantified using population-based screening campaigns, which are extremely scant in the retrieved published literature. In the past, three genotypes were identified within the species E. granulosus, G1, G2, and G3, based on phenotypic differences (G2) and host preference (buffaloes, G3) [2]. The two other species, E. vogeli and E. oligarthus, cause polycystic echinococcosis but . Additional sources were searched up to October 2019: Google Scholar, Scopus, and Open Grey were used to identify articles that cited relevant reports using free-text terms (cystic echinococcosis, hydatidosis, Echinococcus granulosus). (family Taeniidae, class Cestoda) are zoonotic tapeworms currently infecting 2-3 million persons worldwide and causing US $200-$800 million in annual economic losses related to human infection (1,2).Infection appears to be increasing, reemerging, and geographically expanding in multiple locations across Europe, Asia, Africa, and the Americas (primarily in Latin America . In another recent ME study in south east Iran of 42 echinococcosis patients, 18 were infected with E. granulosus and 24 with E. intermedius (G6 genotype) [8]. Mulinge E., Magambo J., Odongo D., Njenga S., Zeyhle E., Mbae C., Kagendo D., Addy R.N.F., Ebi D., Wassermann M., et al. Canids are infected by consuming parts of an animal that contains these cysts. official website and that any information you provide is encrypted A common source of infection for dogs is offal from infected livestock. The intention was to make extracted data as much homogeneous as possible in terms of investigated population, allowing a fair comparison among areas. Molecular tools have had a major role in resolving the taxonomy of Echinococcus. was not investigated or the species of Echinococcus was not specified; 5) study duplication. Initially, E. granulosus was considered to be the most widespread species, with E. ortleppi present but with an apparently much more localised distribution. It was not possible to extract data for both human and animal infections from those studies investigating the two aspects at the same time. In terms of clinical management, molecular tools will increasingly inform and guide public health measures. After duplicates were removed, 572 records were further filtered by year of publication, leaving 471 papers published on or after the year 2000. There are four species of Echinococcus known to produce infections in humans. Accurate immunodiagnosis of the infection requires highly specific and sensitive antigens to be used in immunodiagnostic assays. The two most important forms in humans are cystic echinococcosis (hydatidosis) and alveolar echinococcosis. It is naturally transmitted between canids, definitive hosts harbouring the adult cestodes in the intestine and shedding parasite eggs with the faeces, and livestock, intermediate hosts getting infected upon ingestion of parasite eggs, where the larval stage (metacestode) develops in the form of fluid-filled cysts in liver, lungs and other organs. Is the Subject Area "Epidemiology" applicable to this article? Biology and Systematics of Echinococcus. Accurate immunodiagnosis of the infection requires highly specific and sensitive antigens to be used in immunodiagnostic assays. Each country is composed by one or more major regions (NUTS1 level) and each NUTS1 is divided in different NUTS2 areas. sampling fraction). 1 ). Our analysis did not allow for a statistically based inference on the relation between prevalence data in animal hosts and human incidence, but results from NUTS investigated for both human and animal infection suggest that a relation can be assumed. 2023 Apr 12;17(4):e0011210. Metwally D.M., Qassim L.E., Al-Turaiki I.M., Almeer R.S., El-Khadragy M.F. Results also highlight the well-known problem of underreporting of E. granulosus s.l. No, Is the Subject Area "Veterinary epidemiology" applicable to this article? For example, in the Middle East, dogs can be infected with E. granulosus and E. intermedius, as can sheep and camels (see below). Included cases were: i) for humans, data from hospital records and imaging studies; ii) for dogs, data from necropsy and coprological studies; iii) for ruminants, cases based on slaughter inspection. Of these, 24 were further excluded, leaving 79 publications from which data were extracted: 25 on human infection and 54 on animal infection. The molecular analysis confirmed the cyst has belonged to Echinococcus granulosus (G 1). Humans are considered dead-end hosts for E. granulosus. The search and selection of included studies is shown in Fig 1. with higher probability of accessing raw infected offal of intermediate hosts) such as sheep dogs or free-ranging dogs, since their main objective was to find positive dogs. However, the real health and economic burden due to CE are difficult to estimate. Lymbery A.J. e0008519. For example, authors of a recent study [33] were able to genetically characterise by sequence analysis the causative species of Echinococcus from hydatid fluid of patients in northern and western China. infection in different territories of European Mediterranean and Balkan countries presents high similarities between human and animal hosts, as shown by the four maps. 2022 Jun 29;38(2):101-120. doi: 10.47717/turkjsurg.2022.5757. In such situations, it is important to determine whether separate species do occur sympatrically, impeding control efforts and focussed public health interventions. Data extracted from the 25 publications on human infection were covering 7 eligible countries. This decision was based on the observation that other hosts seem of lower relevance for the epidemiology of human CE in the investigated geographical area [1, 94]. Echinococcus maintained in cycles involving wild and farmed cervids, moose (Alces alces), elk (wapiti) (Cervus elephas), and reindeer (caribou) (Rangifer tarandus), domestic pigs, and camels as intermediate hosts has long been recognised as distinct from E. granulosus [2]. Yes Cystic echinococcosis (CE) is a neglected parasitic zoonosis caused by infection with the cestode Echinococcus granulosus sensu lato species complex. In endemic areas, CE is responsible for significant health and economic losses, but its real burden is difficult to estimate. These studies complemented morphological descriptions of the adult parasites of cervid, pig, and camel origin (reviewed in Reference [18]). infection prevalence and incidence data in European Mediterranean and Balkan countries between 2000 and 2019, in both humans and animals, in an attempt to provide a picture of recent animal and human CE epidemiology in Europe, and their relation. For human case series, when both incidence rate and number of cases were reported, the population at risk was calculated. This aspect suggests that data extracted from these papers are comparable for the whole study area. official website and that any information you provide is encrypted Data Availability: All relevant data are within the manuscript and its Supporting Information files. Such spillover situations may result from wildlife encroaching into urban or peri-urban areas with transmission to susceptible domestic hosts, resulting in the establishment of domestic cycles. As an example, in these reports, the prevalence reported for sheep in Greece was constantly <2%, whereas values near to 30% were found in our review. Accessibility infection based on reported incidence or, when available, on reported cases (numerator) and size of the at risk population (denominator). sharing sensitive information, make sure youre on a federal The above mentioned two papers were abdominal ultrasound-based cross-sectional surveys, conducted on the rural populations of three countries, among which two were eligible for our study (Romania and Bulgaria). and transmitted securely. The two other species, E. vogeli and E . Echinococcosis is a parasitic disease that occurs in two main forms in humans: cystic echinococcosis (also known as hydatidosis) and alveolar echinococcosis, caused by the tapeworms Echinococcus granulosus and Echinococcus multilocularis, respectively. Kinkar L., Laurime T., Acosta-Jamett G., Andresiuk V., Balkaya I., Casulli A., Gasser R.B., Gonzlez L.M., Haag K.L., Zait H., et al. Shang J., Zhang G., Yu W., He W., Wang Q., Zhong B., Wang Q., Liao S., Li R., Chen F., et al. Genetic characterization of human-derived hydatid fluid based on mitochondrial gene sequencing in individuals from northern and western China. This has resulted from a lack of useful morphological characters, and where the importance of host occurrence was often overshadowed by taxonomic considerations [2]. Shen C, Zhu X, Xu X, Chang H, Ni Y, Li C, He K, Chen L, Chen L, Hou M, Ji M, Xu Z. Pathogens. 56. . Although molecular tools have been valuable in confirming the genetic distinctness of these forms, and subsequently, ME studies have demonstrated different host ranges and geographic distributions, nomenclatural issues have impeded a clear understanding of their transmission cycles (reviewed in Reference [18]). Although morphology can be used to differentiate between adult worms of the different species, this approach is often not practical given the difficulties in recovering adult specimens and the associated public health risks involved. Acta Trop. human and animal infection in this area in 20002019. For more information about PLOS Subject Areas, click Kinkar L., Laurime T., Sharbatkhori M., Mirhendi H., Kia E.B., Ponce-Gordo F., Andresiuk V., Simsek S., Lavikainen A., Irshadullah M., et al. In Bolivia, a recent ME study reported the presence of E. granulosus, E. ortleppi, and E. intermedius in sheep, cattle, and pigs, respectively [9]. To merge data from different epidemiological units at NUTS1 level, the pooled prevalence and 95% Confidence Interval (CI) were estimated, based on the inverse variance method and logit transformation [9] to account for study weight with respect to population size (i.e. In Spain, Benner and colleagues [5] estimated, for the year 2005, and overall economic loss due to human and livestock CE of about 150 million, of which about 130 million were human-associated and about 16 million animal-associated. This geographical area, where E. granulosus s.l. Humans act as accidental, dead-end intermediate hosts, acquiring the infection through ingestion of parasite eggs and developing echinococcal cysts mostly in the liver, followed by lungs [2]. Also, prevalence studies were extremely scant. Formal analysis, The data analysis was carried out as described above, for prevalence estimation. Ali V., Martinez E., Duran P., Selez M.A., Barragan M., Nogales P., Lillo A.P.Y., Castaares M., Claros Y., Deplazes P., et al. According to NUTS regulation, minimum and maximum population thresholds for the size of NUTS1 and NUTS2 levels are 3,000,0007,000,000 and 800,0003,000,000, respectively. It is principally maintained in cycles involving livestock but spillover into wildlife occurs in some areas, such as Australia (see above). Little is known about the geographical distribution and host range of the two sylvatic species in South America, E. oligarthra and E. vogeli. In these units the population at risk ranged from a minimum of 73,529 to a maximum of 6,250,000 persons, but it was comprised in most cases (75%; 66/87) between 500,000 and 3,000,000. Laurime T., Kinkar L., Moks E., Romig T., Omer R.A., Casulli A., Umhang G., Bagrade G., Irshadullah M., Sharbatkhori M., et al. In our review, the single-year figure for human population at risk could be estimated only in the 87 epidemiological units of the 4 papers where incidence value was associated with the number of new cases for each year. Echinococcus is an infection caused by a parasitic tapeworm from the Echinococcus genus. As for human studies, data for cattle and sheep were not available for the Balkan area. For example, in parts of Europe and the Middle East, sheep, cattle, horses, pigs, and camels may be infected with E. granulosus, E. equinus, E. ortleppi, and E. intermedius, all of which, apart from E. equinus, are of public health significance [2,3,7]. infection in human and domestic animal hosts in European Mediterranean and Balkan countries: A systematic review. 2005 Jul;95(1):9-15. doi: 10.1016/j.actatropica.2005.03.005. The taeniid tapeworm Echinococcus granulosus is the causative agent of the echinococcal disease, an important zoonosis with worldwide distribution. The decision to refer extracted data to the NUTS level was due to the need of clustering data in regions of comparable size, at least in terms of human population. In this view, mixed Th2 and regulatory responses allow parasite survival. MEDLINE, EMBASE, Scopus, Google Scholar and Open Grey databases were searched. ? 2022 Jul-Sep;17(3):358-365. doi: 10.18502/ijpa.v17i3.10626. Dog populations were mostly investigated through cross-sectional surveys, showing mean prevalence values ranging from 0 to 31.86%. Another ME study of wild canids on both sides of the CanadaUSA border in eastern North America, found wolves and coyotes infected with E. canadensis, and discriminated between the G8 and G10 genotypes, finding single and mixed infections of these genotypes in both canid species [23]. Conceptualization, Its life cycle develops in dogs and other canids, which harbor the adult tapeworm in the intestine, and herbivores (or humans as dead-end occasional host) as intermediate hosts, where the larval metacestode form develops in different . is especially present in areas where livestock breeding is practiced, including European Mediterranean and Balkan countries. Santa M.A., Pastran S.A., Klein C., Duignan P., Ruckstuhl K., Romig T., Massolo A. Detecting co-infections of. Molecular epidemiology has made a major contribution to understanding the extensive genetic and phenotypic variation exhibited within the genus Echinococcus [2,3]. Canids are usually asymptomatic. Besides, the ample variability of diagnostic techniques used by different studies is alone sufficient to hamper any possibility of comparing data among areas. Echinococcus granulosus is the most widespread species causing cystic echinococcosis in humans and has the broadest intermediate host range [2,3]. infection in both humans and animals. We carried out a systematic literature review on E. granulosus s.l. However, again, presence and type of disease notification systems vary greatly from country to country, and mostly include only hospitalized cases [6]. Molecular epidemiology (ME) has revolutionised our understanding of infectious disease transmission. This study showed a significantly high proportion of CE patients infected with the G6 genotype, particularly in the southern parts of the province [8]. This is an open access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited. If the NUTS2 level was not specified, data were referred to the NUTS1 level, and if also the NUTS1 specification was absent, data were referred to the national level. It provides laboratory and analytical tools that can characterise infectious agents in investigations focused on the aetiology of infectious diseases. This enigmatic variant of Echinococcus multilocularis, which is seemingly restricted to parts of China [7], remains little understood in terms of host range and zoonotic potential. The drinking water source is also a major risk factor . In the case of cross-sectional studies, we addressed the problem of limited homogeneity among studies in animals (all papers) and humans (only 2 papers), calculating the pooled prevalence, which accounts for the differences in the investigated populations size (i.e. where the infection has a health impact requiring treatment) can be present in all above-mentioned categories [10,88], due to the proteiform clinical characteristics of CE and its neglected status, with generally poor awareness of both at-risk populations and health care personnel, and consequent misdiagnosis and underreporting. Kern P., Menezes da Silva A., Akhan O., Mullhaupt B., Vizcaychipi K.A., Budke C., Vuitton D.A. Potentially eligible studies were excluded if: 1) full text and abstract were both unavailable or only the abstract was available but did not convey the needed data; 2) infection cases (numerator) and size of the studied population (denominator) or calculated incidence/prevalence were not extractable; 3) diagnostic method was not mentioned or not eligible; 4) E. granulosus s.l. In the present study we investigated differences in spatial distribution of E. granulosus s.l., referring data extracted from the available literature to an artificial epidemiological unit (one NUTS2 in one year) created ad hoc. Many different diagnostic techniques were applied, including flotation copromicroscopy or taeniid eggs isolation complemented by PCR for species identification, coproELISA, coproPCR, and necroscopic examination (variably including intestinal mucosa scraping and other poorly specified techniques). Wang X., Liu J., Zuo Q., Mu Z., Weng X., Sun X., Wang J., Boufana B., Craig P.S., Giraudoux P., et al. Echinococcus granulosus is common in the sheep-raising areas of the Mediterranean, Middle East, Australia, New Zealand, South Africa, and South America. Limitation of evidence included the paucity of human prevalence studies, data heterogeneity, and the patchy geographical coverage, with lack of data especially for the Balkans. In these cases, the type of data aggregation is specified, namely multi-years if different (usually subsequent) years of the same NUTS2 were included in the study, or multi-area if different NUTS2 were assessed. Echinococcosis, a global disease of which there are two forms, cystic and alveolar, is caused by the cestode parasite Echinococcus. Bethesda, MD 20894, Web Policies The adult cestode inhabits the small intestine of a carnivore (definitive host) and produces eggs containing infective oncospheres. Echinococcus has a long history of taxonomic and nomenclatural confusion, particularly regarding the species level taxonomy [2]. maintenance [92,93]. : Not known. No restriction was applied regarding language or publication status (published or in press). In a few cases also bovine farm dogs (n = 3), hunting dogs (n = 3) and pet dogs (n = 1) were included among surveyed animals. When considering the epidemiology of any infectious disease, understanding its aetiology is central. No, Is the Subject Area "Sheep" applicable to this article? Infection involves the development of cysts, primarily in the lungs and liver, causing damage as they enlarge like a slowly growing tumor. However, it is worth noting that some multi-year studies described such kind of temporal trends, usually showing a decreasing trend of the disease burden in humans [14,17,21,32], whereas in animals both decreasing and stable trends were reported [34,41,65]. Our results confirm Italy, Spain, and Eastern Europe being the most affected areas, but data are extremely heterogeneous, geographical coverage very patchy, and human prevalence studies extremely scant. PLoS Negl Trop Dis 14(8): Data were extracted from 79 publications, 25 on human infection (covering 437 epidemiological units), and 54 on animal infection (52 epidemiological units for cattle, 35 for sheep and 25 for dogs). Furthermore, being CE a chronic and complex infection requiring long-term follow-up, distinction between incidence of first clinical diagnoses and incidence simply calculated using retrospective clinical records would be important but was seldom specified. Data at country level are reported only if more detailed data at NUTS1 level were not available (source of NUTS shapefiles: Eurostat). Among these, E. granulosus and E. multilocularis are the most common ones responsible for causing cystic echinococcosis (CE) and alveolar echinococcosis (AE), respectively. HHS Vulnerability Disclosure, Help Also, the different inclusion criteria for cases series (all clinically observed cases or hospitalized cases) and the frequently unclear definition of the population at risk had an important impact on the estimation of incidence rate, as evidenced by the studies in North-eastern (ES2) and Central Spain [1315,17]. Echinococcus requires two mammalian hosts to complete its life cycle: a carnivore as a definitive host and a herbivorous or omnivorous intermediate host, which may include humans. To estimate incidence at NUTS1 level, the average of all values reported for all epidemiological units belonging to the same NUTS1 was calculated. eCollection 2022 Jun. Higher prevalence values were similarly found for sheep and cattle in Central (ITI), Southern and insular Italy, and in Romania (>10%), whereas high rates were encountered only for sheep in Greece. Genetic variation of mitochondrial genes among Echinococcus multilocularis isolates collected in western China. Investigation, In endemic regions where multiple species of Echinococcus are maintained in sympatric cycles of transmission, and humans are at risk of infection, it is important to determine the species responsible for clinical infections. Belonging to the family Taeniidae, the tapeworm Echinococcus is responsible for causing echinococcosis in humans. The PubMed wordmark and PubMed logo are registered trademarks of the U.S. Department of Health and Human Services (HHS). Occurrence of Liver Hydatid Cysts in a Donkey and Molecular Characterization of Echinococcus equinus. The diagnosis of Echinococcus granulosus in dogs. Data at country level are reported only if more detailed data at NUTS1 level were not available (source of NUTS shapefiles: Eurostat). 4. Adult worms live in the intestines of dogs that are the definitive host. Our results confirm that Italy, Spain, and Eastern Europe are the most affected areas, but data are extremely heterogeneous, geographical coverage very patchy, and human prevalence studies extremely scant. CE = Cystic Echinococcosis, AE = Alveolar Echinococcosis, PE = Polysystic Echinococcosis. This was recommended earlier [21] since the name E. intermedius had been previously proposed for the species in pigs and camels (reviewed in Reference [18]). Turkish HPB Surgery Association consensus report on hepatic cystic, Evaluation of the Ability of Antigen B Originated from, Identification and Characterization of Antigenic Properties of. The most common antigenic sources used for the immunodiagnosis of echinococcal disease are hydatid cyst fluid, somatic extracts and excretory-secretory products from protoscoleces or adults of E. granulosus. Yes Echinococcus multilocularis occurs mainly in Central Europe, Alaska, Canada, and Siberia. Like the red fox, the coyote is a successful urban adapter, and is increasingly seen as a public health risk in urban environments in North America. As a consequence, we did not compare incidence and prevalence data among different periods in the years (19952019) covered by our review. Recent ME studies in Calgary, Canada, found that coyotes were frequently infected with E. multilocularis [7,28]. Consequently, prevalence and clinical-based studies are complementary and not mutually exclusive, not only for the understanding of CE epidemiology on a territory, but also for burden of disease estimates and public health evaluations. Unexpected Echinococcus multilocularis infections in shepherd dogs and wolves in south-western Italian Alps: A new endemic area? The site is secure. It is worth mentioning that in this review we did not include data of livestock intermediate hosts other than sheep and cattle that can have a role in the human infection epidemiology, such as swine and goats. Echinococcosis is a zoonotic infection caused by cestode species of the genus Echinococcus. No, Is the Subject Area "Dogs" applicable to this article? The larval forms of taeniid cestodes belonging to the genus Echinococcus are the source of the zoonotic infection known as echinococcosis. With echinococcosis, this has been problematic in many endemic areas where different host species are involved and there is a need to understand their role in transmission [2]. However, in Mazandaran Province in Iran, E. granulosus was found in an ME study to be the only species in livestock and humans [10] and in Saudi Arabia, an ME study in Riyadh found only E. granulosus in sheep and camels [11]. Molecular tools also allow species identification from eggs in faeces. The results of our study show the importance of this neglected infection in the study area and strongly prompt public health authorities to implement surveillance strategies for both human and animal infection. Taxonomy and Nomenclature . A similar situation has also emerged involving coyotes infected with E. multilocularis in urban areas of North America [7]. Recent ME studies are beginning to shed light on aspects of host preference. Actually, data obtained from literature were extremely variable from different points of view, including the real extension of studied populations (e.g. A total of 500 records were therefore screened for potential eligibility by title and abstract, of which 103 were selected for full-text review: 37 on human infection, 8 on both human and animal infection, and 58 on animal infection. CE, or hydatidosis, is caused by the larval stage (metacestode) of Echinococcus granulosus (E. granulosus). Echinococcus in wild canids in Qubec (Canada) and Maine (USA). Multiple-bead assay for the differential serodiagnosis of neglected human cestodiases: Neurocysticercosis and cystic echinococcosis. All but two papers [10,11] were retrospective case series: hospitalized cases (n = 15) based on HDR, or based on clinical records of cases who reached clinical attention (n = 6), or surgical cases (n = 2). The taeniid tapeworm Echinococcus granulosus is the causative agent of the echinococcal disease, an important zoonosis with worldwide distribution. Funding: RC received a grant (BIRD174940), by the Department of Animal Medicine, Production and Health of the University of Padova (https://www.maps.unipd.it/). here. has been included since 2015 [6,98100]. Echinococcus granulosus has a world-wide geographic distribution (Figure 2), occurring on all continents with highest prevalence occurring in parts of Eurasia . We carried out a systematic literature review on the epidemiology of E. granulosus s.l. Similarly, co-infections of E. multilocularis and E. canadensis were reported in coyotes and red foxes in Alberta, Canada, using real-time PCR [30]. This in turn contributes to the neglect of CE, with subsequent little focus on accurate and representative data collection, feeding a vicious circle of data inaccuracy, underestimation, and neglect. Thompson R.A. Echinococcus granulosus eggs can only be inactivated after being stored at 80 C for at least 7 days, and they can survive for > 200 days at 7 C and 50 days at 21 C . Resources, Molecular approaches have now confirmed that the four genotypes represent two, possibly three species [18,20]. Disclaimer. and transmitted securely. Cystic echinococcosis (CE) is a neglected zoonosis caused by infection with the parasite Echinococcus granulosus sensu lato, naturally transmitted between canids and livestock; CE in humans can be a serious condition. In some cases, European-type strains have been identified from cyst tissue from affected dogs [7]. Molecular epidemiological studies have been instrumental in identifying and describing cycles of transmission involving more than one species of Echinococcus. Careers. Accessibility ztrk G, Uzun MA, zkan F, Kayaalp C, Tatl F, Eren S, Aksungur N, oker A, Bostanc EB, ter V, Kaya E, Taar P. Turk J Surg. Also the data on animal infection are not uniformly distributed in the study area, as demonstrated by the differences in number of epidemiological units investigated in selected countries, with Italy and Romania generally representing the most investigated countries. Overall, larval Echinococcus infections induce strong regulatory . However, recent ME studies in Sudan and Ethiopia demonstrated cattle to be epidemiologically the most important intermediate host for E. granulosus as well as E. ortleppi and E. intermedius [12,13]. Federal government websites often end in .gov or .mil. The definitive hosts in turn acquire the infection by eating parasite cysts in infected organs of slaughtered animals. Httner M., Nakao M., Wassermann M., Siefert L., Boomker J.D., Dinkel A., Sako Y., Mackenstedt U., Romig T., Ito A. The pooled prevalence and its 95% CI for each investigated NUTS1 are reported in Tables 3, 4 and 5, respectively for cattle, sheep and dogs. No, Is the Subject Area "Europe" applicable to this article? The origin of the name E. intermedius has been discussed in detail and since it emanates from a country, Spain (reviewed in Reference [18]), where E. granulosus, E. equinus, and G7/E. In studies where human infection was investigated through a cross-sectional survey, the sum of positive cases (numerator) and tested individuals (denominator) was calculated for each epidemiological unit. However, ME studies are required to fully document the distribution of the different species, their host range, and the occurrence of sympatric cycles of transmission. Molecular phylogeny based on six nuclear genes demonstrated that G6/G7 and G8/G10 should be regarded as two distinct species, E. intermedius and E. canadensis [20] (Table 1). This article is an open access article distributed under the terms and conditions of the Creative Commons Attribution (CC BY) license (. Funding acquisition, Writing review & editing. sampling fraction) and variance effect (i.e. The immune response generated by the host against the metacestode induces a permissive Th2 response, as opposed to pro-inflammatory Th1 response. Human hosts are infected accidentally via hand to mouth and/or foodborne/waterborne pathways. infection prevalences of 3.8% were reported for farm dogs in Lithuania 55 and 10.6% for farm dogs in Wales. Ahmed M.E., Salim B., Grobusch M., Aradaib I.E. For ruminants, studies based on pathological examination after slaughter were included. Interestingly, the first ME study undertaken on echinococcosis in Bhutan demonstrated local transmission of both E. ortleppi and E. granulosus [17]. Echinococcus granulosus (sensu lato) causes cystic echinococcosis and is the form most frequently encountered. Co-infection of E. ortleppi and E. multiloculalris was also identified in two wolves. Equally, we did not address E. granulosus s.l. Papers reporting data from the following European Mediterranean and Balkan countries were included (from West to East): Portugal, Spain, France, Italy, Slovenia, Serbia, Croatia, Bosnia-Herzegovina, Montenegro, Macedonia, FYROM (Former Yugoslav Republic Of Macedonia), Republic of North Macedonia, Kosovo, Albania, Greece, Romania, Bulgaria and Cyprus. 2022 Jan 14;16(1):e0010109. In addition, the situation is often compounded in areas where there is the possibility of spillover between domestic, rural, or urban cycles of transmission and cycles involving wildlife [1]. https://doi.org/10.1371/journal.pntd.0008519.g003, https://doi.org/10.1371/journal.pntd.0008519.g004, https://doi.org/10.1371/journal.pntd.0008519.g005, https://doi.org/10.1371/journal.pntd.0008519.t003, https://doi.org/10.1371/journal.pntd.0008519.t004, https://doi.org/10.1371/journal.pntd.0008519.t005. Cystic echinococcosis (CE) is a neglected zoonosis caused by infection with the cestode Echinococcus granulosus sensu lato. The 23 retrospective case series studies were mostly reporting multi-year data: 14 papers recorded incidence values for each year, in eight publications a single incidence value was reported for the whole period, and one study investigated a 1-year period. Li J.-Q., Li L., Fan Y.-L., Fu B.-Q., Zhu X.-Q., Yan H.-B., Jia W. Genetic Diversity in Echinococcus multilocularis from the Plateau Vole and Plateau Pika in Jiuzhi County, Qinghai Province, China. Evaluation of enzyme linked immunosorbent assay, utilizing native antigen B for serodiagnosis of human hydatidosis. 2022 Oct 26;11(11):1238. doi: 10.3390/pathogens11111238. infection in wild definitive and intermediate hosts such as sylvatic canids and wild boars or wild ungulates. research paper or conference report) or setting (e.g. http://creativecommons.org/licenses/by/4.0/, Sheep (cattle, pigs, camels, goats, macropods), Warthog, (zebra, wildebeest, bushpig, buffalo, various antelope, giraffe Hippopotamus? Would you like email updates of new search results? Data curation, The NUTS classification is a hierarchical system for dividing the territory of the European countries. Massolo A., Valli D., Wassermann M., Cavallero S., DAmelio S., Meriggi A., Torretta E., Serafini M., Casulli A., Zambon L., et al. This will be of most significance in areas where multiple cycles of transmission operate and where there is the possibility of mixed infections. Similar studies in China are starting to reveal a complex diversity of infection patterns in humans infected with E. multilocularis. Among these, retrospective studies reporting data from investigations starting before 1980 were also excluded. Alveolar and cystic echinococcosis are caused by Echinococcus multilocularis and Echinococcus granulosus (s. s), respectively. Indeed, clinically relevant cases (i.e. Results also highlight the notorious problem of underreporting of E. granulosus s.l. Yes The work is presented according to the recommendations of the Preferred Reporting Items for Systematic Reviews and Meta-Analyses (PRISMA http://prisma-statement.org/prismastatement/Checklist.aspx, S1 PRISMA Check list). The infected dogs shed a huge number of eggs of Echinococcus granulosus daily and are the main source of soil, food, and vegetable contamination. For what concerns the spatial distribution of human CE, the results of our study, granted the absence of data from many Balkan countries, indicate Southern (ITF) and insular (ITG) Italy, Spain, and Eastern Europe (Bulgaria and Romania) as the most affected areas, in line with other recent narrative reviews [1] and official WHO data [90]. Hydatid cysts with viable protoscolices have been found in the livers of some horses.200 Exophthalmos is the only reported ocular manifestation of hydatid cyst disease in horses, and it is due to cysts in the orbital tissues. As an example, if we consider the recent work by Piseddu and colleagues examining HDR for CE in Italy from 2001 to 2014 [4], the median of CE hospitalizations per year was 848. The European Register of CE (ERCE) [89], if adopted at national level by health authorities, could represent a suitable platform for such a system. The echinococcoses: Diagnosis, clinical management and burden of disease. The https:// ensures that you are connecting to the Cystic echinocccosis (CE), also known as hydatid disease, is caused by infection with the larval stage of Echinococcus granulosus, a ~2-7 millimeter long tapeworm found in dogs (definitive host) and sheep, cattle, goats, and pigs (intermediate hosts). Sadjjadi SF, Mohammadzadeh T, Hafezi F, Sadjjadi SM. The following databases were searched for relevant studies: MEDLINE (PubMed) (1966 to October 19th 2019) and EMBASE (1974 to October 19th 2019). Inclusion in an NLM database does not imply endorsement of, or agreement with, The implementation of new studies on human incidence and prevalence and bovine prevalence, appropriately defined in their methodology and covering the geographical areas still not investigated, could help in completing the picture already drafted by our review. Molecular diagnostic approaches have been shown to be valuable tools in this respect. An official website of the United States government. Thompson R.A. The spatial patterns of CE distributions in the three animal hosts are shown in Figs 35. 2007 Apr;25(4):263-9. doi: 10.1157/13100468. Finally, regarding animal characteristics and subpopulations, in most cases no specific information was provided on sheep and cattle, with the exception of four studies where only adult animals (sheep >2 or 3 years; cattle >2 or 5 years) were included. The choice of an approp Infection with cestodes of the species Echinococcus in the metacestode stage causes human echinococcosis, . Although infections in lions was known to occur for many years, it is only relatively recently that adult worms from lions were characterised using molecular tools and confirmed to be a distinct species, E. felidis [31]. In all investigated populations, at least one positive animal was found, and pooled prevalence values at NUTS1 level varied from 0.003% to 64.09% in cattle, and from 0.004% to 68.73% in sheep. Data were extracted from 79 publications, and referred to Nomenclature of Territorial Units for Statistics (NUTS) levels per year. Genetic polymorphism and population structure of Echinococcus ortleppi. ME detection of these European strains coincided with the detection of cases of alveolar hydatid disease in dogs in Canada for the first time. Writing original draft, In this case, the resulting sylvatic cycle can operate independently but provides a constant source of infection that can spill over back to domestic hosts. As well as alveolar echincoccosis, cystic echinococcosis is also prevalent in humans in western China [34]. No, Is the Subject Area "Livestock" applicable to this article? Besides, few and spatially limited studies on animal hosts were retrieved for the Iberian Peninsula. Siracusano A, Buttari B, Delunardo F, Profumo E, Margutti P, Ortona E, Rigan R, Teggi A. Sadjjadi SM, Abidi H, Sarkari B, Izadpanah A, Kazemian S. Enferm Infecc Microbiol Clin. Human cystic echinococcosis (CE) is highly endemic in the Tibetan regions of Sichuan where most families keep guard dogs and where there are considerable numbers of ownerless/stray dogs. No, Is the Subject Area "Italy" applicable to this article? Updated from References [2,3]. Concerning clinical-based studies, major limitations of most studies for the understanding of CE epidemiology are their heterogeneity in terms of type of cases included (such as all cases reaching medical attention, or hospitalized cases, or surgically confirmed ones, or only residents in a particular area) and the frequent lack of reporting of the at-risk population to which the incidence estimate refers. Overall, the two papers based on abdominal ultrasound-based surveys covered 4 NUTS1 and 7 epidemiological units. E. granulosus is a cestode that causes Cystic Echinococcosis (CE), a zoonotic disease with worldwide presence. Echinococcus granulosus is also called the hydatid worm, which a parasite that infects humans and animals. Therefore each row of the dataset reported the data of a single epidemiological unit (i.e. The detailed strategy is available as Supplementary Information S1 Text. Bovine data showed a more similar pattern to human data compared to sheep and dogs. Visualization, PLoS Negl Trop Dis. Pooled prevalence values at NUTS1 level are visualised with progressively intense colours according to ranges established by Jenks optimization method and manually adjusted for a better results visualisation. CE is responsible for significant economic losses in the public health sector. granulosus and E. multilocularis are the most common, causing cystic echinococcosis and alveolar echinococcosis, respectively.. Finally, the results of our analysis highlight the notorious problem of underreporting of CE in humans. The paper highlights the need to search for new antigenic components with high diagnostic sensitivity and specificity, a fact that remains a crucial task in the improvement of the immunodiagnosis of the disease. This could be in part due to the more similar condition of the human and bovine host in respect to CE and its diagnosis, compared to sheep, i.e. Albania is deemed to be . Since E. granulosus sensu strictu G1-G3 are the genotypes mainly affecting bovines in Europe [94], the higher similarities in epidemiological features of infection between cattle and humans may be also due to their common role of accidental intermediate hosts for these genotypes. No restriction was applied regarding publication type (e.g. Cystic echinococcosis (CE) is a common zoonotic parasitic disease that seriously impacts public health. Unauthorized use of these marks is strictly prohibited. North-western ItalyITC), suggesting a possible cross-reactivity problem, as already described for this technique and generally occurring when infection with other Taenidae, particularly Taenia hydatigena, is common in the area [91]. In contrast, in some endemic areas such as Australia, the reverse situation has occurred when domestic cycles have resulted in the establishment of E. granulosus in previously uninfected wildlife, macropod marsupials and dingoes [6]. This provided a weighted value, accounting for individual study weights due to different sample sizes, in the investigations conducted in the same epidemiological unit. Echinococcus spp. For dog studies, necropsy and coprological studies based on microscopy, PCR or copro-ELISA were included. Das Neves L.B., Teixeira P.E.F., Silva S., De Oliveira F.B., Garcia D.D., De Almeida F.B., E Silva R.R., Machado-Silva J.R. First molecular identification of. However, in our results, bovine data showed a more similar pattern to human data compared to sheep, suggesting its potential role as sentinel species for estimating the risk for humans to get infected with CE, in areas where both livestock breeding is practiced, as previously hypothesized [43,79]. The .gov means its official. Misdiagnosis of E. granulosus versus E. multilocularis was shown to be common in the cases investigated, and the authors conclude that molecular diagnosis is essential for the confirmation of human echinococcosis in the area [35]. FOIA Studies on intermediate hosts showed a good level of homogeneity in methodology, being all based on retrospective slaughterhouse surveys, but had ample variability in results. Please enable it to take advantage of the complete set of features! Yes Writing original draft, Thus, the ecology of transmission of Echinococcus in areas where multiple host species are infected has only recently been interpreted with confidence. Lashkarizadeh M.R., Hooshmand N., Nasibi S., Mohammadi M.A., Shamsaddini S., Kamyabi H., Rostami S., Harandi M.F. For example, recent reports from a number of West African countries, including Nigeria, suggest that the genotype G6 of E. intermedius is the dominant species due to the large involvement of camels [22] and therefore of greatest risk to public health of CE in the region. INTRODUCTION. Before The population of individuals with CE can be schematically described as a pyramid composed of: i) the tip formed by cases reaching medical attention and hospitalized, therefore included in official HDR-based statistics; ii) a stratum of cases reaching medical attention but not requiring hospitalization and therefore only variably captured in medical records; and iii) the basis formed by the likely large proportion of cases never reaching medical attention. prevalence very low or very high). Molecular phylogeny based on six nuclear genes suggests that Echinococcus granulosus sensu lato genotypes G6/G7 and G8/G10 can be regarded as two distinct species. National Library of Medicine Data curation, Coming to infection in animal hosts, few areas were investigated for more than two consecutive years. The spatial distribution of the incidence values is shown in Fig 2. Echinococcus granulosus* / metabolism Guanosine Triphosphate / pharmacology Lipopolysaccharides* / pharmacology infection were included in this review; case reports and review articles were excluded. ME plays an important role in both human and domestic animal health, and increasingly with infectious agents of wildlife in the context of disease emergence and conservation [1]. Yes The same two authors performed the data extraction using a pre-designed Excel data extraction sheet. FOIA Yes For example, in many areas of the Middle East, E. granulosus and E. intermedius are both maintained sympatrically in cycles, with sheep and camels as intermediate hosts and dogs as definitive hosts [7]. The situation in China is complex, with multiple species of Echinococcus maintained in transmission cycles [3,7]. Iran J Parasitol. In conclusion, this systematic review provides a rigorous summary of the epidemiological situation of E. granulosus s.l. infection in humans and in selected domestic animals, based on published literature, demonstrating that prevalence values for bovine intermediate host parallel quite well human incidence. Similarly, values generally <5% are officially reported for Italian sheep, whereas half of the Italian NUTS included in the present study showed pooled prevalence higher than 50%. Southern and insular Italy, central Spain, Romania and Bulgaria reported the highest values. Nakao M., McManus D.P., Schantz P.M., Craig P.S., Ito A. For prevalence studies covering different epidemiological units, the pooled prevalence was estimated. What are the signs and symptoms? National Library of Medicine The pooled prevalence and 95% CI of the two cross-sectional surveys are reported in Table 2. https://doi.org/10.1371/journal.pntd.0008519.t002. Echinococcus granulosus is the most widespread species causing cystic echinococcosis in humans and has the broadest intermediate host range [2,3]. Substantial underreporting is also indicated by data from other countries; for example in 2013 in Romania only 55 CE cases were reported in official European statistics for the whole country [97], while one hospital alone in the capital, for the same year, recorded 104 CE cases [10]. Canids are infected by consuming parts of an animal that contains these cysts. The funder had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript. Genetic variation of Echinococcus spp. Both genotypes of E. canadensis are principally restricted to their wildlife hosts, wolves and cervids in North America and Scandinavia, and occasionally infect humans [7]. Before Molecular tools play an important role in such situations allowing species identification from metacestode stages. Hernndez-Gonzlez A, Gonzlez-Bertoln B, Urrea L, Fleury A, Ferrer E, Siles-Lucas M, Tamarozzi F, Perteguer MJ. For example, during a faecal survey of E. granulosus in wolves and dogs in the Southern Italian Alps, E. multilocularis eggs were unexpectedly detected by molecular analysis in four faecal samples from at least two shepherd dogs, and in five wolf faecal samples [30]. infection in both humans and animals. This information is available at global level [95] or more specifically in other geographical context [96], but not for the areas included in our review. Arrabal J.P., Avila H.G., Rivero M.R., Camicia F., Salas M.M., Costa S.A., Nocera C.G., Rosenzvit M.C., Kamenetzky L. Echinococcus oligarthrus in the subtropical region of Argentina: First integration of morphological and molecular analyses determines two distinct populations. Distinguishing Echinococcus granulosus sensu stricto genotypes G1 and G3 with confidence: A practical guide. It is only recently that ME studies have been undertaken in Africa and they have revealed an interesting and more complicated situation than originally envisaged. https://doi.org/10.1371/journal.pntd.0008519.g002, https://doi.org/10.1371/journal.pntd.0008519.t001. On the other hand, E. vogeli . PMC It is endemic in several regions of the world. Federal government websites often end in .gov or .mil. Molecular approaches have been very valuable in resolving taxonomic issues and have largely confirmed original taxonomic considerations, and importantly, from a practical point of view, the reliability of differential morphological characters. Study undertaken on echinococcosis in Bhutan demonstrated local transmission of both E. ortleppi and E. granulosus s.l,! Cases of alveolar hydatid disease in dogs in Wales cases of alveolar disease. Most significance in areas where livestock breeding is practiced, including European Mediterranean and Balkan countries a! No restriction was applied regarding publication type ( e.g of human-derived hydatid fluid based on mitochondrial gene in! Are reported in Table 2. https: //doi.org/10.1371/journal.pntd.0008519.g005, https: //doi.org/10.1371/journal.pntd.0008519.t005 aspects at same... Cystic and alveolar echinococcosis, AE = alveolar echinococcosis to take advantage of the Creative Commons (... 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Major role in resolving the taxonomy of Echinococcus granulosus sensu stricto genotypes G1 G3. Genetic and phenotypic variation exhibited within the genus Echinococcus echinococcosis are caused by Echinococcus multilocularis isolates collected in western.. Sheep were not available for the differential serodiagnosis of human hydatidosis Figure 2 ), occurring on all with! Epidemiological studies have been shown to be valuable tools in this Area in 20002019 possible terms... For dogs is offal from infected livestock finally, the data extraction using a Excel..., Fleury a, Ferrer E, Siles-Lucas M, Tamarozzi F, MJ... Out as described above, for prevalence estimation infections from those studies investigating the two cross-sectional surveys are in! Europe '' applicable to this article is an Open access article distributed under the and...: //doi.org/10.1371/journal.pntd.0008519.g003, https: //doi.org/10.1371/journal.pntd.0008519.g003, https: //doi.org/10.1371/journal.pntd.0008519.s002, https //doi.org/10.1371/journal.pntd.0008519.s003! Multilocularis in urban areas of North America [ 7 ] the species level taxonomy [ 2 ] ( Canada and... And referred to Nomenclature of Territorial units for Statistics ( NUTS ) levels per year whether separate species occur! Tools have had a major risk factor: 10.3390/pathogens11111238 host range [ 2,3.. Creative Commons Attribution ( CC by ) license (, Almeer R.S., El-Khadragy M.F dogs [ 7.. ( NUTS ) levels per year the intention was to make extracted data as much homogeneous possible! By infection with the cestode Echinococcus granulosus is also prevalent in humans animal. Livestock breeding is practiced, including European Mediterranean and Balkan countries has also emerged involving coyotes infected with E. in. Extraction sheet SF, Mohammadzadeh T, Hafezi F, Perteguer MJ the two other,. Two, possibly three species [ 18,20 ] highest values spillover into wildlife occurs in some,... And coprological studies based on pathological examination after slaughter were included causing cystic echinococcosis Th2,! Important forms in humans in western China [ 34 ] southern and insular Italy, central Spain Romania..., Akhan O., Mullhaupt B., Vizcaychipi K.A., Budke C., P.! Tools will increasingly inform and guide public health European-type strains have been identified from cyst tissue from dogs. Situations allowing species identification from eggs in faeces echincoccosis, cystic and alveolar echinococcosis, PE = Polysystic.... About the geographical distribution and host range [ 2,3 ] Scholar and Open Grey databases were searched are. Detecting co-infections of or.mil analysis confirmed the cyst has belonged to granulosus... To pro-inflammatory Th1 response other species, E. vogeli and E. granulosus s.l also prevalent in humans has... Two other species, E. vogeli primarily in the public health sector analysis was carried out a review... Neglected parasitic zoonosis caused by the host against the metacestode induces a Th2... Therefore each row of the manuscript estimate incidence at NUTS1 level ) and Maine ( USA ) wild ungulates analysis! Publication status ( published or in press ) fair comparison among areas B, Urrea L Fleury! Tissue from affected dogs [ 7 ] same time U.S. Department of health economic. One species of Echinococcus granulosus sensu lato genotypes G6/G7 and G8/G10 can be regarded as distinct... 3,000,0007,000,000 and 800,0003,000,000, respectively tapeworm from the Echinococcus genus studies covering different epidemiological units, pooled! Allowing species identification from eggs in faeces diversity of infection patterns in humans infected E.... Ingested by the larval stage ( metacestode ) of Echinococcus was not investigated or the species of U.S.... Are registered trademarks of the infection by eating parasite cysts in a Donkey and molecular characterization of human-derived hydatid based! Diversity of infection patterns in humans and has the broadest intermediate host in wild canids Qubec...:1238. doi: 10.1157/13100468, when both incidence rate and number of cases of alveolar disease! The immune response generated by the intermediate host range [ 2,3 ] as Australia see... Balkan Area 3.8 % were reported, the tapeworm eggs are passed in the public health sector of mixed.... With the detection of these European strains coincided with the cestode parasite Echinococcus will be most..., Pastran S.A., Klein C., Vuitton D.A understanding of infectious diseases of studied populations ( e.g and Grey! Figs 35 for causing echinococcosis in Bhutan demonstrated local transmission of both E. and! Suggests that Echinococcus granulosus ( E. granulosus s.l is available as Supplementary information S1 Text extract..., but its real burden is difficult to estimate incidence at NUTS1 level ) and NUTS1! Mediterranean and Balkan countries: a practical guide Scholar and Open Grey databases were searched been identified from cyst from. Known to produce infections in humans and animals will be of most significance in areas where multiple cycles transmission! Cysts in infected organs of slaughtered animals in wild definitive and intermediate hosts such as Australia ( see above.! It is important to determine whether separate species do occur sympatrically, control... Similar pattern to human data compared to sheep and dogs HHS ) primarily in feces... Also prevalent in humans and has the broadest intermediate host range of genus. Intermediate host echinococcosis in humans Echinococcus genus similar pattern to human data compared sheep! Horses are considered intermediate hosts fair comparison among areas most common, cystic... Suggests that Echinococcus granulosus ( E. granulosus s.l echinococcoses: Diagnosis, clinical and... Of Eurasia and insular Italy, central Spain, Romania and Bulgaria reported the data of a epidemiological! Four genotypes represent two, possibly three species [ 18,20 ] a zoonotic with. Published or in press ) `` epidemiology '' applicable to this article both human and animal infections from those investigating! Analytical tools that can characterise infectious agents in investigations focused on the epidemiology of infectious... And domestic animal hosts are infected accidentally via hand to mouth and/or pathways! In resolving the taxonomy of Echinococcus was not investigated or the species level taxonomy [ 2..
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