Open Access
Research Article
Issue
Parasite
Volume 27, 2020
Article Number 41
Number of page(s) 41
DOI https://doi.org/10.1051/parasite/2020024
Published online 03 June 2020

© D.A. Vuitton et al., published by EDP Sciences, 2020

Licence Creative Commons
This is an Open Access article distributed under the terms of the Creative Commons Attribution License (https://creativecommons.org/licenses/by/4.0), which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.

Introduction

Echinococcus species (spp.) are parasites of the class Cestoda and belong to the phylum Platyhelminthes; they cause a variety of diseases in humans, most importantly cystic echinococcosis (CE; also found in scientific publications and professional/public communications under “hydatid cyst”, or “hydatid disease”, “hydatidosis”, “echinococcus cysticus”, etc.), alveolar echinococcosis (AE; also found under “alveococcosis”, “echinococcus alveolaris”, “alveolar hydatid”, “alveolar hydatidosis”, “alveolar hydatid disease”, “multilocular hydatid cyst”, “multilocular hydatid disease”, “multilocular hydatidosis”, etc.), and neotropical echinococcosis (NE; also found under “polycystic echinococcosis”, “polycystic hydatid disease”, “hydatidosis of the New World”, etc.) [35]. The simple enumeration of the various alternative names of the diseases, still in use in 2020, readily shows the absence of standardization of the terminology used in this field. Echinococcoses are zoonoses, and the complexity of the life cycle of the various species of Echinococcus involved, the variety of their hosts, as well as the impact of the diseases due to Echinococcus spp. on public health, require the involvement of specialists from nearly all disciplines (medicine and surgery, veterinary medicine, zoology, parasitology, ecology, agriculture, public health, economics, etc.) which have their own history and their own jargon. However, they must cooperate to solve the multiple problems of Echinococcus spp. infection, within the “One-Health” concept. This makes the use of a common vocabulary crucial. Time has thus come for standardization of the terminology in the field of echinococcosis.

From Hippocrates, who first described the cysts in patients more than 2400 years ago [18], to the 20th century, languages of Greek and Latin origin have served to name the parasites/diseases associated with Echinococcus spp. because in the Western world, countries around the Mediterranean were the known endemic regions for CE, the only recognized Echinococcus-related disease [13]. In the 19th century, physicians and researchers of German and Russian languages and in the 20th century, of French and English languages [18] brought new terms, and AE, then NE, were added to the list of Echinococcus-related diseases. At the end of the 20th century, China was recognized the main endemic region for CE and AE. Meanwhile, publishing in English became more and more common for physicians and scientists working in the field of echinococcosis worldwide, and everyone had to work with the variety of words and expressions describing Echinococcus spp. and echinococcosis in international publications in English [77]. Differences in wording, in the various professional environments, as well as in the various endemic countries, have become sources of misunderstanding, with influences related to the local language of the professionals.

The first decade of the 21st century, with the development of molecular biology techniques and the complete elucidation of the genomes of E. granulosus (Batsch, 1786) [87] and E. multilocularis (Leuckart, 1863) [73], has seen the emergence of new species within the genus Echinococcus, that have increased and refined our taxonomic knowledge of these parasites; such developments have also had an impact on several domains of echinococcosis research including not only genomics, proteomics and metabolomics, but also immunology and epidemiology [81, 86]. There has been and still is coexistence of already defined species based on genetic sequences with “types”, and “strains”, based on morphological characteristics [55]. A better definition of the limits of the species has led to an agreement between specialists on the definition and names of the “new” species, and nine species are now recognized and characterized by the sequences of their genomes, and defined in terms of host species and endemic areas [81]. The application of binomial nomenclature for genera and species is now governed by various internationally agreed codes of rules, of which the “International Code of Zoological Nomenclature (ICZN)” governs the scientific designation of parasites (https://www.iczn.org/the-code/the-international-code-of-zoological-nomenclature/the-code-online/). This international system must be followed, and any new species designation has to be registered for its international use. However, the translation of the “new” Echinococcus species defined by specialists into common usage by professionals has not yet been achieved, and many publications still use “E. granulosus” as a single species name responsible for CE.

The situation is also problematic for disease names and all other terms and expressions. This may be due to the status of echinococcoses as “orphan” diseases or “neglected diseases” (e.g., for the World Health Organization they are now recognized as “Neglected Tropical Diseases” (https://www.who.int/neglected_diseases/diseases/en/), even though most human cases and animal infections are not in tropical areas). For “non-neglected” diseases, authoritative international scientific societies have fixed the terminology and published recommendations that are regularly updated. The World Federation of Parasitologists has endorsed the Standardised Nomenclature of Parasitic Diseases (SNOPAD), initially published in 1988 for animal parasitic diseases by the World Association for the Advancement of Veterinary Parasitology, and has established rules for the names of parasitic diseases [32] (cf. https://www.waavp.org/documents/snopad-guidelines/#.XS9gBvIza00). The disease names are derived from the genus of the parasite with a suffix in “-osis” (e.g., Echinococcus would give “echinococcosis”). The rule is simple and clear; but the application of this rule has not been consistently followed and, especially for echinococcosis, coexistence of various names prevails, with a subsequent impact on database searching and misunderstanding between researchers and professionals [33, 34]. Other terms used in the “echinococcosis field” are equally ill-defined.

The “Asociación Internacional de Hidatidología” was founded in 1941 in Colonia del Sacramento (Uruguay), during the first “International South American Conference to Fight against Hydatidosis”, aiming at coordinating echinococcosis control, especially in the endemic countries of South America, and organizing conferences. From 1951 to the end of the 1990s, Spanish, French and English were the official languages of the biennial “World Congress of Hydatidology”, the main activity of the “International Association of Hydatidology” (IAE). At the 26th congress in Bucharest, Romania, in 2015, the name of the association in English was officially changed to “World Association of Echinococcosis (WAE)”, a formal step towards the adoption of “echinococcosis” for the denomination of the diseases (and of the field of research in general). In 1985, the WHO Informal Working Group on Echinococcosis (IWGE) was created, with the double aim of creating a network of scientists working in basic sciences in the realm of echinococcosis, and in standardizing practices for the diagnosis and treatment of Echinococcus spp. – related diseases, in line with the priorities of the WHO [18].The group is currently working on a Technical Manual to help clinicians in the care management of patients with echinococcosis. Both professional entities (IAE and IWGE) hold their main meeting at the same location and have always joined efforts to issue manuals on echinococcosis including veterinary aspects, prevention and control [1517], or write and update guidelines for diagnosis and treatment of patients with echinococcosis [10, 83]. In a plenary session of the 27th World Congress of Echinococcosis (WCE) in Algiers, Algeria, 2017, the need for harmonizing the terminology of echinococcosis, on sound scientific and linguistic grounds, was stressed; a working group and a consensus process were established to provide recommendations applicable to scientific publications in English, and to the communication between professionals. Such recommendations should then be used as a basis for translation into other languages spoken in endemic countries for communication, teaching and training. This report and its and its illustrations (Tables and Figures) and Appendix are the ultimate result of the process.

Materials and methods

The methodology proposed to the participants in the working groups established at the 27th WCE was the “Formal consensus” approach, as used by the French “Haute Autorité de Santé” (https://www.has-sante.fr/upload/docs/application/pdf/2018-03/good_practice_guidelines_fc_method.pdf), inspired by both the Delphi process [30] and the Consensus Conference methods [19]. As the methodology was initially described to set up guidelines for good clinical practices, the method was slightly modified, as described below, to fit with the objectives of the present work, i.e. an agreement on terminology and good publishing practices. All participants in the various groups involved in the “formal consensus” process are cited as “associated authors” in the final publication (names in Appendix).

Definition and modalities of constitution of the Working Groups

Steering and Writing Group (SWG)

The mission of the SWG was: (1) to draft the list of words and expressions, and provide a critical analysis of their scientific and linguistic relevance, from the international scientific literature and all available sources (international nomenclature, international recommendations, historical notes, etymology), and submit it to the participants in the Consultation and Rating Group (CRG); (2) to collect and discuss the feedback from the participants in the CRG, and if necessary to submit difficult cases to appropriate external experts; (3) to draft the final lists of words and expressions and submit them to rating by the participants in the CRG; (4) to select 12 experts in the various disciplines of interest to the field of echinococcosis, not involved in the CRG, as members of the Reading and Review Group (RRG); (5) to analyze the rating data and draft the initial version of the Recommendation Paper, including the final tables with recommended terminology, to be submitted to the RRG; (6) to consider the remarks of the RRG on the draft, finalize the paper and the tables with the members of the CRG, and submit it to the appropriate journal; and (7) to ensure the follow-up of the paper and the dissemination of its content to end-users.

The composition of the SWG, chaired by a project manager, was approved by the president and the members of the WAE attending the 27th WCE, and three topics of interest were proposed, each coordinated by two members of the SWG, experts in the area.

Consultation and Rating group (CRG)

The mission of the CRG in the “formal consensus” process was (1) in the first step of consultation, to provide input on the initial list of terms and expressions drafted by the SWG, taking into account the available literature in all fields and the personal experience of the various participants; (2) in the second step of consultation, to participate in the poll, and provide independent rating on all words and expressions submitted to vote by the SWG; and (3) to finalize the text of the paper with the SWG after its evaluation by the RRG, and before its submission to the appropriate journal.

Sub-groups, corresponding to the three topics of interest were composed on a voluntary basis at the 27th WCE, and completed after a call for volunteering launched by email by the SWG after the congress. On their request, participants could belong to more than one subgroup. The list of the CRG participants who were involved in the whole process, and their country/countries of residence and field work, is provided in the Appendix. For the “Species and epidemiology”, “Biology and immunology” and “Clinical aspects” subgroups of the CRG, 17, 18, and 14 participants were identified, respectively from 15 countries in total. The project manager coordinated all activities of the groups but was not involved in any rating; however, other members of the SWG who volunteered for the task could be involved in rating but only for those subgroups they were not coordinating.

Reading and Review Group (RRG)

The mission of the RRG, multidisciplinary and multi-professional, was to give a formal opinion on the content and form of the initial version of the paper and the recommendations it may contain, especially in terms of applicability, acceptability, and readability in their own domain. According to the rules of the “formal consensus” process, the participants in the RRG would offer an advisory opinion on an individual basis, without de novo questioning the decisions from the votes obtained in the first 2 steps of the process. The list of the RRG participants (four experts for each topic) who were involved in the reviewing process, and their country/countries of residence and field of expertise, is given in the Appendix.

Schedule of the process

The time schedule of the process, from October 2017 to February 2020, is given in Figure 1. The main steps included: (1) constitution of the SWG, presentation of the project, and constitution of the CRG; (2) provision of a list of words and expressions, with arguments for their acceptance or rejection, provided by the SWG to the participants in the CRG; (3) input from the participants in the CRG and open discussion; (4) constitution of the RRG by the SWG; (5) a preliminary summary by the SWG, and preparation of three lists of words and expressions for each of the three topics, according to three levels of decision: (a) a priori approved terms, (b) a priori rejected terms, (c) debated issues submitted to vote; (6) vote on “debated issues” by the participants in the CRG; (7) analysis of data and drafting of the Recommendation Paper by the SWG; (8) reviewing of the draft by the RRG; (9) last review by the CRG; (10) submission of the manuscript by the SWG; and (11) follow-up of the publication process and dissemination of the recommendations by the SWG.

thumbnail Figure 1

Time schedule and main activities within the “Formal consensus” process for the definition of the terminology of echinococcosis.

Except for the first kick-off meeting at the 27th WCE and the final presentation at the 28th WCE in Lima, Peru, and given the worldwide extent of the consultation group and absence of funding, there were no further face-to-face meetings; all discussions and exchanges were managed by email. The project manager and members of the SWG answered all messages sent by the members of the CRG and all contributions were taken into account at any stage.

Analysis of the poll

Medians and means of the ratings, on a possible agreement range from 1 to 10, were calculated for the answers to each question. A majority of agreement for approval or rejection was considered when more than half of the ratings were equal to or higher than 5, or equal to or lower than 5, respectively. Unanimous approval or rejection was defined as ratings higher than or lower than 5 for all voters, respectively. Agreement for rejection was defined for a median equal to 3.5 or lower, and majority or unanimity of ratings; agreement for approval was defined for a median equal to 7.5 and higher; and majority or unanimity of ratings. A question was deemed “undecided” when the median was between 3.5 and 7.5 and/or there was no majority of ratings. After the poll and when needed, i.e. whenever the result of the votes was “undecided” and/or whenever there was no full agreement on the definition of a term, the SWG submitted the term/expression to further discussion between specialists in order to reach final agreement. To this purpose, subgroups of specialists (e.g., surgeons) were constituted to propose final agreement.

Results

Final composition of the CRG subgroups

For the “Species and epidemiology” subgroup, 1 participant could not be reached by email and 1 never answered emails; the final rating was thus provided independently by 15 participants, from 10 countries. For the “Biology and immunology” subgroup, three participants could not be reached; five participants from the same research team worked together for the final rating; thus the final rating was provided independently by 11/15 participants from 11 countries. For the “Clinical aspects” subgroup, one participant could not be reached and one did not answer emails; 2 participants from the same research group worked together for the final rating; thus the final rating was provided by 11/12 participants from 8 countries.

Results of the first stage of consultation

The first stage of consultation generated numerous comments with associated arguments and references from all participants in the CRG. This input was carefully collated in a summary version of the preliminary tables by the SWG. In case of need, other experts of the specific field were consulted by the coordinators of the subgroups, and their opinion was brought to the attention of the CRG participants. The synthetic tables as well as additional pictures if necessary (especially for the subgroup on “Biology and immunology”), were again sent to all participants to obtain initial evaluation of possible consensus, and set up a list of still “debated issues”.

For the “Species and epidemiology” subgroup, it was agreed that the nomenclature of old and new species of Echinococcus should follow the rules of the ICZN. Thus, the names of the species (and their number) listed in the tables reflect the results of current taxonomic research and do not preclude future changes, provided these are based on convincing new evidence. There was also a consensus on the use of the “G” genotypes in cases where genetic differences are apparent, but where – based on current knowledge – these differences are deemed too small to warrant recognition of the variants as named taxa. In addition, the term “genotype” should be reserved for characterization using molecular biology/sequencing, and “strain” or “type” should be reserved for characterization using morphological and host-range characteristics. Consequently, there were no “debated issues” for this subgroup. However, definitions and clarifications on species names and on other words and expressions regarding this topic were given in provisional tables; they were submitted for approval or rejection in the second stage of the process (with an answer of the “YES/NO” type).

For the “Biology and immunology” subgroup, there was far more debate since there is no official institution in charge of such terminology. Divergences appeared about the various stages of development of the Echinococcus spp. in their intermediate hosts, and particularly on the definition of the term metacestode. Other minor divergences were noted on the use of certain words to designate the cells and components of these parasites, either adult or larval, as well as the host’s reaction. References were provided by parasitology and immunology specialists to support data interpretation, thus the use of specific words. From that stage of the consultation, there was general agreement that the adjective “hydatid” should only be used for E. granulosus sensu lato; as this was a sensitive issue, it was however kept in the “debated issues” submitted to vote, both for the “Biology and immunology” and for the “Clinical aspects” subgroups. For details on the names of the various components of the egg of all Echinococcus spp. and of the cyst in CE, it was decided to provide a figure that would fix the definitions of the various words (Figs. 2A, 2B and 2C). The definition of “cyst” was initially the main disagreement between “parasitologists” (2-layer cyst) and “clinicians” (3-layer cyst). At the end of the first stage, it was finally agreed by all experts, whatever their field of expertise, that all cysts due to Echinococcus spp. and, especially for clinicians, those due to E. granulosus s.l., included two “layers” (and not “membranes”) of parasite origin and one layer of host origin, thus three layers. This clarification helped when defining several derived terms.

thumbnail Figure 2A and B

General description of the egg and oncosphere of Echinococcus spp, according to Jabbar et al., 2010 [27]. (A) Schematic diagram of an oncosphere illustrating the structure and bilateral symmetry in the pattern of hooks and cellular organization of the hexacanth embryo. VL: vitelline layer; EM: embryophore; GL: granular layer; OM: oncospheral membrane; Hex: hexacanth embryo. (B) Cellular organization of the oncosphere. Oncospheres are approximately 25 × 30 μm.

thumbnail Figure 2C

General description of the metacestode of Echinococcus spp. (see also Table 1B and Fig. 3).

For the “Clinical aspects” subgroup, it was readily agreed that the names of diseases due to the various species of Echinococcus should follow the rules proposed by the SNOPAD and the generic name “echinococcosis” should always be used, irrespective of the species and type of disease. “Cystic” and “Alveolar” should be used as adjectives to designate the diseases due to E. granulosus (Batsch, 1786) sensu lato, and to E. multilocularis (Leuckart, 1963), respectively. Some discussion remained for the use of the adjective “hydatid”, and for the names of the diseases due to E. oligarthra (Diesing, 1863) and E. vogeli Rausch and Bernstein, 1972, in South America. Most of the debated issues concerned the names of therapeutic interventions (surgical or using other techniques); however, the common definition of “cyst”, shared by parasitologists and clinicians, led to an easier consensus on the meaning of “cystectomy”.

Results of the second stage of consultation

Agreement for approval or rejection

A few terms proposed in the lists for “approval” or “rejection” at the end of the first stage of the process still received objections from participants in the CRG. More precision (or references) were provided in order to reach a final consensus on these terms and their definition. Approved terms were provisionally included in Tables 1A (Genetics and epidemiology), 1B (Biology and immunology) and 1C (Clinical aspects). Rejected terms were provisionally included in Tables 2A (Genetics and epidemiology), 2B (Biology and immunology) and 2C (Clinical aspects).

Table 1A

Recommended terms for the genetics and epidemiology of Echinococcus species.

Table 1B

Recommended terms for the biology and immunology of Echinococcus species.

Table 1C

Recommended terms for the clinical aspects of echinococcosis.

Table 2A

Rejected terms for the genetics and epidemiology of Echinococcus species.

Table 2B

Rejected terms for the biology and immunology of Echinococcus species.

Table 2C

Rejected terms for the clinical aspects of echinococcosis.

Poll on debated issues

Among the 39 final participations in the poll about “debated issues” nine were incomplete; the questionnaire was sent back to these participants for completion; precise answers were eventually obtained. The ratings provided for the poll on “debated issues” were analyzed in order to obtain means and medians, and thus a final score for approval or rejection of each term. Results of the median rating for the “debated terms”, and whenever useful the agreement between participants, are given in the “Comments” column of Tables 1A1C and 2A2C. Objections and concerns on the use of some terms were re-discussed by specialists before making a final decision on their final rejection or approval, and minor modifications in the wording of definitions were made in order to obtain a final consensus. An important result of the poll, since it was distinctly and clearly agreed upon both by the participants in the “Biology and immunology” subgroup and those in the “Clinical aspects” subgroup, was on the word “hydatid”. According to the polls, all names of diseases or operations composed from the radical “hydatid” (e.g., in “hydatid-osis” or “hydatid-ectomy”, etc.) should be abandoned, and the adjective “hydatid”, whenever used, should never be used to qualify entities different from those due to E. granulosus sensu lato, thus never be used for E. multilocularis, E. vogeli and E. oligarthra. A final discussion on the characterization of the surgical procedures aimed at removing CE cysts eventually retained a simple framework that should be used whenever surgical operations are described in publications, with four levels of mandatory qualification, regarding (1) Approach: “laparotomy”, “laparoscopy” or “robotic”; (2) Cyst Opening: “non-opened cyst” (NOP) versus “opened-cyst” (OP); (3) Resection type: “cystectomy”, “hepatectomy”, or “liver transplantation”; and (4) Completeness of resection: “total”, “subtotal”, and “partial”. Description of the AORC unified framework for surgical interventions in CE is given in Figures 3A and 3B. Precise description of the procedure actually performed should complete the mandatory terms (description of the removed parasite layers, area in square centimetres or percentage of cyst actually resected, closure of communications with bile ducts, etc.).

thumbnail Figure 3

“AORC” nomenclature framework for CE surgery. (A) (top) – Vocabulary and acronyms. AORC: acronym for Approach, Opening, Resection and Completeness; CE: cystic echinococcosis; OC: opened cyst; NOC: non-opened cyst. (B) (bottom) – A. Schematic structure of CE cyst: the CE cyst consists (from inside to outside) of the germinal layer, laminated layer and adventitial layer. B. Total cystectomy requires the resection of all three layers completely. C. Subtotal cystectomy requires the nearly total resection of all three layers; only parts of the adventitial layer are preserved because of surgical safety. D. Partial cystectomy refers to the incomplete resection of any of three layers (usually of the adventitial layer) due to technical and safety issue. E. Hepatectomy requires the en bloc resection of part of liver parenchyma, following the rules of hepatic resection.

Review by the RRG and meeting at the 28th WCE in Lima, Peru

Feedback from the RRG members usually addressed minor aspects of text readability and/or definitions/descriptions in the Tables. Clarification was provided by the reviewers on the definition of the species and their hosts, especially regarding species involved in NE. The major issues raised by one reviewer (clinician) concerned the definition of the “cyst”, and the retention of the adjective “hydatid”, even in its very restrictive sense as described in Tables 1B and 1C. However, because of the clear results of the consensus process, these objections could not be taken into account in the final version. At the meeting of the WHO-IWGE held in Lima, Peru, during the 28th WCE, the still debated issues were raised and final adjustments were made between the SWG and the writers of the WHO-IWGE Technical Manual on CE treatment. Words and expressions finally approved and rejected after the poll and the last discussions were added to the list of approved and rejected terms. Terms finally approved (95 items) are thus included in Tables 1A (Genetics and epidemiology), 1B (Biology and immunology) and 1C (Clinical aspects). Rejected terms (60 items) are included in Tables 2A, (Species and epidemiology), 2B (Biology and immunology) and 2C (Clinical aspects). To facilitate consultation, Tables 1A1C and 2A2C are organized by topics of interest (A, B and C), and within each topic, in alphabetic order of the words or expressions.

Discussion

This 2-year multidisciplinary and international exchange of views has allowed physicians, veterinarians and basic science researchers to freely discuss opinions about terms used in all fields relating to Echinococcus spp., and to reach a consensus on the use of the most appropriate ones, based on sound scientific and/or linguistic grounds. When evidence was not available, consensus was based on reasoned arguments, including usage when no suitable alternative was found, confirmed by a poll. This is the first and only endeavour of this type in the domain of echinococcosis; and it is endorsed by the WAE. Definitions of 155 terms and expressions and recommendations provided in Tables 1A1C and 2A2C and Figures 2A2C and 3 should be followed in the future by all scientists writing scientific papers in English; scientific editors and referees/reviewers should recommend article authors to use the approved terms. These recommendations should help the recognized experts, involved in scientific work on echinococcosis at the international level, to set up a similar list of recommended and rejected words in their country language(s), so that similar wording could be used by all professionals. Major advances promoted by the multidisciplinary work on echinococcosis terminology were: (1) the confirmation of the current recognition of nine species of Echinococcus; (2) an agreement on the names of the three types of diseases due to Echinococcus spp. and rejection of all others; (3) the restriction of the adjective “hydatid” to E. granulosus s.l.; and (4) the proposal of the “AORC” framework to describe surgical interventions in CE.

The participants involved in the work were representative of the “echinococcosis” scientific community. Half of the 61 participants in the three working groups belonged to the top 50 experts in the area (as cited from their publications retrieved with the key words “echinococcosis”: http://expertscape.com/ex/echinococcosis or “hepatic echinococcosis”: http://expertscape.com/ex/echinococcosis%2C+hepatic). Health professionals and young researchers were also involved in the CRG; there was a balanced proportion of researchers and professionals. The participants in the three groups were from 15 endemic countries, and all five continents were represented with a balance of male and female contributors to the debate. Recruitment of the participants in the CRG at the 27th WCE on a volunteer basis enabled researchers and professionals from the Maghreb and Middle East countries, highly endemic countries for CE, to participate in the CRG. Additional colleagues, especially from South America and China, were solicited after the congress. However, only Chinese colleagues answered positively, which resulted in a relatively low participation of South American colleagues in the “Clinical aspects” subgroup, perhaps because of language issues: Spanish and Portuguese are the publication languages of most South American clinicians; publications in English from South America are mostly in biology and public health. All members of the RRG were selected by the SWG on the basis of their international academic recognition in the fields of CE, AE and NE. Despite the absence of face-to-face meetings to discuss the undecided questions, open email discussions were initiated by the coordinators of the subgroups, and this procedure was very efficient. If there were missing values for the poll, the project manager actively and individually contacted the voters in question in order to ask them to provide their opinion. Feedback from the RRG members was also followed by active discussions in order to reach consensus on important terms and to revise and finalize this paper.

Major outcomes and conclusions

Currently, a precise genetic definition is available for nine species: E. granulosus (Batsch, 1786) sensu stricto, E. canadensis (Webster & Cameron, 1961), E. ortleppi Lopez-Neyra & Soler Planas, 1943, E. felidis Ortlepp, 1937, and E. equinus (Williams & Sweatman, 1963), within the E. granulosus (Batsch, 1786) sensu lato cluster and responsible for cystic echinococcosis, E. multilocularis (Leuckart, 1863), and E. shiquicus Xiao, Qiu, Nakao, Li, Yang, Chen, Schantz, Craig & Ito, 2005, responsible for alveolar echinococcosis, and E. vogeli Rausch and Bernstein, 1972 and E. oligarthra (Diesing, 1863), responsible for neotropical echinococcosis; the responsibility of some of the species (e.g., E. equinus (Williams and Sweatman, 1963) or E. shiquicus Xiao et al., 2005) in human infection is still being questioned; this does not challenge the genetic definition of these species (Table 1A). Recognition of additional species within E. canadensis and E. granulosus s.s. is to be expected (Table 1A). Thus, distinct Echinococcus spp. genotypes within the E. canadensis cluster may move to full species status, and the names E. intermedius (for G6/7), E. borealis (for G8) and E canadensis (for G10) have been proposed; however, no conclusion on the number and names of these species has yet been reached [57].

Variations around the radical “hydatid” have long been used to designate diseases due to Echinococcus spp. The presence of “hydatid” cysts had long been recognized as a feature of a parasitic disease when the natural cycle of the parasite responsible for its occurrence was identified in the middle of the 19th century [18, 77]; the species was first named Taenia echinococcus before becoming Echinococcus granulosus. In humans, the disease was clearly not a “taeniasis”, and “hydatid disease”, “hydatidosis” (if the disease was considered) or “hydatid cyst” (if the lesion was considered) thus prevailed. It took another century before the Echinococcus sp. which causes AE was identified as a distinct species, E. multilocularis [18, 77]. It is thus easy to understand why several terms, not related to the current name of the genus, were used for centuries, and why they were used to designate both diseases, alveolar and cystic echinococcosis. The inappropriate use of “hydatid” has been a source of confusion, both for disease surveillance and treatment indication [10, 35]. Until recently, echinococcosis surveillance by the European Centre for Disease Control (ECDC) did not distinguish between the two diseases [23]. A clear distinction between three types of diseases, with a single name for each of them, will make all studies on epidemiology, socio-economic burden, and care management more reliable. There was total agreement to never use terms based on the “hydatid” root to designate any disease due to Echinococcus spp., and to strictly restrict the use of “hydatid” to qualify a lesion or part of a lesion due to E. granulosus s.l. in intermediate hosts, entirely excluding its use to qualify anything regarding (1) E. granulosus s.l. infection of the definitive host, and (2) AE and NE. With regards to a cystic lesion, “CE cyst” should be preferred to “hydatid cyst” since the large majority of voters preferred to use this term, and did not wish to keep both names for E. granulosus s.l.-related cysts.

Although specialists of the genetics of Echinococcus spp. rapidly agreed on the correct spelling of the species E. oligarthra on historical and linguistic arguments (and not oligarthrus, as commonly spelled in the last few decades; see e.g., [5, 17]), clinicians were more hesitant on the names of the diseases that E. oligarthra and E. vogeli may cause in humans. There was no term/expression entirely satisfactory to designate both diseases. Because both are infections of the “tropical areas of the New World”, “neotropical” has been commonly used in the scientific literature and was presented at the WHO-Forum in 2015 to be included among the U50-U99 “Codes for research and alternative subclassifications” of the International Statistical Code of Diseases and Related Health Problems (https://apps.who.int/iris/bitstream/handle/10665/246208/9789241549165-V2-eng.pdf), as: U51X: “Infection due to Neotropical Echinococcosis”. The suggestion of South American specialists, which was confirmed by the poll, was thus to keep this denomination. To avoid the confusion with “polycystic liver and kidney disease”, a genetic disease, the adjective “polycystic” (of Greek origin) should definitively be replaced by “multicystic” (of Latin origin, but with exactly the same meaning) when multiple aggregated cysts are observed on imaging, regardless of the species; “multiple cyst-” characterizes the co-existence of several separated and independent cysts in the same organ or different organs.

It was agreed that the current international classifications already approved by the WHO-IWGE, i.e. the “CE” classification of CE cysts [82], and the PNM classification of AE lesions [37], would not be questioned, and that further work on the refinement of imaging classification of AE would not proceed until fixing of international recommendations. However, an unexpected and extremely useful outcome of the terminology discussions was the agreement on a new and internationally recognized system to describe surgical operations in CE, the “AORC” framework (Fig. 3), with consensus on the single word “cystectomy” to describe the removal of the CE cyst, thus excluding “pericystectomy” when it consists of the removal of the three layers of the cyst without “pericystic” liver. This recommendation will help professionals to share a common description that is relevant in terms of perioperative risks and the risk of CE recurrence after operation. A precise description of the procedure actually performed by the surgeon for a given patient should accompany the mandatory terms (description of the removed parasite layers, area in square centimeters or percentage of cyst actually resected, closure of communications with bile ducts, content of the cyst if it was opened, etc.); this is beyond the objectives of a work on terminology and will be further discussed in the “Technical Manual” for the diagnosis and treatment of CE, which is currently being prepared by the WHO-IWGE. For non-surgical CE interventions, the clear distinction between the PAIR (puncture, aspiration, injection, reaspiration, through a needle, without catheterization), S-CAT (standard catheterization), and Mo-CAT (modified catheterization) techniques provides accepted acronyms and will also help professionals to better understand the specific indications of each technique and the results of clinical trials.

The work in terminology aimed to cover all fields of echinococcosis; it was the first attempt at standardizing scientific and medical language in a specific area of parasitic disease – echinococcosis. However, it did not claim to solve all points of debate and/or to address everything definitively. The words and expressions reported in Tables 1A1C and 2A2C do not encompass all technical aspects; such details should be considered by subgroups of specialists. Regular updating will also be necessary, following future advances in scientific and medical knowledge. Apparently “easy-to-solve” dilemmas were in fact more difficult to resolve when several disciplines reported on their own usages. This was the case for the debate between “daughter cyst” and “daughter vesicle”. Purists will certainly regret that “daughter cyst” will stay in use, despite the paradoxical female gender, explained by the use of the feminine “vésicule” (vesicle) in the first descriptions in French. Although “daughter” is not justified in English, the alternative adjective “secondary” cannot replace it since it is widely used to designate new cysts developed in the peritoneum, pleura or meningeal space after cyst rupture and/or protoscolex spillage Although “cyst” was not fully justified either, because it has no fully developed adventitial layer, biologists readily agreed to keep the noun “vesicle” with restricted use for the in vitro situation. The results of the poll (Tables 1C and 2C) confirmed the problematic nature of the issue: “daughter cyst” was not preferred, “daughter vesicle” was not either, and the alternative expression “daughter hydatid” was unequivocally rejected; it was thus agreed to keep the “historical wording”, i.e. “daughter cyst”. We recommend the constitution of a permanent group on “terminology” common to the WAE and the WHO-IWGE so that such “unresolved” issues may be further discussed, and that the certainly numerous new terms used in the field in the future may be handled in a timely manner.

Appendix

List of the 9 participants in the Steering and Writing Group (SWG)

Project manager: Vuitton Dominique A.

Subgroup coordinators:

Species and epidemiology: McManus Donald P., Australia; Romig Thomas, Germany.

Biology and immunology: Rogan Michael R., UK; Gottstein Bruno, Switzerland.

Clinical aspects: Menezes da Silva Antonio*, Portugal; Wen Hao, PR China.

Data collection and writing assistants: Naidich Ariel, Argentina; Tuxun Tuerhongjiang, PR China.

*Representative of the World Association of Echinococcosis, as Past-President.

List of the 42 participants in the Consultation and Rating Group (CRG)

Subgroup “Species and epidemiology” (15 participants, listed in alphabetic order)

Avcioglu Amza, Turkey; Boufana Belgees, UK; Budke Christine, USA; Casulli Adriano, Italy; Güven Esin, Turkey; Hillenbrand Andreas, Germany; Jalousian Fateme, Iran; Jemli Mohamed Habib, Tunisia; Knapp Jenny, France; Laatamna Abdelkarim, Algeria; Lahmar Samia, Tunisia; Naidich Ariel, Argentina; Rogan Michael T., UK; Sadjjadi Seyed Mahmoud, Iran; Schmidberger Julian, Germany.

Subgroup “Biology and immunology” (15 participants, listed in alphabetic order)

Amri Manel*, Algeria; Bellanger Anne-Pauline, France; Benazzouz Sara*, Algeria; Brehm Klaus, Germany; Hillenbrand Andreas, Germany; Jalousian Fateme, Iran; Kachani Malika, USA/Morocco; *Labsi Moussa, Algeria; Masala Giovanna, Italy; Menezes da Silva Antonio, Portugal; Sadjjadi Seyed Mahmoud, Iran; Soufli Imene*, Algeria; Touil-Boukoffa Chafia*, Algeria; Wang Junhua, Switzerland/PR China; Zeyhle Eberhard, Kenya.

Subgroup “Clinical aspects” (12 participants, listed in alphabetic order)

Aji Tuerganaili, PR China; Akhan Okan, Turkey; Bresson-Hadni Solange, France; Dziri Chadli, Tunisia; *Gräter Tilmann, Germany; *Grüner Beate, Germany; Haïf Assia, Algeria; Hillenbrand Andreas, Germany; Koch Stéphane, France; Rogan Michael T., UK; Tamarozzi Francesca, Italy; Tuxun Tuerhongjiang, PR China.

* Rating from these participants, who worked together, was considered as only one rating.

List of the 12 participants in the Reading and Review Group (RRG)

Subgroup “Species and epidemiology” (4 participants, listed in alphabetic order):

Giraudoux Patrick, France; Torgerson Paul, Switzerland/Central Asia; Vizcaychipi Katherina, Argentina; Xiao Ning, PR China.

Subgroup “Biology and immunology” (4 participants, listed in alphabetic order):

Altintas Nazmiye, Turkey; Lin Renyong, PR China; Millon Laurence, France; Zhang Wenbao, PR China.

Subgroup “Clinical aspects” (4 participants, listed in alphabetic order):

Achour Karima, Algeria; Fan Haining, PR China; Junghanss Thomas, Germany; Mantion Georges A., France.

Names, affiliations and email addresses of Collaborators

Algeria

Achour Karima, Service de chirurgie thoracique, cardio-vasculaire et de transplantation rénale, Hôpital universitaire Mustapha, DZ-16000 Bab-El-Oued, Algeria; achour.karima@gmail.com

Amri Manel, Laboratoire de Biologie Cellulaire et Moléculaire, Faculté des Sciences Biologiques, Université des Sciences et Technologie Houari Boumediene, DZ-16111 Algiers, Algeria; manelamri@yahoo.fr

Benazzouz Sara, Laboratoire de Biologie Cellulaire et Moléculaire, Faculté des Sciences Biologiques, Université des Sciences et Technologie Houari Boumediene, DZ-16111 Algiers, Algeria; sara.and1@hotmail.fr

Haïf Assia, Service de Chirurgie Pédiatrique, Université Ferhat Abbas, DZ-19000 Setif, Algeria; haif_chu.setif@yahoo.fr

Laatamna Abdelkarim, Département de Parasitologie, Université Ziane Achour, DZ-B.P. 3117 Djelfa, Algeria; laatamnaabdelkarim@yahoo.com

Labsi Moussa, Laboratoire de Biologie Cellulaire et Moléculaire, Faculté des Sciences Biologiques, Université des Sciences et Technologie Houari Boumediene, DZ-16111 Algiers, Algeria; touilboukoffa@yahoo.fr

Soufli Imene, Laboratoire de Biologie Cellulaire et Moléculaire, Faculté des Sciences Biologiques, Université des Sciences et Technologie Houari Boumediene, DZ-16111 Algiers, Algeria; touilboukoffa@yahoo.fr

Touil Boukoffa Chafia, Laboratoire de Biologie Cellulaire et Moléculaire, Faculté des Sciences Biologiques, Université des Sciences et Technologie Houari Boumediene, DZ-16111 Algiers, Algeria; touilboukoffa@yahoo.fr

Argentina

Naidich Ariel, Departamento de Parasitología, Instituto Nacional de Enfermedades Infecciosas, ANLIS “Dr. Carlos G. Malbrán”, AR-CP 1281 - Buenos Aires, Argentina; anaidich@anlis.gob.ar

Vizcaychipi Katherina, Instituto Nacional de Medicina Tropical (INMeT) Pto. Iguazú Misiones, Ministerio de Salud de la Nación, AR- CP 1281 Buenos Aires, Argentina; kvizcaychipi@gmail.com

Australia

McManus Donald P., Molecular Parasitology Laboratory, Infectious Diseases Division, QIMR Berghofer Medical Research Institute, AU-4006 Herston-Brisbane, QLD, Australia; don.McManus@qimrberghofer.edu.au

China

Aji Tuerganaili, Department of Hepatic Surgery; WHO Collaborating Centre for Prevention and Care Management of Echinococcosis; 1st Affiliated Hospital of Xinjiang Medical University, CN-830011 Urumqi, China; dr.wenhao@163.com

Fan Haining, China; Department of Hepatic Surgery; 1st Affiliated Hospital of Qinghai University, CN-810001 Xining, China; fanhaining@medmail.com.cn

Lin Renyong, State Key Laboratory of Pathogenesis, Prevention and Treatment of High Incidence Diseases in Central Asia, CN-830011 Urumqi, China; renyong_lin@sina.com

Tuxun Tuerhongjiang, Department of Hepatic Surgery; WHO Collaborating Centre for Prevention and Care Management of Echinococcosis; 1st Affiliated Hospital of Xinjiang Medical University, CN-830011 Urumqi, China; turgunbay@163.com

Wen Hao, WHO Collaborating Centre for Prevention and Care Management of Echinococcosis & State Key Laboratory of Pathogenesis, Prevention and Treatment of High Incidence Diseases in Central Asia, CN-830011 Urumqi, China; dr.wenhao@163.com

Xiao Ning, National Institute of Parasitic Diseases, Chinese Centers for Disease Control, CN-200025 Shanghai, China; ningxiao116@126.com

Zhang Wenbao, WHO Collaborating Centre for Prevention and Care Management of Echinococcosis & State Key Laboratory of Pathogenesis, Prevention and Treatment of High Incidence Diseases in Central Asia, CN-830011 Urumqi, China; wenbaozhang2013@163.com

France

Bellanger Anne-Pauline, Laboratoire de Parasitologie et Mycologie; Centre National de Référence pour les Echinococcoses, Centre Hospitalier Régional Universitaire, FR-25030 Besançon, France; apbellanger@chu-besancon.fr

Bresson-Hadni Solange, Centre National de Référence pour les Echinococcoses, Centre Hospitalier Régional Universitaire, FR-25030 Besançon, France; solange.bresson.sbh@gmail.com

Giraudoux Patrick, UMR Chrono-environnement; Université Bourgogne Franche-Comté, FR-25030 Besançon, France; patrick.giraudoux@univ-fcomte.fr

Knapp Jenny, France; Laboratoire de Parasitologie; Centre National de Référence pour les Echinococcoses, Centre Hospitalier Régional Universitaire, FR-25030 Besançon, France

Koch Stéphane, Service de Gastroentérologie; Centre Hospitalier Régional Universitaire, FR-25030 Besançon, France; skoch@chu-besancon.fr

Mantion Georges, Université Bourgogne Franche-Comté, FR-25030 Besançon, France; gmantion@univ-fcomte.fr

Millon Laurence, Laboratoire de Parasitologie; Centre National de Référence pour les Echinococcoses, Centre Hospitalier Régional Universitaire, FR-25030 Besançon, France; lmillon@univ-fcomte.fr

Vuitton Dominique Angèle, EA 3181, Université Bourgogne Franche-Comté, FR-25030 Besançon, France; dvuitton@univ-fcomte.fr

Germany

Brehm Klaus, Institut für Hygiene und Mikrobiologie Universität Würzburg, DE-97080 Würzburg; Germany; kbrehm@hygiene.uni-wuerzburg.de

Gräter Tilmann, Klinik für Diagnostische und Interventionelle Radiologie Universitätsklinikum Ulm, DE-89081 Ulm; Germany; tilmann.graeter@uniklinik-ulm.de

Grüner Beate, Comprehensive Infectious Diseases Center; Klinik für Innere Medizin III, Universitätsklinikum Ulm, DE-89081 Ulm, Germany; beate.gruener@uniklinik-ulm.de

Hillenbrand Andreas, Klinik für Allgemein- und Viszeralchirurgie, Universitätsklinikum Ulm, DE-89081 Ulm, Germany; andreas.hillenbrand@uniklinik-ulm.de

Junghanss Thomas, Sektion Klinische Tropenmedizin, Universitätsklinikum Heidelberg, Heidelberg, DE-69120 Germany; thomas.junghanss@urz.uni-heidelberg.de

Romig Thomas, Department of Parasitology, Fachgebiete Parasitologie, Universität Hohenheim, D-70593 Stuttgart, DE-70599 Stuttgart, Germany; thomas.romig@uni-hohenheim.de

Schmidberger Julian, Klinik für Innere Medizin I, Universitätsklinikum Ulm, DE-89081 Ulm, Germany; julian.schmidberger@uniklinik-ulm.de

Italy

Casulli Adriano, WHO Collaborating Centre for the Epidemiology, Detection and Control of Cystic and Alveolar Echinococcosis; European Union Reference Laboratory for Parasites; Foodborne and Neglected Parasitic Diseases Unit, Department of Infectious Diseases, Istituto Superiore di Sanità, IT-00161 Rome, Italy; adriano.casulli@iss.it

Masala Giovanna, Istituto Zooprofilattico Sperimentale della Sardegna, IT-07100 Sassari, Italy; giovanna.masala@izs-sardegna.it

Tamarozzi Francesca, WHO Collaborating Centre for the Epidemiology, Detection and Control of Cystic and Alveolar Echinococcosis; Department on Infectious Diseases, Istituto Superiore di Sanità, IT-00161 Rome, Italy; f_tamarozzi@yahoo.com

Iran

Jalousian Fateme, Department of Parasitology, Faculty of Veterinary Medicine, University of Tehran, IR-1417466191Iran; jalousian_f@ut.ac.ir

Sadjjadi Seyed Mahmoud, Dept. Parasitology and Mycology, School of Medicine, Shiraz University of Medical Sciences, IR-PO Box 71348-14336 Shiraz, Iran; sadjjadi316@gmail.com

Kenya

Zeyhle Eberhard, Meru University of Sciences and Technology, KE-60200 Meru, Kenya; zeana07@gmail.com

Morocco

Kachani Malika, Département de Parasitologie Institut Agronomique et Vétérinaire Hassan II, MA-BP 6202, Rabat, Morocco & College of Veterinary Medicine, Western University of Health Sciences, US-91766-1854 Pomona, CA, USA; mkachani@westernu.edu

Portugal

Menezes da Silva Antonio, World Association of Echinococcosis (Past-President); College of General Surgery of the Portuguese Medical Association (Associação dos Médicos Portugueses), PT-1749–084 Lisbon, Portugal; mensilvapt@yahoo.com

Switzerland

Gottstein Bruno, Institut für Parasitologie, Vetsuisse Facultät Bern, & Immuno-parasitologie, Medizinische Fakultät, Universität Bern, CH-3008 Bern, Switzerland; bruno.gottstein@vetsuisse.unibe.ch

Torgerson Paul, Abteilung für Epidemiologie, Vetsuisse Facultät Zürich, Universität Zürich, CH-8057 Switzerland; paul.torgerson@access.uzh.ch

Wang Junhua, Institut für Parasitologie, Vetsuisse Facultät Bern, Universität Bern, CH-3008 Bern, Switzerland; junhua.wang@vetsuisse.unibe.ch

Tunisia

Dziri Chadli, Département de Chirurgie Générale, Faculté de Médecine de Tunis, & Centre de Simulation Médicale Honoris, Université El Manar, TN-1068 Tunis, Tunisia; chadli.dziri@planet.tn

Jemli Mohamed Habib, Service de Parasitologie- Département Clinique de l’École Nationale de Médecine Vétérinaire – TN-2020 Sidi Thabet, Tunisia; jemli.medhabib@yahoo.fr

Lahmar Samia, Service de Parasitologie, Département Clinique de l’École Nationale de Médecine Vétérinaire, TN-2020 Sidi Thabet, Tunisia; drlsamia@yahoo.fr

Turkey

Akhan Okan, Department of Radiology, Hacettepe Üniversitesi/University, TR- 06230 Ankara, Turkey; akhano@tr.net

Altintas Nazmiye, Department of Parasitology, Ege Üniversitesi/University, TR-35040 Bornova-Izmir, Turkey; nazmiye.altintas@ege.edu.tr

Avcioglu Amza, Department of Veterinary Parasitology, Ataturk Üniversitesi/University, TR-25030 Yakutiye-Erzurum,Turkey; havcioglu@atauni.edu.tr

Güven Esin, Department of Parasitology, Ataturk Üniversitesi/University, TR-25030 Yakutiye-Erzurum, Turkey; esinguven@atauni.edu.tr

United Kingdom

Boufana Belgees, National Reference Laboratory for Trichinella & Echinococcus, National Wildlife Management Centre, Animal and Plant Health Agency, GB-YO41 1LZ Sand Hutton, York, United Kingdom; belgees.boufana@apha.gov.uk

Rogan Michael, School of Science, Engineering & Environment, University of Salford, GB-M5 4WT, Manchester, United Kingdom; m.t.rogan@salford.ac.uk

USA

Budke Christine, Department of Veterinary Integrative Biosciences, College of Veterinary Medicine & Biomedical Sciences, Texas A&M University, US-77843-4458 College Station, TX, USA; cbudke@cvm.tamu.edu

Acknowledgments

The Steering and Writing Committee would like to thank in particular Dr. Francesca Tamarozzi for her involvement in the fruitful exchanges between the WAE and the WHO-IWGE, and for her very helpful revision of the final manuscript.

References

  1. Addy F, Wassermann M, Banda F, Mbaya H, Aschenborn J, Aschenborn O, Koskei P, Umhang G, De La Rue M, Elmahdi IE, Mackenstedt U, Kern P, Romig T. 2017. Genetic polymorphism and population structure of Echinococcus ortleppi. Parasitology, 144, 450–458. [CrossRef] [PubMed] [Google Scholar]
  2. Aji T, Dong J-H, Shao Y-M, Zhao J-M, Li T, Tuxun T, Shalayiadang P, Ran B, Jiang T-M, Zhang R-Q, He Y-B, Huang J-F, Wen H. 2018. Ex-vivo liver resection and autotransplantation as alternative to allotransplantation for end-stage hepatic alveolar echinococcosis. Journal of Hepatology, 69, 1037–1046. [CrossRef] [PubMed] [Google Scholar]
  3. Akhan O, Salik AE, Ciftci T, Akinci D, Islim F, Akpinar B. 2017. Comparison of long-term results of percutaneous treatment techniques for hepatic cystic echinococcosis types 2 and 3b. American Journal of Roentgenology, 208, 878–884. [CrossRef] [Google Scholar]
  4. Ambregna S, Koch S, Sulz MC, Grüner B, Öztürk S, Chevaux J-B, Sulima M, de Gottardi A, Napoléon B, Abergel A, Bichard P, Boytchev I, Deprez P, Dumortier J, Frossard J-L, Kull E, Meny B, Moradpour D, Prat F, Vanbiervliet G, Thevenot T, Vuitton DA, Bresson-Hadni S, Vuitton L. 2017. A European survey of perendoscopic treatment of biliary complications in patients with alveolar echinococcosis. Expert Review of Anti-Infective Therapy, 15, 79–88. [CrossRef] [PubMed] [Google Scholar]
  5. Arrabal JP, Avila HG, Rivero MR, Camicia F, Salas MM, Costa SA, Nocera CG, Rosenzvit MC, Kamenetzky L. 2017. Echinococcus oligarthrus in the subtropical region of Argentina: first integration of morphological and molecular analyses determines two distinct populations. Veterinary Parasitology, 240, 60–67. [CrossRef] [PubMed] [Google Scholar]
  6. Azizi A, Blagosklonov O, Lounis A, Berthet L, Vuitton DA, Bresson-Hadni S, Delabrousse E. 2015. Alveolar echinococcosis: correlation between hepatic MRI findings and FDG-PET/CT metabolic activity. Abdominal Imaging, 40, 56–63. [CrossRef] [PubMed] [Google Scholar]
  7. Batsch AJGK. 1786. Naturgeschichte der Bandwurmgattung und ihrer Arten insbesondere, nach den neuern Beobachtungen in einem systematischen Auszuge.Halle: Ben Johann Jacob Gebauer. [Google Scholar]
  8. Ben Amor N, Gargouri M, Gharbi HA, Golvan YJ, Ayachi K, Kchouck H. 1986. Essai de traitement par ponction des kystes hydatiques abdominaux inopérables. Annales de Parasitologie Humaine et Comparée, 61, 689–692. [Google Scholar]
  9. Boufana B, Stidworthy MF, Bell S, Chantrey J, Masters N, Unwin S, Wood R, Lawrence RP, Potter A, McGarry J, Redrobe S, Killick R, Foster AP, Mitchell S, Greenwood AG, Sako Y, Nakao M, Ito A, Wyatt K, Lord B, Craig PS. 2012. Echinococcus and Taenia spp. from captive mammals in the United Kingdom. Veterinary Parasitology, 190, 95–103. [CrossRef] [PubMed] [Google Scholar]
  10. Brunetti E, Kern P, Vuitton DA, Writing Panel for the WHO-IWGE. 2010. Expert consensus for the diagnosis and treatment of cystic and alveolar echinococcosis in humans. Acta Tropica, 114, 1–16. [CrossRef] [PubMed] [Google Scholar]
  11. D’Alessandro A, Rausch RL. 2008. New aspects of neotropical polycystic (Echinococcus vogeli) and unicystic (Echinococcus oligarthrus) echinococcosis. Clinical Microbiology Reviews, 21, 380–401. [CrossRef] [PubMed] [Google Scholar]
  12. Denk D, Boufana B, Masters NJ, Stidworthy MF. 2016. Fatal echinococcosis in three lemurs in the United Kingdom – a case series. Veterinary Parasitology, 218, 10–14. [CrossRef] [PubMed] [Google Scholar]
  13. Deplazes P, Rinaldi L, Alvarez Rojas CA, Torgerson PR, Harandi MF, Romig T, Antolova D, Schurer JM, Lahmar S, Cringoli G, Magambo J, Thompson RCA, Jenkins EJ. 2017. Global distribution of alveolar and cystic echinococcosis. Advances in Parasitology, 95, 315–493. [CrossRef] [PubMed] [Google Scholar]
  14. Diesing K. 1863. Revision der Cephalocotyleen. Abteilung: Paramecocotyleen. Sitzungsber. k. p. Akad. Wissensch. Wien, Math. Naturw. p. 48. [Google Scholar]
  15. Eckert J, Deplazes P, Craig PS, Gemmell M, Gottstein B, Heath D, Jenkins D, Kamiya M, Lightowlers M. 2001. Echinococcosis in animals: clinical aspects, diagnosis and treatment, in WHO/OIE manual on echinococcosis in humans and animals: a public health problem of global concern, Eckert J, Gemmell MA, Meslin FX, Pawlowski ZS, Editors. World Organization for Animal Health (OIE): Paris. p. 72–99. [Google Scholar]
  16. Eckert J, Gottstein B, Heath D, Liu F. 2001. Prevention of echinococcosis in humans and safety precautions, in WHO/OIE manual on echinococcosis in humans and animals: a public health problem of global concern, Eckert J, Gemmell MA, Meslin FX, Pawlowski ZS, Editors. , World Organization for Animal Health (OIE): Paris. p. 258–267. [Google Scholar]
  17. Eckert J, Rausch R, Gemmell M, Giraudoux P, Kamiya M, Liu F, Schantz P, Romig T. 2001. Epidemiology of Echinococcus multilocularis, Echinococcus vogeli and Echinococcus oligarthrus, in WHO/OIE manual on echinococcosis in humans and animals: a public health problem of global concern, Eckert J, Gemmell MA, Meslin FX, Pawlowski ZS, Editors. World Organization for Animal Health (OIE): Paris. p. 164–194. [Google Scholar]
  18. Eckert J, Thompson RCA. 2017. Historical aspects of Echinococcosis. Advances in Parasitology, 95, 1–64. [CrossRef] [PubMed] [Google Scholar]
  19. Einsiedel EF, Eastlick DL. 2000. Consensus conferences as deliberative democracy: a communications perspective. Science Communication, 21, 323–343. [Google Scholar]
  20. Gargouri M, Ben Amor N, Ben Chehida F, Hammou A, Gharbi HA, Ben Cheikh M, Kchouk H, Ayachi K, Golvan JY. 1990. Percutaneous treatment of hydatid cysts (Echinococcus granulosus). Cardiovascular and Interventional Radiology, 13, 169–173. [CrossRef] [PubMed] [Google Scholar]
  21. Gottstein B, Soboslay P, Ortona E, Wang J, Siracusano A, Vuitton DΑ. 2017. Immunology of alveolar and cystic echinococcosis (AE and CE). Advances in Parasitology, 96, 1–54. [CrossRef] [PubMed] [Google Scholar]
  22. Gottstein B, Wang J, Blagosklonov O, Grenouillet F, Millon L, Vuitton DA, Müller N. 2014. Echinococcus metacestode: in search of viability markers. Parasite, 21, 63. [CrossRef] [EDP Sciences] [PubMed] [Google Scholar]
  23. Graeter T, Kratzer W, Oeztuerk S, Haenle MM, Mason RA, Hillenbrand A, Kull T, Barth TF, Kern P, Gruener B. 2016. Proposal of a computed tomography classification for hepatic alveolar echinococcosis. World Journal of Gastroenterology, 22, 3621–3631. [CrossRef] [PubMed] [Google Scholar]
  24. Grenouillet F, Umhang G, Arbez-Gindre F, Mantion G, Delabrousse E, Millon L, Boué F. 2014. Echinococcus ortleppi infections in humans and cattle, France. Emerging Infectious Diseases, 20, 2100–2102. [CrossRef] [PubMed] [Google Scholar]
  25. Hüttner M, Romig T. 2009. Echinococcus species in African wildlife. Parasitology, 136, 1089–1095. [CrossRef] [PubMed] [Google Scholar]
  26. Hüttner M, Nakao M, Wassermann T, Siefert L, Boomker JDF, Dinkel A, Sako Y, Mackenstedt U, Romig T, Ito A. 2008. Genetic characterization and phylogenetic position of Echinococcus felidis (Cestoda: Taeniidae) from the African lion. International Journal for Parasitology, 38, 861–868. [CrossRef] [PubMed] [Google Scholar]
  27. Jabbar A, Swiderski Z, Mlocicki D, Beveridge I, Lightowlers MW. 2010. The ultrastructure of taeniid cestode oncospheres and localization of host-protective antigens. Parasitology, 137, 521–535. [CrossRef] [PubMed] [Google Scholar]
  28. Jacobs D, Fox M, Gibbons L, Hermosilla C. 2015. Principles of Veterinary Parasitology. Hoboken, New Jersey, USA: Willey-Blackwell. [Google Scholar]
  29. Jarnagin W. 2012. Blumgart’s surgery of the liver, biliary tract and pancreas, 5th edn. Philadelphia: Saunders. [Google Scholar]
  30. Jones J, Hunter D. 1995. Consensus methods for medical and health services research. British Medical Journal, 311, 376–380. [CrossRef] [PubMed] [Google Scholar]
  31. Junghanss T, da Silva AM, Horton J, Chiodini PL, Brunetti E. 2008. Clinical management of cystic echinococcosis: state of the art, problems, and perspectives. American Journal of Tropical Medicine and Hygiene, 79, 301–311. [CrossRef] [Google Scholar]
  32. Kassai T, Cordero del Campillo M, Euzeby J, Gaafar S, Hiepe T, Himonas CA. 1988. Standardized nomenclature of animal parasitic diseases (SNOAPAD). Veterinary Parasitology, 29, 299–326. [CrossRef] [PubMed] [Google Scholar]
  33. Kassai T. 2006. Nomenclature for parasitic diseases: cohabitation with inconsistency for how long and why? Veterinary Parasitology, 138, 169–178. [CrossRef] [PubMed] [Google Scholar]
  34. Kassai T. 2006. The impact on database searching arising from inconsistency in the nomenclature of parasitic diseases. Veterinary Parasitology, 138, 358–361. [CrossRef] [PubMed] [Google Scholar]
  35. Kern P, Menezes da Silva A, Akhan O, Müllhaupt B, Vizcaychipi KA, Budke C, Vuitton DA. 2017. The Echinococcoses: diagnosis, clinical management and burden of disease. Advances in Parasitology, 96, 259–369. [CrossRef] [PubMed] [Google Scholar]
  36. Kern P. 2010. Clinical features and treatment of alveolar echinococcosis. Current Opinion in Infectious Diseases, 23, 505–512. [CrossRef] [PubMed] [Google Scholar]
  37. Kern P, Wen H, Sato N, Vuitton DA, Gruener B, Shao Y, Delabrousse E, Kratzer W, Bresson-Hadni S. 2006. WHO classification of alveolar echinococcosis: principles and application. Parasitology International, 55(Suppl), S283–287. [CrossRef] [PubMed] [Google Scholar]
  38. Kinkar L, Laurimäe T, Acosta-Jamett G, Andresiuk V, Balkaya I, Casulli A, Gasser RB, van der Giessen J, González LM, Haag KL, Zait H, Irshadullah M, Jabbar A, Jenkins DJ, Kia EB, Manfredi MT, Mirhendi H, M’rad S, Rostami-Nejad M, Oudni-M’rad M, Pierangeli NB, Ponce-Gordo F, Rehbein S, Sharbatkhori M, Simsek S, Soriano SV, Sprong H, Šnábel V, Umhang G, Varcasia A, Saarma U. 2018. Global phylogeography and genetic diversity of the zoonotic tapeworm Echinococcus granulosus sensu stricto genotype G1. International Journal for Parasitology, 48, 729–742. [CrossRef] [PubMed] [Google Scholar]
  39. Kinkar L, Laurimäe T, Acosta-Jamett G, Andresiuk V, Balkaya I, Casulli A, Gasser RB, González LM, Haag KL, Zait H, Irshadullah M, Jabbar A, Jenkins DJ, Manfredi MT, Mirhendi H, M’rad S, Rostami-Nejad M, Oudni-M’rad M, Pierangeli NB, Ponce-Gordo F, Rehbein S, Sharbatkhori M, Kia EB, Simsek S, Soriano SV, Sprong H, Šnábel V, Umhang G, Varcasia A, Saarma U. 2018. Distinguishing Echinococcus granulosus sensu stricto genotypes G1 and G3 with confidence: a practical guide. Infection, Genetics and Evolution, 64, 178–184. [CrossRef] [Google Scholar]
  40. Kinkar L, Laurimäe T, Sharbatkhori M, Mirhendi H, Kia EB, Ponce-Gordo F, Andresiuk V, Simsek S, Lavikainen A, Irshadullah M, Umhang G, Oudni-M’rad M, Acosta-Jamett G, Rehbein S, Saarma U. 2017. New mitogenome and nuclear evidence on the phylogeny and taxonomy of the highly zoonotic tapeworm Echinococcus granulosus sensu stricto. Infection, Genetics and Evolution, 52, 52–58. [CrossRef] [Google Scholar]
  41. Kinkar L, Laurimäe T, Simsek S, Balkaya I, Casulli A, Manfredi MT, Ponce-Gordo F, Varcasia A, Lavikainen A, González LM, Rehbein S, Van der Giessen J, Sprong H, Saarma U. 2016. High-resolution phylogeography of zoonotic tapeworm Echinococcus granulosus sensu stricto genotype G1 with an emphasis on its distribution in Turkey, Italy and Spain. Parasitology, 143, 1790–1801. [CrossRef] [PubMed] [Google Scholar]
  42. Knapp J, Bart JM, Maillard S, Gottstein B, Piarroux R. 2010. The genomic Echinococcus microsatellite EmsB sequences: from a molecular marker to the epidemiological tool. Parasitology, 137, 439–449. [CrossRef] [PubMed] [Google Scholar]
  43. Kodama Y, Fujita N, Shimizu T, Endo H, Nambu T, Sato N, Todo S, Miyasaka K. 2003. Alveolar echinococcosis: MR findings in the liver. Radiology, 228, 172–177. [CrossRef] [PubMed] [Google Scholar]
  44. König C, Claussen C. 1997. Echinococcus cysticus. RoFo: Fortschritte Auf Dem Gebiete Der Rontgenstrahlen Und Der Nuklearmedizin, 167, M31. [Google Scholar]
  45. Koziol U, Brehm K. 2015. Recent advances in Echinococcus genomics and stem cell research. Veterinary Parasitology, 213, 92–102. [CrossRef] [PubMed] [Google Scholar]
  46. Koziol U, Jarero F, Olson PD, Brehm K. 2016. Comparative analysis of Wnt expression identifies a highly conserved developmental transition in flatworms. BMC Biology, 14, 10. [CrossRef] [PubMed] [Google Scholar]
  47. Koziol U, Rauschendorfer T, Zanon Rodríguez L, Krohne G, Brehm K. 2014. The unique stem cell system of the immortal larva of the human parasite Echinococcus multilocularis. EvoDevo, 5, 10. [CrossRef] [PubMed] [Google Scholar]
  48. Laurimäe T, Kinkar L, Moks E, Romig T, Omer RA, Casulli A, Umhang G, Bagrade G, Irshadullah M, Sharbatkhori M, Mirhendi H, Ponce-Gordo F, Soriano SV, Varcasia A, Rostami-Nejad M, Andresiuk V, Saarma U. 2018. 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. Parasitology, 145, 1929–1937. [CrossRef] [PubMed] [Google Scholar]
  49. Laurimäe T, Kinkar L, Romig T, Omer RA, Casulli A, Umhang G, Gasser RB, Jabbar A, Sharbatkhori M, Mirhendi H, Ponce-Gordo F, Lazzarini LE, Soriano SV, Varcasia A, Rostami Nejad M, Andresiuk V, Maravilla P, González LM, Dybicz M, Gawor J, Šarkūnas M, Šnábel V, Kuzmina T, Saarma U. 2018. The benefits of analysing complete mitochondrial genomes: Deep insights into the phylogeny and population structure of Echinococcus granulosus sensu lato genotypes G6 and G7. Infection, Genetics and Evolution, 64, 85–94. [CrossRef] [Google Scholar]
  50. Leuckart R. 1863. Die menschlichen Parasiten und die von ihnen herrührenden Krankheiten. Leipzig and Heidelberg: C. F. Winter. [Google Scholar]
  51. Lopez-Neyra C, Soler Planas M. 1943. Revision del genero Echinococcus Rud y description de una especie nueva parasita intestinal del porro en America. Revista Iberica de Parasitologia, 3, 169–194. [Google Scholar]
  52. Lymbery AJ. 2017. Phylogenetic pattern, evolutionary processes and species delimitation in the genus Echinococcus. Advances in Parasitology, 95, 111–145. [CrossRef] [PubMed] [Google Scholar]
  53. Lymbery AJ, Jenkins EJ, Schurer JM, Thompson RCA. 2015. Echinococcus canadensis, E. borealis, and E. intermedius. What’s in a name? Trends in Parasitology, 31, 23–29. [CrossRef] [PubMed] [Google Scholar]
  54. Lymbery AJ, Jenkins EJ, Schurer JM, Thompson RCA. 2015. Response to Nakao et al. – is Echinococcus intermedius a valid species? Trends in Parasitology, 31, 343–344. [CrossRef] [PubMed] [Google Scholar]
  55. McManus DP. 2013. Current status of the genetics and molecular taxonomy of Echinococcus species. Parasitology, 140, 1617–1623. [CrossRef] [PubMed] [Google Scholar]
  56. Mohammadzadeh T, Sadjjadi SM, Rahimi H. 2014. Still and moving image evidences for mating of Echinococcus granulosus reared in culture media. Iranian Journal of Parasitology, 9, 129–133. [PubMed] [Google Scholar]
  57. Nakao M, Lavikainen A, Hoberg E. 2015. Is Echinococcus intermedius a valid species? Trends in Parasitology, 31, 342–343. [CrossRef] [PubMed] [Google Scholar]
  58. Nakao M, Lavikainen A, Yanagida T, Ito A. 2013. Phylogenetic systematics of the genus Echinococcus (Cestoda: Taeniidae). International Journal for Parasitology, 43, 1017–1029. [CrossRef] [PubMed] [Google Scholar]
  59. Ortlepp J. 1937. South African helminths – Part I. Onderstepoort Journal of Veterinary Science and Animal Industry, 9, 311–336. [Google Scholar]
  60. Ozdemir F, Ince V, Barut B, Onur A, Kayaalp C, Yilmaz S. 2015. Living donor liver transplantation for Echinococcus Alveolaris: single-center experience. Liver Transplantation, 21, 1091–1095. [CrossRef] [Google Scholar]
  61. Popa AC, Akhan O, Petruţescu MS, Popa LG, Constantin C, Mihăilescu P, Creţu CM, Botezatu C, Mastalier B. 2018. New options in the management of cystic echinococcosis – a single centre experience using minimally invasive techniques. Chirurgia (Bucharest, Romania: 1990), 113, 486–496. [Google Scholar]
  62. Rausch RL, Bernstein JJ. 1972. Echinococcus vogeli sp. n. (Cestoda: Taeniidae) from the bush dog, Speothos venaticus (Lund). Zeitschrift für Tropenmedizin und Parasitologie, 23, 25–34. [Google Scholar]
  63. Rausch RL, Nelson GS. 1963. A review of the genus Echinococcus Rudophi, 1801. Annals of Tropical Medicine and Parasitology, 57, 127–135. [CrossRef] [PubMed] [Google Scholar]
  64. Rogan MT, Hai WY, Richardson R, Zeyhle E, Craig PS. 2006. Hydatid cysts: does every picture tell a story? Trends in Parasitology, 22, 431–438. [CrossRef] [PubMed] [Google Scholar]
  65. Romig T, Deplazes P, Jenkins D, Giraudoux P, Massolo A, Craig PS, Wassermann M, Takahashi K, de la Rue M. 2017. Ecology and life cycle patterns of Echinococcus species. Advances in Parasitology, 95, 213–314. [CrossRef] [PubMed] [Google Scholar]
  66. Romig T, Ebi D, Wassermann M. 2015. Taxonomy and molecular epidemiology of Echinococcus granulosus sensu lato. Veterinary Parasitology, 213, 76–84. [CrossRef] [PubMed] [Google Scholar]
  67. Rudolphi CA. 1801. Beobachtungen über die Eingeweidewürmer. Archiv für Zoologie und Zootomie, 2, 1–65. [Google Scholar]
  68. da Silva AM. 2011. Hydatid cyst/cystic echinococcosis: anatomical and surgical nomenclature and method to quantify the cyst content solidification. Chinese Medical Journal, 124, 2806–2812. [PubMed] [Google Scholar]
  69. Soares Mdo C, Rodrigues AL, Moreira Silva CA, Brito EM, Gomes-Gouvêa MS, Corrêa IR, Pinho JRR, Malheiros AP, Nunes HM, Póvoa MM. 2013. Anatomo-clinical and molecular description of liver neotropical echinococcosis caused by Echinococcus oligarthrus in human host. Acta Tropica, 125, 110–114. [CrossRef] [PubMed] [Google Scholar]
  70. Spiliotis M, Brehm K. 2009. Axenic in vitro cultivation of Echinococcus multilocularis metacestode vesicles and the generation of primary cell cultures. Methods in Molecular Biology, 470, 245–262. [CrossRef] [Google Scholar]
  71. Tamarozzi F, Vuitton L, Brunetti E, Vuitton DA, Koch S. 2014. Non-surgical and non-chemical attempts to treat echinococcosis: do they work? Parasite, 21, 75. [CrossRef] [EDP Sciences] [PubMed] [Google Scholar]
  72. Thompson R, McManus D. 2001. Aetiology: parasites and life-cycles, in WHO/OIE manual on echinococcosis, in humans and animals: a public health problem of global concern, Eckert J, Gemmell MA, Meslin FX, Pawlowski ZS, Editors. World Organization for Animal Health (OIE): Paris. [Google Scholar]
  73. Tsai IJ, Zarowiecki M, Holroyd N, Garciarrubio A, Sánchez-Flores A, Brooks KL, Tracey A, Bobes RJ, Fragoso G, Sciutto E, Aslett M, Beasley H, Bennett HM, Taenia solium Genome Consortium, Cai X, Camicia F, Clark R, Cucher M, De Silva N, Day TA, Deplazes P, Estrada K, Fernández C, Holland PWH, Hou J, Hu S, Huckvale T, Hung SS, Kamenetzky L, Keane JA, Kiss F, Koziol U, Lambert O, Liu K, Luo X, Luo Y, Macchiaroli N, Nichol S, Paps J, Parkinson J, Pouchkina-Stantcheva N, Riddiford N, Rosenzvit M, Salinas G, Wasmuth JD, Zamanian M, Zheng Y, Cai J, Soberón X, Olson PD, Laclette JP, Brehm K, Berriman M. 2013. The genomes of four tapeworm species reveal adaptations to parasitism. Nature, 496, 57–63. [Google Scholar]
  74. Vuitton D, Bresson-Hadni S. 2014. Alveolar echinococcosis: evaluation of therapeutic strategies. Expert Opinion on Orphan Drugs, 2, 67–86. [Google Scholar]
  75. Vuitton DA. 2009. Benzimidazoles for the treatment of cystic and alveolar echinococcosis: what is the consensus? Expert Review of Anti-Infective Therapy, 7, 145–149. [CrossRef] [PubMed] [Google Scholar]
  76. Vuitton DA, Gottstein B. 2010. Echinococcus multilocularis and its intermediate host: a model of parasite-host interplay. Journal of Biomedicine & Biotechnology, 2010, 923193. [CrossRef] [PubMed] [Google Scholar]
  77. Vuitton DA, Wang Q, Zhou H-X, Raoul F, Knapp J, Bresson-Hadni S, Wen H, Giraudoux P. 2011. A historical view of alveolar echinococcosis, 160 years after the discovery of the first case in humans: part 1. What have we learnt on the distribution of the disease and on its parasitic agent? Chinese Medical Journal, 124, 2943–2953. [PubMed] [Google Scholar]
  78. Wassermann M, Aschenborn O, Aschenborn J, Mackenstedt U, Romig T. 2015. A sylvatic lifecycle of Echinococcus equinus in the Etosha National Park, Namibia. International Journal for Parasitology, Parasites and Wildlife, 4, 97–103. [CrossRef] [Google Scholar]
  79. Wassermann M, Woldeyes D, Gerbi BM, Ebi D, Zeyhle E, Mackenstedt U, Petros B, Tilahun G, Kern P, Romig T. 2016. A novel zoonotic genotype related to Echinococcus granulosus sensu stricto from southern Ethiopia. International Journal for Parasitology, 46, 663–668. [CrossRef] [PubMed] [Google Scholar]
  80. Webster G, Cameron T. 1961. Observations on experimental infections with Echinococcus in rodents. Canadian Journal of Zoology, 39, 877–889. [Google Scholar]
  81. Wen H, Vuitton L, Tuxun T, Li J, Vuitton DA, Zhang W, McManus DP. 2019. Echinococcosis: advances in the 21st Century. Clinical Microbiology Reviews, 32, pii: e00075-18. [Google Scholar]
  82. WHO Informal Working Group. 2003. International classification of ultrasound images in cystic echinococcosis for application in clinical and field epidemiological settings. Acta Tropica, 85, 253–261. [CrossRef] [PubMed] [Google Scholar]
  83. WHO Informal Working Group on Echinococcosis (WHO-IWGE). 1996. Guidelines for treatment of cystic and alveolar echinococcosis in humans. Bulletin of the World Health Organization, 74, 231–242. [PubMed] [Google Scholar]
  84. Williams RJ, Sweatman GK. 1963. On the transmission, biology and morphology of Echinococcus granulosus equinus, a new subspecies of hydatid tapeworm in horses in Great Britain. Parasitology, 53, 391–407. [CrossRef] [PubMed] [Google Scholar]
  85. Xiao N, Qiu J, Nakao M, Li T, Yang W, Chen X, Schantz PM, Craig PS, Ito A. 2005. Echinococcus shiquicus n. sp., a taeniid cestode from Tibetan fox and plateau pika in China. International Journal for Parasitology, 35, 693–701. [CrossRef] [PubMed] [Google Scholar]
  86. Zhang W, Wang S, McManus DP. 2014. Echinococcus granulosus genomics: a new dawn for improved diagnosis, treatment, and control of echinococcosis. Parasite, 21, 66. [CrossRef] [EDP Sciences] [PubMed] [Google Scholar]
  87. Zheng H, Zhang W, Zhang L, Zhang Z, Li J, Lu G, Zhu Y, Wang Y, Huang Y, Liu J, Kang H, Chen J, Wang L, Chen A, Yu S, Gao Z, Jin L, Gu W, Wang Z, Zhao L, Shi B, Wen H, Lin R, Jones MK, Brejova B, Vinar T, Zhao G, McManus DP, Chen Z, Zhou Y, Wang S. 2013. The genome of the hydatid tapeworm Echinococcus granulosus. Nature Genetics, 45, 1168–1175. [CrossRef] [PubMed] [Google Scholar]

Cite this article as: Vuitton DA, McManus DP, Rogan MT, Romig T, Gottstein B, Naidich A, Tuxun T, Wen H & Menezes da Silva A, and the World Association of Echinococcosis. 2020. International consensus on terminology to be used in the field of echinococcoses. Parasite 27, 41.

All Tables

Table 1A

Recommended terms for the genetics and epidemiology of Echinococcus species.

Table 1B

Recommended terms for the biology and immunology of Echinococcus species.

Table 1C

Recommended terms for the clinical aspects of echinococcosis.

Table 2A

Rejected terms for the genetics and epidemiology of Echinococcus species.

Table 2B

Rejected terms for the biology and immunology of Echinococcus species.

Table 2C

Rejected terms for the clinical aspects of echinococcosis.

All Figures

thumbnail Figure 1

Time schedule and main activities within the “Formal consensus” process for the definition of the terminology of echinococcosis.

In the text
thumbnail Figure 2A and B

General description of the egg and oncosphere of Echinococcus spp, according to Jabbar et al., 2010 [27]. (A) Schematic diagram of an oncosphere illustrating the structure and bilateral symmetry in the pattern of hooks and cellular organization of the hexacanth embryo. VL: vitelline layer; EM: embryophore; GL: granular layer; OM: oncospheral membrane; Hex: hexacanth embryo. (B) Cellular organization of the oncosphere. Oncospheres are approximately 25 × 30 μm.

In the text
thumbnail Figure 2C

General description of the metacestode of Echinococcus spp. (see also Table 1B and Fig. 3).

In the text
thumbnail Figure 3

“AORC” nomenclature framework for CE surgery. (A) (top) – Vocabulary and acronyms. AORC: acronym for Approach, Opening, Resection and Completeness; CE: cystic echinococcosis; OC: opened cyst; NOC: non-opened cyst. (B) (bottom) – A. Schematic structure of CE cyst: the CE cyst consists (from inside to outside) of the germinal layer, laminated layer and adventitial layer. B. Total cystectomy requires the resection of all three layers completely. C. Subtotal cystectomy requires the nearly total resection of all three layers; only parts of the adventitial layer are preserved because of surgical safety. D. Partial cystectomy refers to the incomplete resection of any of three layers (usually of the adventitial layer) due to technical and safety issue. E. Hepatectomy requires the en bloc resection of part of liver parenchyma, following the rules of hepatic resection.

In the text

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