Open Access
Research Article

Table 1B

Recommended terms for the biology and immunology of Echinococcus species.

Word/expression Definition Arguments for acceptance; references; linguistic clarifications Comments
* Aborted (cyst, lesion), Adjective Non-viable parasitic structure as evidenced by imaging (complete calcification in AE, CE5 cyst in CE) or histological examination (absence of viable parasitic cells). Could be used in clinical or experimental situations when evidence of absence of viability is not obtained by transplantation or in vitro culture. Distinct from “non-viable”; the definition was approved unanimously by the voters; the adjective “aborted” was preferred to the alternative “died-out” by the majority of voters (median: 10).
* Adult form, Expression Sexual reproduction stage of Echinococcus spp. parasites in their definitive hosts. More popular alternative expression to the specific scientific expression “strobilar stage” to designate this step in the development of Echinococcus spp. cestodes; expression coherent with “larval form” in the intermediate hosts. “Adult” may include all stages of development in the definitive host (fertile or immature worms i.e. with the last segment containing eggs or not).
This expression with its definition was approved by the majority of voters (median: 10)
* Adventitial layer, Expression Partly cellular and fibrous layer of host origin surrounding the inner 2 layers of parasite origin (germinal and laminated layers) of the metacestode in the intermediate host of E. granulosus sensu lato The expression was approved in order to have a coherent denomination of the various “layers” of the hydatid cyst, irrespective of their origin (parasite or host). “Adventitia” was an alternative term; it was rejected by voters (median: 2). The expression “adventitial layer” with its definition was approved by the majority of voters (median: 10)
As for “germinal membrane” and “laminated membrane”, the use of the expression “adventitial membrane” is not relevant. The correct description of the parasitic structures in the intermediate host thus includes 3 similar expressions, from inside to outside:
  • Germinal layer

  • Laminated layer

  • Adventitial layer

* Border (periparasitic), Noun For both E. granulosus s.l. and E. multilocularis, structures that surround the laminated layer, at the border with the organ parenchyma. Alternative term to “boundary” The use of “boundary” was rejected by all voters but one.
The noun “border” with its definition was approved by the majority of voters (median: 10).
Brood capsule, Expression Element budding from the germinal layer which produces protoscoleces. No synonyms. In some publications, some confusion may be found with “daughter cysts”. The 2 entities are totally different in their origin and their components (see Figs. 2A2C).
* Cyst (echinococcal or hydatid), Noun Anatomical entity produced by the growth of the metacestode of Echinococcus spp. distinct from the surrounding organ parenchyma and filled with fluid, which includes (from outside to inside)
  • Adventitial layer (of host origin, even reduced to a few infiltrating cells or to fibrous tissue)

  • Laminated layer (of parasite origin)

  • Germinal layer (of parasite origin)

  • - Cyst fluid (and its content, of both parasite and host origin).

The word “cyst” should be reserved to the clinical (or experimental) situation in CE (“hydatid” cyst) or NE; it may be observed by a variety of imaging techniques such as ultrasound imaging, computed tomography, or magnetic resonance imaging. Should never be used to designate the central necrotic cavity often developed in the AE lesions. “Pseudocyst” should be used for this cavity.
The international classification of CE cysts is based on ultrasound imaging with 5 CE stages [82] All voters supported the restriction of the noun “cyst” to CE or NE, in the context of echinococcosis (median: 10).
Two types of CE3 cysts (a and b) are now described [10, 31].
* Cyst fluid, Expression Liquid secreted by the germinal layer of Echinococcus spp. larval form and collected at the center of the “cyst” (for E. granulosus s.l.) or of the “microcysts” (for E. multilocularis). Should be reserved for in vivo situations: hydatid cysts in CE, and NE, and microcysts of AE in human and animal hosts, including experimental models. The distinction between “vesicle fluid” and “cyst fluid” was approved by all voters (median: 10); they also approved the use of “cyst” for the in vivo situation only.
* Echinococcal, Adjective Adjective proposed to qualify anything relating to all Echinococcus spp. irrespective of the species, of the pathology, or of the clinical presentation of the disease that occurs in humans or in animal intermediate or definitive hosts. Completely generic term that does not assume the species and/or stage of Echinococcus spp. The term “hydatid” is more common, but also more confusing, and should be restricted to E. granulosus s. l. Usage of “echinococcal” with the generic definition was approved by the majority of voters (median: 8).
Based on the recommendations of the World Federation of Parasitologists regarding the names of parasitic diseases [32].
https://www.waavp.org/documents/snopad-guidelines/#.XS9gBvIza00
Egg, Noun Product of the hermaphrodite fecundation in the last proglottis of the adult form of Echinococcus spp. parasites; released in the feces of the definitive hosts and the environment. Should be restricted to the stages preceding ingestion by the intermediate host and oncosphere release [27]. See Figures 2A2C for detailed description and terminology.
Fertile (strobilar stage/adult form, or worm), Adjective Adult form/strobilar stage (worm) of Echinococcus spp. in the definitive host, the last segment of which contains eggs (i.e. infectious to intermediate hosts). Production of eggs, observable in the last segment of the adult form implies that the worm is fertile (conversely, absence of eggs does not automatically imply that it is non-fertile; it may just be “immature”) Please see also the definition of “fertile” for the parasitic structures in the intermediate host, and the definition of “immature”, in this table.
* Fertile (metacestode, larva, cyst, microcyst…), Adjective Larval parasitic structure that contains viable protoscoleces and thus allows infection of the definitive hosts through scoleces or in some pathological or experimental circumstances production of newly developed metacestodes in the intermediate host. Production of protoscoleces by the germinal layer and their release in the parasitic fluid (whatever the species) implies that the metacestode is fertile. This adjective with its definition for the metacestode in intermediate hosts was approved unanimously by the voters (median: 10).
Germinal layer, Expression Inner cellular part of Echinococcus spp. metacestode, which includes several types of cells and produces several types of biological components of the metacestode (cyst fluid, brood capsules, and protoscoleces). The term “layer” should be preferred to “germinal membrane” because of the complexity of the various “layers” of the cyst, and the possible confusion of “membrane” with the cell “membrane”, which has a specific definition in biology. The correct description of the parasitic structures in the intermediate host includes three similar expressions, from inside to outside:
  • Germinal layer

  • Laminated layer

  • Adventitial layer

See also Figures 2A2C.
* Germinative cell, Expression Pluripotent somatic stem cell with some homologies but also differences to neoblasts of free-living flatworms. Germinative cells are the only mitotically active cells in the metacestode and give rise to all differentiated cells. Most commonly used expression in the literature, with this definition [47]. The expression was approved by the majority of voters (median: 8) against the alternative “germinal” (median: 3).
However, it must be noted that not all cells of the germinal layer are germinative cells.
Hooks, Noun Appendices of the adult form of Echinococcus spp. parasites that allow them to attach to the intestinal wall of the definitive hosts. This term should be used because all hooks on the scolex of Echinococcus spp. have the same size.
* Hydatid, Adjective Refers to Echinococcus spp. metacestode in intermediate hosts; more specifically refers to the metacestode of Echinococcus granulosus s.l. From the ancient Greek ὑδατίς –hydatis-, genitive – ὑδατίδος -hydatidos (vesicle/bladder full of water), “hydatid”, which describes the larval stage of Echinococcus spp. (metacestode) should never be used for the adult stage of Echinococcus spp. The restriction of the definition of the adjective “hydatid” to the metacestode of E. granulosus s.l. was approved unanimously by the voters (median: 10).
In order to avoid confusion between human diseases caused by the various species, “hydatid” should not be used to designate anything relating to alveolar echinococcosis (or E. multilocularis) or neotropical echinococcoses (or E. vogeli or E. oligarthra).
Hydatid, Noun Parasitological description of the cyst-like asexual larval form of cestodes; more specifically, description of the last stage of the metacestode of E. granulosus s.l. From the ancient Greek ὑδατίς –hydatis-, genitive – ὑδατίδος -hydatidos (vesicle/bladder full of water). Usable with this definition only for purely parasitological descriptions. Should be restricted (by usage, not strictly by definition) to the metacestode of E. granulosus s.l. It should not be used for the metacestode of E. multilocularis.
* Hydatid fluid, Expression Liquid secreted by the germinal layer of Echinococcus spp. metacestode. Following the suggestion of using “hydatid” only to qualify nouns or expressions related to E. granulosus s.l. (see above), this expression should also be restricted to these species. For any other species “fluid” should be preceded by the taxonomic name of the species, or the expression “cyst fluid” (for in vivo situations) or “vesicle fluid” (for in vitro situations) could be used. All voters but one (median: 10) approved the use of “hydatid fluid” for E. granulosus s.l. only.
** Immature (strobilar stage/adult form), Adjective Strobilar stage/adult form of Echinococcus spp. in the definitive host the last segment of which does not contain eggs (i.e. at least temporarily non-infectious to intermediate hosts). “Immature” just indicates that the adult form has not fully developed to the stage of egg production; it does not imply that the adult worm will never become fertile, as could suggest the alternative “non-fertile”. See also the entry “non-fertile” in Table 2B regarding the strobilar stage/adult form; and also “non-fertile”, approved for the metacestode in the intermediate host, in this table.
This adjective was added by the SWG, on experts by suggestion, to the list of approved terms after the poll.
* Infiltrate (periparasitic), Noun Histological components (cellular and fibrous) of host origin in alveolar echinococcosis; opposite to the “adventitial layer” of CE cysts, the cellular and fibrous infiltrate in AE has no clear limits with the surrounding liver parenchyma. Alternative term to “infiltration”. The use of “infiltrate” was approved by all voters but one (median: 10).
Laminated layer, Expression Peripheral acellular outer part of Echinococcus spp. metacestode, mostly composed of mucopolysaccharides. The laminated layer is produced by the parasite and exerts important functions in the interaction between the metacestode and the intermediate host [21]. The correct description of the parasitic structures in the intermediate host includes 3 similar expressions, from inside to outside:
  • Germinal layer

  • Laminated layer

  • Adventitial layer

The term “layer” should be preferred because of the complexity of the various “layers” of the metacestode, and the possible confusion of “membrane” with the cell “membrane”, which has a specific definition in biology. See also Figures 2A2C.
* Larva, Noun Asexual reproduction stage of Echinococcus spp. parasites in their intermediate host. Generally used as a popular equivalent of “metacestode”. All voters but 2 considered that “larva” and “metacestode” were synonymous; however, metacestode should be preferred for scientific communication; see also the entry “larval form”.
Larval form, Expression Asexual reproduction form of Echinococcus spp. parasites in their intermediate hosts. Expression coherent with the recommended expression “adult form”. The expression may be used as an equivalent of metacestode (or of larva) for communication to the public and to professionals.
** Metacestode (singular) metacestodes (plural), Noun Asexual reproduction form of Echinococcus spp. parasites in their intermediate hosts; second phase of development which includes all stages from the post-oncospheral stage to the fertile stage (with production of protoscoleces, if any). Scientific designation of cestode parasites in their intermediate hosts; larva is an alternative noun usable for communication to the public and to professionals. As the voters did not agree on the definition of “metacestode” (i.e. stages of development included in the definition), this was further discussed by experts after the poll, and the final definition (shown in the second column) was approved.
The approved definition is supported by textbooks of veterinary parasitology [28] and those on Echinococcus spp. [72].
* Microcysts (echinococcal, E. multilocularis, AE), Noun, microcystic, Adjective Multiple small cysts (under 1 cm of diameter) with germinal layer, laminated layer and periparasitic infiltrate of host’s cells and fibrosis, characteristic of AE lesions (due to E. multilocularis). Should be reserved for AE lesions in vivo; may be observed with selected imaging techniques such as Magnetic Resonance Imaging (T2-weighted images) in humans or preclinical models, and/or histological examination in experimental models. In this situation, “micro” does not refer to “microscopic” but to “small” (from ancient Greek μικρός –micros (small)) macroscopic aggregated cysts in AE, opposite to the “big” –often isolated – cysts in CE or E. oligarthra-NE or multicystic presentation of E. vogeli-NE. This noun with this definition was approved by 8/10 voters (median: 9).
Microcysts are parasitic structures, distinct from the central necrotic cavity often developed in the AE lesions (“pseudocyst” should be used for this cavity). See also the entry “pseudocyst” in this table.
The noun “microcysts”[6] may replace the expression “multiple small round cysts” found in Kodama et al., 2003[43].
* Non-fertile (metacestode, larva, cyst, microcyst…), Adjective Parasitic structure in the intermediate host that does not contain viable protoscoleces, and thus is unable to infect definitive hosts. A “non-fertile” metacestode may be “viable”; these adjectives are not synonymous [22]. This definition of “non-fertile” for the metacestode in intermediate hosts was approved by all voters but one (median: 10)
* Non-viable (metacestode, larva, cyst, microcyst, protoscolex…), Adjective Parasitic structure in the intermediate host that does not contain living cells able to proliferate in appropriate conditions, i.e. which does not grow when transplanted into a new intermediate host, or put into culture in vitro. “Non-viable” implies that the parasitic structure does not grow when transplanted into the same or a new intermediate host, or put into culture in an appropriate medium in vitro. However, non-invasive evaluation of non-viability in vivo is still imperfect [22]. This definition of “viable” for the metacestode in intermediate hosts was approved by all voters (median: 10).
Oncosphere, Noun Infectious form of Echinococcus spp. parasites resulting from the release from the egg through the action of proteolytic enzymes in the digestive system of intermediate hosts. Should be restricted to the stage following ingestion by the intermediate host, just before the cell proliferation stage (post-oncospheral stage) that will constitute the metacestode. See Figures 2A and 2B for detailed description and terminology [27].
Pericyst, Noun; pericystic, Adjective Tissue surrounding the cyst. Regarding echinococcosis, the adjective applies to E. granulosus sensu lato only: tissue/structure (e.g. liver, lung, adrenal gland, brain, etc.) that surrounds the CE cyst which includes:
  • the cyst fluid,

  • the germinal layer,

  • the laminated layer,

  • the adventitial layer.

As the cyst, in E. granulosus sensu lato infection, includes the adventitial layer, the pericyst only corresponds to the organ parenchyma (plus vessels and ducts) which surrounds the cyst. In the clinical (or animal/experimental) situation in CE, the noun “pericyst” (or the adjective “pericystic”) should not be used to designate the adventitial layer (which is “periparasitic”, not “pericystic”).
Should not be used in E. multilocularis infection to qualify the tissue/structure that surrounds the lesions.
Periparasitic, Adjective Tissue surrounding the parasite. For E. granulosus s.l.: tissue/structures that surround the laminated layer of the hydatid. In the cyst developed in E. granulosus s.l. infection in the intermediate host, the adventitial layer, produced by the host, surrounded by the normal parenchyma (plus vessels and ducts) represents the “periparasitic” tissue. In the clinical (or animal/experimental) situation in CE, “periparasitic” (which includes the adventitial layer and the normal parenchyma of the organ) should not be a synonym for “pericystic” (which only includes the normal parenchyma of the organ; see also the definition of “(hydatid) cyst” and Figs. 2A2C).
For E. multilocularis: tissue/structures that surround the laminated layer of E. multilocularis microcysts. In the lesion developed in E. multilocularis infection, the inflammatory tissue (granuloma) that surrounds the lesion without clear limit with the organ parenchyma represents the “periparasitic infiltrate”.
* Post-oncospheral stage, Expression Stage between the oncosphere and the fully constituted metacestode. As it textually refers to the “oncosphere”, this expression more precisely addresses Echinococcus spp. than “transitional larva” which may apply to any type of larvae. From a developmental biology/immunology point of view, the early stages of development in the intermediate host are crucial as this is the time when the parasite is most susceptible to killing [21, 76]; agreement on this point was unanimous (median: 10).
* Proglottis (singular), proglottides (plural), Noun Part of the adult form of Echinococcus spp. parasites resulting from the segmentation of the scolex in the intestine of definitive hosts. Referring to the Greek origin of the word (γλῶττίς: strap), “proglottis (sing), proglottides (plur) should be preferred to “proglottid”; in British English, the original plural of words from other languages is kept, hence “proglottides”. Both spellings “proglottis” and “proglottid” were in use. However, the majority of voters (median: 9) selected the original (Greek) spelling.
Protoscolex (plural: protoscoleces), Noun Prefiguration of the scolex, produced by the brood capsules budding to the outside of the germinal layer of Echinococcus spp. metacestode and released in the cyst (CE) or micro-cyst (AE) fluid. From the ancient Greek “σκὠλεξ”-scolex (worm), genitive: σκὠλεκος -scolecos, and not -scolicos; the plural form is σκὠλεκες, scoleces, and not scolices; with the prefix “πρῶτος”-protos (first/before). For illustration of the formation of the protoscoleces, see Figure 1 in Koziol et al., 2016 [46].
Scolex (plural: scoleces), Noun First segment (“head”) of the adult form of cestodes. From the ancient Greek “σκὠλεξ”-scolex (worm), genitive: σκὠλεκος -scolecos, and not -scolicos; the plural form is ςσκὠλεκες, scoleces, and not scolices. The plural form of scolex (and of all derived words) should definitely be “scoleces”.
Segment, Noun Part of the adult form of Echinococcus spp. parasites resulting from segmentation of the scolex in the intestine of definitive hosts. English equivalent of “proglottis”. May be used as a popular equivalent of “proglottis” in reviews for students and professionals, or communication to the public, etc.
** Strobilar stage, Expression Sexual reproduction stage (also called “adult form”) of Echinococcus spp. parasites in their definitive hosts. Specific scientific expression to designate this step in the development of Echinococcus spp. cestodes. Like its more popular synonym “adult form”, it includes all stages of development in the definitive host (fertile or immature worms i.e. with the last segment containing eggs or not).
Suckers, Noun Appendices of the adult form of Echinococcus spp. parasites which allow them to attach to the intestinal wall of the definitive hosts and to feed from it. No synonyms. See also Figures 2A2C.
* Vesicle fluid, Expression Liquid produced in vitro by the metacestode of Echinococcus spp., regardless of the species. Should be reserved for the in vitro situation where the fluid is devoid of host components, and when the Echinococcus spp.-derived nature is clear from the context. The distinction between “vesicle fluid” (in vitro situation) and cyst fluid (in vivo situation) and usage of the noun “vesicle” for in vitro cultures only were approved by all voters but one (median: 10).
* Vesicle (parasitic or echinococcal), Noun Anatomical entity produced by the growth in vitro of the metacestode of Echinococcus spp. regardless of the species. Should be reserved for the in vitro situation where the vesicles are devoid of host components. The distinction between “vesicle” (in vitro) and cyst (in vivo) and usage of the noun “vesicle” for in vitro cultures only, were approved by all voters but one (median: 10).
* Viable (metacestode, germinal layer, larva, cyst, microcyst, protoscoleces…), Adjective Parasitic structure of the metacestode which contains living cells able to proliferate in appropriate conditions. “Viable” implies that the structure (of any type) may grow in the same or a new intermediate host or in appropriate in vitro culture medium; viable parasitic structures may or may not contain protoscoleces (parasite stage necessary for the infection of definitive hosts). However, non-invasive evaluation of viability in vivo is still imperfect [22]. This definition of “viable” for the metacestode in intermediate hosts was approved by all voters (median: 10).
* Worm, Noun Strobilar stage of Echinococcus spp. parasite in its definitive hosts (popular term). Used as an even more popular equivalent of “strobilar stage” than “adult form”. May be a source of confusion with non-parasitic worms.
However, it is tolerated because it is useful for teaching, reviews for students and professionals, and communication to the public.
*

Agreement obtained at the second stage of the consultation (the participants in the Consultation and Rating Group had to rate their approval or rejection of the words/expressions independently on a scale from 0 to 10; whenever relevant, the median of the votes and the nature of the agreement (majority or unanimity) are given in the “Comments” column

**

Agreement to recommend a word that was not selected at the first stage of consultation; the approval was obtained at the second stage after further discussion between experts or after recommendation by the RRG.

Current usage metrics show cumulative count of Article Views (full-text article views including HTML views, PDF and ePub downloads, according to the available data) and Abstracts Views on Vision4Press platform.

Data correspond to usage on the plateform after 2015. The current usage metrics is available 48-96 hours after online publication and is updated daily on week days.

Initial download of the metrics may take a while.