Anatomia Histologia Embryologia

ORIGINAL ARTICLE

Terminology of the Tonsils

C. Casteleyn*, P. Simoens and W. Van den Broeck
Address of authors: Department of Morphology, Faculty of Veterinary Medicine, Ghent University, Salisburylaan 133, B-9820 Merelbeke, Belgium

*Correspondence: Tel.: (+32) 92647715; fax: (+32) 92647790; e-mail: christophe.casteleyn@ugent.be With 7 gures and 1 table Received November 2010; accepted for publication December 2010 doi: 10.1111/j.1439-0264.2010.01060.x

Summary Many terms used for referring to tonsillar structures are applied in immunological research. However, in many cases, the use of these terms is not in compliance with ofcial veterinary anatomical nomenclature. This is partly attributable to ambiguous descriptions present in conventional anatomical textbooks. This study gives an overview of pertaining controversial terms and promotes the ofcial anatomical terminology applicable to the tonsils, to enhance the unequivocal transfer of knowledge generated during immunological research. clarication of the role of the tonsils in the immunological protection of the body opened perspectives for further research, for example, on immunostimulation by intranasal and oral vaccination (Beisel and Morens, 2004). As a result, more and more researchers investigating mucosal immunology are interested in the morphology of the tonsils. Acquiring basic morphological knowledge of these structures is, however, hampered by a number of ambiguous descriptions of their anatomical localisation and microstructure in conventional anatomical textbooks. Moreover, the terminology used by different authors is equivocal. Therefore, this study aims at giving an overview of common ambiguities concerning the terminology of the tonsils in domestic mammals and discussing the ofcial anatomical nomenclature pertaining to these structures. Denition of tonsils h et al. (2003), a tonsil is dened as a According to Ola complex organ that contains a crypt (crypta tonsillaris) surrounded by dense lymphoid tissue. This lymphoid tissue is organised in well-circumscribed aggregations of mainly B lymphocytes, ofcially called lymph nodules (lymphonodulus or nodulus lymphaticus) (World Association of Veterinary Anatomists, 2005), which are separated by inter-follicular, or better inter-nodular, regions h et al., 2003). where T cells are predominant (Ola The term lymph nodule is not commonly used by immunologists. Instead, the term lymphoid follicle is applied (Brandtzaeg and Pabst, 2004; Brandtzaeg et al.,
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Introduction Tonsils are the rst line of defence to protect the body against hazardous organisms taken up during feeding and breathing. They belong to the mucosa-associated lymphoid tissue and consist of aggregations of lymphoid cells that are located in the naso-, oro- and laryngopharynx (Cocquyt et al., 2005; Kuper, 2006; Casteleyn, 2010). This lymphoid tissue is organised in a ring of tonsils, commonly known as the ring of Waldeyer (von WaldeyerHartz, 1884), consisting of the lingual tonsil (tonsilla lingualis), the palatine tonsil (tonsilla palatina), the paraepiglottic tonsil (tonsilla paraepiglottica), the tonsil of the soft palate (tonsilla veli palatini), the tubal tonsil (tonsilla tubaria) and the pharyngeal tonsil (tonsilla pharyngea) (Table 1) (Habel, 1992; World Association of Veterinary Anatomists, 1994, 2005, Casteleyn et al., 2008b). To correspond to the ofcial anatomical nomenclature (World Association of Veterinary Anatomists, 2005), the term tonsilla pharyngea should be preferred above tonsilla pharyngealis which is mentioned in the Nomina Histologica (World Association of Veterinary Anatomists, 1994) and Terminologia Anatomica (Federative Committee on Anatomical Terminology, 1998). In dogs, an additional sublingual tonsil (tonsilla sublingualis) is present in the region of the carunculae sublinguales (Barone, 1997), but this tonsil is not a part of Waldeyers ring (Gille, 2005). During the last decades, tonsils have gained much scientic attention because it was demonstrated that they can form a portal of entry for pathogen agents such as prions (van Keulen et al., 2008; Casteleyn, 2010). The
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Terminology of the Tonsils

Table 1. Characteristics of the six tonsils in domestic mammals with indication of the type of tonsil and the position of the tonsil of the soft palate Lingual tonsil nf nf nf f f f Absent nf Palatine tonsil nfa nf f f f Absent nfa f Paraepiglottic tonsil nf Absent nf Absent Absent f Absent nf Pharyngeal tonsil nf nf nf nfb nf f Absent nf Tonsil of the soft palate Absent Absent nf, nph f, oph nfb, nph f, oph Absent nf, nph Tubal tonsil Absent Absent nf nf nf f Absent nf

Species Cat Dog Goat Horse Ox Pig Rabbit Sheep

f, follicular tonsil; nf, non-follicular tonsil; nph, nasopharyngeal location; oph, oropharyngeal location. The palatine tonsils of the cat and rabbit are categorised as non-follicular tonsils situated in a tonsillar fossa which is bordered by lymphoid semilunar fold (see text). b Schummer and Nickel (1973) mention that the equine pharyngeal tonsil and the bovine tonsil of the soft palate are of the follicular type.
a

(a)

(c)

(b)

Fig. 1. (a) and (b) Macroscopic and scanning electron microscopic images of the mucosal surface of the lingual root of the ox showing various tonsillar follicles of which the orices (arrows) are exposed in the oropharyngeal lumen. (c) Histological cross section through a lingual follicle that is composed of a crypt (1) with its fossule (2) and its surrounding lymphoid tissue consisting of lymph nodules (3) and inter-nodular lymphoid tissue (4).

2008). However, this term is not appropriate to dene a well-circumscribed aggregation of lymphoid cells because follicles, such as ovarian follicles, contain a lumen (World Association of Veterinary Anatomists, 2005). It should, however, be noticed that only tertiary and mature ovarian follicles contain a lumen (Bacha and Bacha, 2000). Conventional histological textbooks dene a tonsil as a mucosal aggregation of lymph nodules in the pharynx (Liebich, 1990; Banks, 1993; Eurell and Frappier, 2006; Samuelson, 2007). Using this denition of a tonsil, the presumed lingual tonsil in small ruminants cannot be considered as a proper tonsil because it consists only of small aggregations of lymphoid cells and no lymph nodules (Habel, 1992; Casteleyn et al., 2007b). As such,
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together with Peyers patches, tonsils can be categorised as lymphonoduli aggregati (World Association of Veterinary Anatomists, 2005). It should be noted that the term Peyers patch, which is a commonly used eponym (Brandtzaeg and Pabst, 2004; Brandtzaeg et al., 2008; Nakamura et al., 2008; Beyaz and Liman, 2009), is not an ofcial term and could be replaced by lymphonoduli aggregati intestinales in immunological literature. In contrast to lymph nodes (lymphonodi or nodi lymphatici), which are also well-organised secondary lymphoid structures that contain numerous lymph nodules and are drained by efferent lymph vessels (vasa lymphatica), tonsils do not enclose lymphatic sinuses (sinus lymphatici) and receive no afferent lymph vessels. In addition,
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Terminology of the Tonsils

C. Casteleyn, P. Simoens and W. Van den Broeck

(a)

(b)

(c)

Fig. 3. Dorsal view of the bovine lingual root and laryngopharynx. The sinus of the palatine tonsil (arrows) is bilaterally visible in the lateral oropharyngeal wall. The encircled areas represent the region in which the tonsillar fossules of the bovine lingual tonsil can be visualised macroscopically.

Fig. 2. (a) Histological section through the lingual root of the pig demonstrating the presence of lymphoid tissue in the conical tonsillar papillae. The encircled area represents a single tonsillar papilla. (b) and (c) The vallate papillae of the ovine (b) and caprine (c) tongues harbour aggregated lymphoid cells (arrows).

lymph nodes are encapsulated by connective and smooth muscle tissue (Casteleyn et al., 2008a), whereas tonsils are only partially encircled by a capsule, except for the palatine tonsils of ruminants which are completely encapsulated by a tonsillar capsule (capsula tonsillaris). Lymphoid follicle versus tonsillar follicle Two types of tonsils exist, i.e. those composed of tonsillar follicles (Balgmandeln or balghaltige Mandeln in German) and those that are not (Plattenmandeln or balgfreie Mandeln in German) (Table 1) (Schummer and Nickel, 1973). The term tonsillar follicle (folliculus tonsillaris) is used to dene the tonsillar unit that is composed of a crypt (crypta tonsillaris), its orice (fossula tonsillaris) and its surrounding lymphoid tissue consisting of lymph nodules
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and inter-nodular lymphoid tissue (Habel, 1992; World Association of Veterinary Anatomists 2005). Tonsillar follicles occur in the bovine lingual tonsil where the openings of the bulging tonsillar follicles (folliculi tonsillares) are macroscopically visible at the mucosal surface (Habel, 1992; World Association of Veterinary Anatomists, 2005; Casteleyn et al., 2007a; Cocquyt et al., 2008; Rebmann et al., 2010) (Fig. 1). In the pig, no lingual follicles are present, but lymph nodules are located within the conical papillae at the root of the tongue. These papillae are therefore called tonsillar papillae (papillae tonsillares) (Habel, 1992; World Association of Veterinary Anatomists, 2005) (Fig. 2). Similar tonsillar papillae are also present in the sheep and goat (Fig. 2). In these species, aggregated lymphoid cells are located within the connective tissue cores of the vallate papillae. The term tonsillar papilla is, however, not yet ofcially recognised in these species. In the bovine palatine tonsil, the tonsillar fossules are not directly visible at the oropharyngeal wall as the crypts of the aggregated tonsillar follicles open into a deep, narrow-mouthed cavity named the tonsillar sinus (sinus tonsillaris) (Schummer and Nickel, 1973) (Fig. 3). This tonsillar sinus was formerly called the tonsillar fossa (fossa tonsillaris) by Ackerknecht (1943) (vide infra). The tonsillar sinus is unique and specic for the bovine palatine tonsil, although Sisson and Grossman (1938) have previously mentioned the presence of sinuses in the
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Terminology of the Tonsils

(a)

(b)

Fig. 4. Histological section through the palatine tonsil of the sheep composed of two tonsillar follicles (one follicle is encircled). Each follicle has a crypt (1) of which the fossule (2) is exposed to the oropharyngeal lumen.

palatine tonsil of the sheep as well. In the latter species, however, the palatine tonsil is composed of one to three tonsillar follicles of which the fossules are directly exposed in the oropharyngeal lumen (Fig. 4). Non-follicular tonsils are composed of lymph nodules and clusters of lymphoid cells that are located underneath the pharyngeal surface epithelium (Schummer and Nickel, 1973). Examples of non-follicular tonsils are the tonsil of the soft palate and the tubal tonsil of ruminants (Fig. 5 and Table 1). Tonsillar fossa versus tonsillar sinus In domestic mammals, a tonsillar fossa is only present in carnivores and the rabbit. It is the depression that is situated in the lateral oropharyngeal wall between the palatoglossal and palatopharyngeal arches and contains the

Fig. 6. (a) The palatine tonsil of the dog (1), which is located in the lateral oropharyngeal wall, is exposed after retraction of the semilunar fold (2). A tonsillar fossa (3) is formed between this fold and the tonsil. (b) Histological section of the canine palatine tonsil (1) showing the position of the semilunar fold (2) and the tonsillar fossa (3).

palatine tonsil (Habel, 1992; World Association of Veterinary Anatomists, 2005) (Fig. 6). The tonsillar fossa has formerly been called the tonsillar sinus (Sisson and Grossman, 1938; Ackerknecht, 1943; Bradley and Grahame, 1948; Berg, 1995; Budras and

Fig. 5. Longitudinal histological section through the soft palate of the sheep. The non-follicular tonsil of the soft palate is composed of various lymph nodules (arrows) lying at the nasopharyngeal side of the soft palate, directly underneath the smooth surface epithelium.

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Terminology of the Tonsils

C. Casteleyn, P. Simoens and W. Van den Broeck

(a)

(b)

Erroneous localisation of tonsils The most prominent ambiguity concerning the localisation of the tonsils deals with the position of the tonsil of the soft palate. The studies by Cocquyt et al. (2005) and Casteleyn et al. (2007b, 2008b) have unequivocally shown that this tonsil is located at the nasopharyngeal side of the soft palate in ruminants (Fig. 5). In conventional anatomical textbooks, however, the tonsil of the soft palate is allocated to the oropharyngeal side of the soft palate in these species (Schummer and Nickel, 1973; Barone, 1997; Buda et al., 2003). In domestic carnivores, a tonsil of the soft palate that is located at the oropharyngeal side of the soft palate is mentioned by Schummer and Nickel (1973) and Habermehl (1994). This tonsil was, however, not observed in the dog by Cesta (2006), nor could it demonstrated by personal investigation. Conclusion

Fig. 7. Histological sections of the palatine tonsils of the cat (a) and rabbit (b). The tonsil (1) is covered by a semilunar fold (2) that contains an abundant amount of lymphoid tissue. A tonsillar fossa (3) is formed between this fold and the tonsil.

McCarthy, 2002). The medial wall of the tonsillar fossa is formed by a prominent mucosal fold which is called the semilunar fold (plica semilunaris) (Fig. 6). Because this fold also contains lymphoid tissue in the cat and rabbit (Barone, 1997), the palatine tonsils of these species resemble tonsillar follicles when seen on histological cross section (Fig. 7). On these sections, they present indeed a central cavity which is entirely surrounded by lymphoid tissue and could erroneously be designated as a tonsillar crypt. Its orice could be mistaken for the tonsillar fossule (Fig. 7). It should be noted that Ackerknecht (1943) mentioned the presence of both tonsillar fossae and tonsillar fossules in the equine palatine tonsil. In this ancient description, the tonsillar fossae are dened, like in the bovine palatine tonsil, as larger invaginations of the pharyngeal mucosa in which several fossules of the equine palatine tonsil open. This viewpoint is, however, no longer acknowledged in recent equine anatomical nomenclature (Barone, 1997). Erroneous names of tonsils In the pig and horse, the well-developed tonsil of the soft palate is located at the oropharyngeal side of the soft palate (Budras and Sack, 2001; Wissdorf et al., 2002). This tonsil is sometimes erroneously called the palatine tonsil in the pig (Ackerknecht, 1943; Banks, 1993; Effat and Milad, 2007). However, the latter tonsil lacks in the porcine species, and this should also be mentioned in the Nomina Histologica (Schummer and Nickel, 1973). In horses, the tonsil of the soft palate has also been designated by other names such as tonsilla palatina impar or tonsilla veli palatini impar (Ackerknecht, 1943; Dyce et al., 1991).
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The tonsils at the pharyngeal entrance of domestic mammals form only an incomplete and variably developed tonsillar ring. The number, size, organisation and location of the different tonsils vary considerably between species. For an unambiguous description of the various tonsils, a correct nomenclature of tonsillar structures, including the terms tonsillar follicle, sinus, crypt, fossa and fossula, is prerequisite. Acknowledgements The authors are indebted to Dr Griet Cocquyt and Liliane Standaert for scientic and technical assistance, respectively. References
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