Oral biology and disorders of tusked mammals

Vet Clin Exot Anim 6 (2003) 689–725

Oral biology and disorders of tusked mammals Gerhard Steenkamp, BVSc, BSc Department of Companion Animal Clinical Studies, Faculty of Veterinary Science, University of Pretoria, Private Bag X04, Onderstepoort 0010, South Africa

Mammalian tusks have caught the imagination of many hunters, traders, and researchers during the past century. Ivory from elephant tusks, as well as that of hippopotamuses, narwhals, warthogs, boars, and walruses, was sold in auctions at the turn of the eighteenth century [1]. By 1910, Bland Sutton estimated that the industrial world required, and obtained, 500 to 600 tons of ivory annually [1]. Ivory was used for a variety of products like billiard balls, furniture inlays, bangles, art pieces, piano keys, utensil handles, and even complete dentures [2,3]. Hippopotamus ivory was favored for dentures because of its hardness; walrus ivory was another favorite for this purpose [2]. Fortunately today, many of these everyday commodities can be manufactured from alternative materials and the demand for ivory has therefore, decreased. During the 1970s and 1980s elephant poaching for ivory was rife in Africa. This was an easy way of obtaining foreign currency to fuel various wars that were fought on the continent. The banning of the ivory trade in 1989 has gone a long way to help stabilize the elephant populations in Africa [3]. Unfortunately, this has also led to a decline in income for wildlife conservation in countries that manage their elephant populations well. In most of these countries, ivory that was obtained from natural deaths and those that were confiscated from illegal hunters are currently stockpiled. No clear scientific definition of the terminology ‘‘tusk,’’ ‘‘tush,’’ and ‘‘ivory’’ has been established; these words are often used as synonyms [4–7]. The term ‘‘tush’’ has also been used for the description of the primary incisor tooth in elephants that does not erupt [8]. Sperber [2] described a tusk

E-mail address: [email protected] 1094-9194/03/$ - see front matter Ó 2003 Elsevier Inc. All rights reserved. doi:10.1016/S1094-9194(03)00035-5

Berardius sp

Hyperoodon sp

Ziphius sp

(Beaked whales)

Ziphiidae

Tragulidae Cervidae

Tayassuidae

Suidae

Hippopotamus amphibius Choeropsis liberiensis Sus scrofa domesticus Sus scrofa Sus scrofa cristatus Sus verrucosus Sus verrucosus celebensis Babyrousa babyrousa Phachochoerus aethiopicus Potamochoerus porcus Hylochoerus meinertzhageni Tayassu tayacu Tayassu albirostris Tragulus javanicus Moschus Hydropotes Mesoplodon spa

Hippopotamidae

Artiodactyla

Species

Family

Order

Collared pecarry White-lipped peccary Chevrotain Musk deer Chinese water deer

Hippopotamus Pygmy hippopotamus Domestic/feral pig Wild boar Indian wild boar Java pig Celebes pig Babirussa Warthog Bushpig Giant forest hog

Common name 2/2 C 1/1 PM 3/3 M 3/3 2/1 C 1/1 PM 4/4 M 3/3 3/3 C 1/1 PM 4/4 M 3/3 3/3 C 1/1 PM 4/4 M 3/3 3/3 C 1/1 PM 4/4 M 3/3 3/3 C 1/1 PM 4/4 M 3/3 3/3 C 1/1 PM 4/4 M 3/3 2/3 C 1/1 PM 2/2 M 3/3 1/2-3 C 1/1 PM 2/1 M 3/3 3/3 C 1/1 PM 3/3 M 3/3 1/2 C 1/1 PM 3/1 M 3/3

I 2/3 C 1/1 PM 3/3 M 3/3 I 2/3 C 1/1 PM 3/3 M 3/3 I 0/3 C 1/1 PM 3/3 M 3/3 I 0/3 C 1/1 PM 3/3 M 3/3 I 0/3 C 1/1 PM 3/3 M 3/3 All males have two mandibular tusks only All males have two mandibular tusks only All males have two mandibular tusks only All males have four mandibular tusks only

I I I I I I I I I I I

Dental formula

Table 1 Tusked mammals, placed in their orders and families. Dental formulae are given and the teeth forming the tusks are indicated

C C C C C

C+I C+I C C C C C C C C C

Tusks

[15]

[15]

[15]

[10] [10] [10] [10] [10] [15]

[12] [13] [10] [10] [10] [10] [10] [10] [14] [10] [10]

Reference

690 G. Steenkamp / Vet Clin Exot Anim 6 (2003) 689–725

Elephantidae

Proboscidia

Odobenus rosmarus Dugong dugon Procavia capenisis Heterophyrax sp Derdrohyrax sp Loxodonta africana Elephas maximus African elephant Indian elephant

Walrus Dugong Rock dassie

Gray’s beaked whale

Mesoplodon grayi

34–42/46-56 (Males mandibular rostral two) 34–44/2 (Males mandibular rostral two) I 1-2/0 C 1/1 PM 3–5/3–4 M 0/0 I 1/0 C 0/0 PM 0/0 M 6/6 I 1/2 C 0/0 PM 4/4 M 3/3 I 1/2 C 0/0 PM 4/4 M 3/3 I 1/2 C 0/0 Pm 4/4 M 3/3 I 1/0 C 0/0 m 3/3 M 3/3 I 1/0 C 0/0 m 3/3 M 3/3

a

Abbreviations: C, permanent canine, I, permanent incisor, M, permanent molar, m, deciduous molar, PM, permanent mo. Mesoplodon grayi is the only species in this genus that does have maxillary teeth. b Manatees do not have incisor teeth. c The molar dentitions of the manatee and dugong are similar. They may produce up to 40 molars in a jaw during their life.

Odebaenidae Dugongidae Procaviidae

Pinnipedia Sirenia Hyracoidea

Shepherd’s beaked whale

Tasmacetus shepherdi

I I I I I I I

[11] [16,17]b,c [10] [10] [10] [18] [18]

[15]

[15]

G. Steenkamp / Vet Clin Exot Anim 6 (2003) 689–725 691

692

G. Steenkamp / Vet Clin Exot Anim 6 (2003) 689–725

as an elongated anterior tooth that protrudes beyond the occlusal plane, out of the mouth. A further distinction was made by referring to tusks as either continuously growing canines or incisors of a heterodont dentition. Tusk and tush are colloquial terms that have no broad scientific base and are used across the board for all species that have teeth that protrude from the oral cavity. In fact, Sperber [2] believes that the long canine teeth of baboons (Papio sp) deserve to be called tusks. In the literature, many species have specific teeth that have been called tusks (Table 1). Ivory is another colloquial term that is described as a whitish-yellow dentin structure, seldom covered by enamel, that makes up the tusk of the elephant, hippopotamus, walrus, narwhal, and mammoth (see references [4,5,7]). Raubenheimer et al [9] alluded to the unique pattern of the dentin of elephant tusks; they believe that the term ‘‘ivory’’ should be reserved for elephant tusks only. It is beyond the scope of this article to address all dental and oral disease of the species that are mentioned in Table 1. This article focuses mainly on the dental, and some oral, aspects of the elephant, walrus, various suids, and the Hippopotamidae.

Functions of tusks The diversity in the function of tusks is paralleled only by the variation in the species in which they occur. Where the canines form the tusks, they are often associated with defending the individual [2]. This is a phenomenon seen in the Chinese water deer (Hydropotes inermis) and musk deer (Moschus moschiferus), where the deer species that do not have antlers, develop canines that are long and protruding from the oral cavity. It is also present in the chevrotain (Tragulus javanicus) [10]. It is possibly an adaptation for their forest habitat. Apart from physically attacking another individual, tusks can also be used as a defensive shield as in the case with the babirusa (Babyrousa babyrussa) [19]. Sub adult elephants and narwhals (Monodon monoceros) can often be seen to spar with one another, using their tusks as weapons [20–22]. In the walrus (Odobenus rosmarus) tusks are used to help with locomotion when they haul out onto the ice [23]. The generic name Odobenus translates into English as ‘‘tooth walker’’ [24]. Mate selection on the basis of tusk size occurs in most tusked mammals. In most cases there is an exaggerated sexual dimorphism in these species. It is not clear whether larger tusked Asian elephant males attract significantly more females [25–27]. Incisor tusks of elephants and hippopotamuses are used for foraging or digging for food (see references [2,12,23]). Elephants can often be seen debarking trees with their tusks [20]. Asian elephant (Elephas maximus) bulls have been reported to debark trees for their tuskless cows [20]. African elephants will often use their tusks to rest their trunk on (Fig. 1).

G. Steenkamp / Vet Clin Exot Anim 6 (2003) 689–725

693

Fig. 1. An African elephant resting at a waterhole, with the trunk draped over the left tusk.

Among the Suidae, warthogs (Phacochoerus aetiopicus) are well known for their digging behavior with their canine tusks [28,29]. In other Suidae where the tusk does not exit the oral cavity, rooting is performed by the snout [30]. In the beaked whales of the genus Mesoplodon, a single pair of sexually dimorphic tusks is present. It is postulated that the position of these teeth may aid in species recognition of sympatric, and otherwise morphologically similar, species in this genus [31].

Dentition of tusked mammals Hippopotamidae The two hippopotamus species have incisors and canines that protrude from the oral cavity that can be classified as tusks. They are grazers and have brachyodont and bunodont premolars and molars [10]. There is some discrepancy in the literature about the number of premolars in the

694

G. Steenkamp / Vet Clin Exot Anim 6 (2003) 689–725

hippopotamus (Hippopotamus ampibius) (see references [10,12,23,32]. Laws [12] described the first premolar tooth, as a deciduous tooth that is lost by about 7 years of age. This tooth is not succeeded by a permanent tooth. If this was so, the permanent dentition of the hippopotamus should reflect three premolar teeth, and not four, as is generally the case. Suidae The Suidae differ from true herbivores because they are omnivorous [10]. The members of this family usually have canine teeth that may or may not protrude from the mouth, grow continuously, and form the tusks. The incisors occlude on each other and form a functional shearing apparatus. Suidae, like the Hippopotamidae, have a relatively unspecialized premolar and molar dentition that is brachyodont and bunodont [10]. The warthog has a specialized third molar that is necessary to grind the grass and tough rhizomes that have associated soil particles (Fig. 2A). The soil particles increase the abrasivity of the diet [14]. This molar erupts continuously throughout life and the rostro–caudal (mesio–distal) length is often longer than the rest of the cheek teeth together [14]. The triturating occlusal surface consists of three rows, in a mesio–distal direction, of enamel-covered dentin columns that are bound by cementum. These columns are formed in the caudal mandible, as in elephants, and then migrate mesially (rostrally) to come into occlusion (Fig. 2B) [14]. In the babirusa, the maxillary canines do not exit the maxilla through the oral cavity, but erupt dorsally through the maxilla (Fig. 3) [33]. Tayassuidae The peccaries, or New World pigs, are closely related to the Suidae. The canines form the tusks in this family; however, they rarely protrude from the oral cavity [34]. Their cheek teeth are also brachyodont and bunodont [10]. Monodontidae The narwhal is edentulous except for two maxillary incisors. The left maxillary incisor usually elongates in males to form the magnificent and unique tusk [23,35]. Ziphiidae Most species of beaked whale only have two to four mandibular teeth. These are conically-shaped and are much larger in the males than the females. Two of the genera have additional teeth; the dentition is homodont except the tusks (see Table 1) [15].

G. Steenkamp / Vet Clin Exot Anim 6 (2003) 689–725

695

Fig. 2. (A) The warthog has a specialized third molar (*) that is adapted to cope with its coarse diet. It is formed over a 3- to 4-year period as the tooth erupts fully into wear. (B) A warthog third molar fully in occlusion (*) having encroached upon the worn second (#) and first molars as it has migrated mesially (rostrally).

Odobaenidae Incisors occur in the maxilla of walruses, however, their function is unclear. The maxillary canines are enlarged and form the tusks in this species. All postcanine teeth are uniform in size and have single roots [11,36]. They have a simple crown morphology that is well-adapted to their seafood diet that needs to be prehended and consumed in the water [10]. Dugongidae The dugong (Dugong dugon) is the only member of this family, and, like the elephant, has two incisors in the maxilla that develop into tusks (Fig. 4). These tusks, however, rarely protrude beyond the borders of the oral cavity.

696

G. Steenkamp / Vet Clin Exot Anim 6 (2003) 689–725

Fig. 3. A lateral radiograph of a babirusa’s maxilla. The open apices of the maxillary tusks are indicated by ‘‘A’’.

Various other characteristics, like continuously-forming molars, internal genitalia, two mammary glands on the chest, similar heart structure, and so forth, makes them close relatives to the Elephantidae [16]. Dugongs share the same Paleocene terrestrial mammal ancestor with the Proboscidea and Hyracoidea [37]. The dugong is a herbivore and feeds on soft aquatic vegetation, seagrass, and marine algae with its hypsodont molars [37]. Procaviidae Hyraxes are nonruminant herbivores that can use a wide variety of grasses and browsing depending on the environment factors [38,39]. The members of this family are closely related to the Elephantidae [38]. Their incisors have evolved into defensive tusks [38]. The premolars are molariform and the molars are lophodont and either brachydont or hypsodont [10]. Elephantidae Maxillary incisors are the prominent tusks that are seen in both genera of this family. Elephants do not have any canines and the cheek teeth are hypsodont [10]. Most investigators describe the first three cheek teeth that are present at birth, or soon thereafter, as deciduous molars (and not premolars). They are replaced with true molar teeth [10,40–44]. Elephant molars are made up of transverse plates of enamel-covered dentin that are bound together by cementum (Fig. 5). Each successive molar has a fairly specific number of these transverse plates (laminae) and the tooth is of

G. Steenkamp / Vet Clin Exot Anim 6 (2003) 689–725

697

Fig. 4. Rostral view of a dugong skull, showing the large maxillary bone in which two incisor tusks are carried.

specific size; both characteristics are used to determine age [40,45]. These transverse ridges are described by the term ‘‘lophodont’’ [23]. The sequential formation of new molar teeth is unique to the Elephantidae (Fig. 6) and the Sirenia [46]. Sikes [44] described the ageing of African elephants by using a fixed point [foramen mentale (FM)] of the right mandible. The number of laminae that moves past this fixed point has been correlated to relative age. The operator determines which molar is most rostral and can then work out the number of laminae at the point of the FM. The relative age is then read from a chart. The explanation of ‘‘horizontal tooth replacement’’ for the molars has been disputed [42]. Hooijer [42] described the horizontal movement of the elephant teeth as the phenomenon of ‘‘closing the ranks’’ which is seen in many other mammals. This seems to be nothing different than mesial drift that is seen in humans, primates, and other mammals.

Tusks Tusks may vary in size and origin (incisor versus canine) but they all have a similar structure. All tusks grow continuously throughout life (elodont

698

G. Steenkamp / Vet Clin Exot Anim 6 (2003) 689–725

Fig. 5. A weathered African elephant molar found near the east coast of South Africa. The components of the molars are clearly visible. The following are identifiable, cementum (A), enamel-covered dentin lamella (B), and the worn rostral portion of the tooth (C).

tooth) [23]. The distinction between the crown and root of the tusk is not clear [2]. Enamel can partly cover the dentin of a tusk (eg, hippopotamus and domestic pig canines) or is only apparent for a short period of time after eruption (eg, hippopotamus, and elephant incisors, walrus canines) (Fig. 7). The root is covered by cementum; as this tooth erupts past the gingival

Fig. 6. The continuous development of the elephant molars occurs in the caudal part of the mandible (1). Enamel-covered dentin columns are formed and gradually drift mesially (rostrally) (2). This process is continuous and as soon as the columns have moved far enough they will come into occlusion (3). After all lamellae have fused (4), molar formation is complete. As the tooth gradually drifts mesially, the mesial lamellae are lost (5) through wear. The foramen mentale (FM) has two openings.

G. Steenkamp / Vet Clin Exot Anim 6 (2003) 689–725

699

Fig. 7. The erupting second incisor of a hippopotamus. There is still an enamel covering (*) present on the tusk.

margin, it will be worn away and disappear with time. Elodont teeth have a large, conically-shaped pulp with a wide apical opening (Fig. 8) [2,23]. New dentin is deposited apically and lines the pulp cavity throughout the life of the tooth. This leads to the elongation of the tusk and closure of the pulp coronally [23,47]. In the elephant, a central area of the tusk often fails to fill

Fig. 8. Longitudinal sections of two African elephant tusks. Clearly visible is the wide apex (left) and the conical shape of the pulp chamber. In the larger tusk, the two arrows show the poorly mineralized central canal.

700

G. Steenkamp / Vet Clin Exot Anim 6 (2003) 689–725

with dentine as the tusk elongates. This is where pulp remnants have become compressed as the pulp cavity closes. These remnants are subject to dystrophic calcification but this may be incomplete. With abrasion, this poorly-mineralized area is often exposed and forms a black spot in the center of the tusk. The pulp can be described as a modified connective tissue organ that contains ground substance, vascular tissue, connective tissue, interstitial fluid, odontoblasts, fibroblasts, nervous tissue, and other minor cellular components [2,48,49]. Weatherford [48] described the innervation of the Asian elephant’s pulp. It consists of myelinated and nonmyelinated nerve fibers that terminate in the odontoblast layer [45]. Fagan et al [40,49] disputed this anatomy in the African elephant. The author is currently undertaking research in this field.

Disorders of tusks Trauma In tusked mammals, trauma is the most commonly described problem that affects the tusk. In captive elephants, fractures most commonly result from falling [50–54], fighting with exhibit mates [55], and trauma from structures in the environment [56–64]. One study of 60 North American zoos revealed that 31% of the animals had tusk fractures (N = 379) [50]. This is significantly higher than incidence rate of 5% that is reported for wild populations [17]. Inflammation of the tusk sulcus (pericoronitis) has been described in captive elephants, unrelated to tusk trauma [17]. The cause was reported to be acute or chronic infections of the sulcus, sulcular abscesses, or trauma to the sulcus itself (Fig. 9). Pericoronitis is frequently observed in otherwise healthy African elephants who are captured for translocation in the Kruger National Park, South Africa (Dr. Markus Hofmeyer, personal communication, 2001). Tusk abrasion and wear have been described on several occasions as the inciting cause of pulp exposure in the captive walrus because of the continuation of its normal digging behavior in the unnatural environment [65–68]. Kertesz and Harrison [67] described pulpitis and pulpnecrosis in a walrus that had abraded his canines on the cement enclosure. A dentinal plug had formed inside the pulp cavity, but it did not extend to the normal dentinal wall, leaving a gap through which infection gained entry to the pulp cavity. Tusk fractures with exposure of the pulp have also been described in a captive babirusa (Fig. 10) [69]. Unerupted/impacted tusks Single-tusked and tuskless elephants have been described in the literature (see references [10,25,26,70–73]). The fact that tusklessness occurs more commonly in certain localities and families suggests that this phenomenon is a heritable trait; it has been described as being sex-linked [18,71,72].

G. Steenkamp / Vet Clin Exot Anim 6 (2003) 689–725

701

Fig. 9. Trauma to the coronary band (gingiva) of an African elephant cow, in left lateral recumbency. The cause of the trauma is unknown, but it may have been caused by another family member’s tusk, during transportation. Tongue (A), Ventral surface of left tusk (normally covered by alveolar bone and gingiva) (B), Coronary band (gingiva) of the tusk (C), Trauma to coronary band, ventral to left tusk (D).

Hunting pressures on tusked animals has led to the demise of large, tuskbearing elephants in the East [26]. The impact of hunting pressures on a population and the artificial creation of a higher incidence of tusklessness has been clearly demonstrated [73]. Apart from a congenital absence of tusks, failure of a tusk to erupt because of entrapment by the overlying gingival tissue (impaction) can occur [74,75]. Aberrant growth Aberrant growth in tusked animals may occur as a result of abnormalities of an opposing tooth in species where tusks normally occlude [76] or because of trauma to the tooth itself [77]. Overgrowth of tusks is a feature that is common to most of the species that have canine tusks [76]. Probably the most common examples in museum collections are the spiral and circular tusks from wild boars found on the South Pacific Islands [2,76,78]. Circular tusks form when the occlusion between mandibular and maxillary canines is lost. The two canines usually wear each other down which maintains a normal occlusion (see references [2,12,13]). In most of the Suidae and Tayassuidae this also aids in the sharpening of these tusks (Fig. 11). The exception to this is the babirusa, where the mandibular canines cannot make contact with the maxillary canines which erupt dorsally. In this species, the animals physically abrade the tusks by rubbing them on trees and other objects; in captivity, these include enclosure walls or even the keeper’s legs

702

G. Steenkamp / Vet Clin Exot Anim 6 (2003) 689–725

Fig. 10. Fracture of a left maxillary canine (tusk) in a babirusa.

[19,76]. The maxillary tusks of the babirusa have been seen to grow in a circular fashion until they eventually penetrated the skull [76]. Subluxation of canine teeth occurs frequently in the hippopotamus during fighting. If the injury heals with the tooth displaced, this will lead to overgrowth of the canine, often in a direction out of the oral cavity [12,13]. Spiral tusks in elephants (Fig. 12) have been described by many investigators (see references [1,77,79,80]). This condition, however, has not been seen as a problem in captivity. Abnormal growth of a regrowing tusk in a walrus was recorded several years postextraction [81]. Another case of this occurring in a walrus was recently presented at the grand rounds of the Zoo Veterinary Dental Congress in Milwaukee (Dr. G. Willis, personal communication, 2002). A growth and eruption abnormality was witnessed by the author in a warthog skull that is housed in the Transvaal Museum, Pretoria, South Africa. The apex had elongated and penetrated through the mandibular bone into the oral cavity (Fig. 13). Supernumerary tusks Supernumerary tusks have been reported for most tusk-bearing mammals [10,35,76,82]. Exceptions are the beaked whales, chevrotain, and other tuskbearing deer, as well as the dugongs [10,82]. To the author’s knowledge, these have rarely been encountered in captivity.

G. Steenkamp / Vet Clin Exot Anim 6 (2003) 689–725

703

Fig. 11. Tusks of a domestic pig. The mandibular canine is long and slender whereas the maxillary canine is short and robust. Continuos wear between these two teeth keeps them sharp.

Treatment principles for dealing with tusk problems Prevention Preventing tusk fractures and stopping excessive tusk abrasion in captivity are challenges that face the administrators of collections of tusked mammals. Emphasis seems to have shifted from making the captive environment more tusk-friendly toward protecting tusks from trauma. Many zoological gardens routinely reduce tusk length in species like the elephant and babirusa [83,84]. In the elephant, caps are being used regularly on the shortened tusks to prevent further abrasion to them (see references [53,59,61,62]). This method of tusk protection has also been used with promising results in one collection of walruses [6]. The use and type of concrete for floor coverings in elephant enclosures, as well as walrus pools, has been mentioned as hazards to these tusked

704

G. Steenkamp / Vet Clin Exot Anim 6 (2003) 689–725

Fig. 12. Two malformed tusks from African elephants, spiral tusk (A) and a dilacerated tusk (B).

mammals. Using water under high pressure is often the method of choice for cleaning elephant enclosures. A flat floor is preferred because it can be cleaned much faster than a floor with corrugations. The latter, however, would give these animals a better grip and would hopefully be one way to reduce the incidence of falling and tusk fracture in elephants.

Fig. 13. Supereruption of a warthog’s mandibular tusk root apex (R). There is evidence of bone remodeling of the alveolar bone ventrolateral to the root. The mandibular third molar is the only tooth that is left in the caudal mandible (*).

G. Steenkamp / Vet Clin Exot Anim 6 (2003) 689–725

705

Walrus enclosures have received much attention throughout the years (see references [65–67,85–87]). These animals continuously dig at the pool floor or even at junctions between the wall and observation glass panels. When these animals haul out they also use their tusks for locomotion, so pools and enclosures should be constructed in such a way that the normal locomotor and digging behaviors can occur without damage to the tusks. Babirusas need objects, like trees, in their enclosures on which to abrade their mandibular tusks. The maxillary tusks are brittle and break easily during fighting. In captivity, bairusas’ maxillary tusk needs frequent trimming to reduce the risk of fracture [84]. If there is a malocclusion, the canine tusks of the hippopotamus may require regular trimming to avoid secondary problems [13,32]. Elephant tusks that have longitudinal or oblique fractures without pulp exposure, have been successfully treated by application of circumferential rings or bands (Fig. 14). These protect the tusk, prevent the extension of splits, and avoid pulp exposure [53,63]. Gingivectomy Impacted tusks can cause localized swelling and can be painful to the touch [74]. In two recorded cases, normal eruption occurred after excessive gingiva was removed [74,75]. Partial pulpectomies Tusked mammals have a large proportion of pulp with a good blood supply compared with that seen in humans and dogs; therefore, they can deal better with pulpitis [80,88,89]. Pulpitis may lead to pulp necrosis (Fig. 15),

Fig. 14. A tusk ring applied to a juvenile African elephant to prevent further splitting of a longitudinally-fractured tusk. The fracture line did not extend into the pulp canal.

706

G. Steenkamp / Vet Clin Exot Anim 6 (2003) 689–725

Fig. 15. A complicated fracture of a 6-year-old African elephant’s tusk. Pulp necrosis was present. Purulent material is being curetted out of the pulp canal. The canal was then thoroughly lavaged before pulp amputation was performed.

which, in turn, is likely to progress to periapical abscessation (see references [32,57,90,91]. Animals who suffer fromo pulpitis may feed poorly, have pain, be aggressive, depressed or unresponsive to handlers, and, ultimately, may die (see references [32,57,90–93]. Elephant tusks have a great potential to withstand trauma (see referenecs [80,88–90,94]. Many cases, from as far back as the nineteenth century, have been documented where musket balls or spear blades have been walled off within the pulp canal. This regenerative/ reparative potential makes these teeth good candidates for partial pulpectomies. Pulp exposure often leads to extensive tertiary/reparative dentin formation in the pulp (Fig. 16) [95]. Reparative dentin formation in African elephant tusks is well-described. In the walrus, tertiary/reparative dentin is often found throughout the entire length of the pulp canal; only a small part of the apical pulp is free from it. This dentinal plug, unlike those in elephants, is not attached to the wall of the pulp cavity. This complicates the use of partial pulpectomies in tusk treatment in the walrus [67]. Before applying a pulp dressing to the exposed pulp, necrotic/inflamed tissue should be removed and the canal should be cleaned (see references [59,60,96–98]). In the literature, many different irrigating solutions have been used, as listed in Table 2. The author uses copious amounts of lactated ringers solution for lavage while curetting or amputating necrotic pulp. The amount of pulp to be removed depends on the specific tooth, but it is recommended that pulp is excised to a depth equal to four times the pulpcavity diameter at the coronal end of the live tissue (Dr. Peter Kertesz, personal communication, 2002). An ideal dressing is one that is antibacterial, biocompatible, and stimulates the formation of a hard tissue (reparative dentin) bridge to seal the pulp.

G. Steenkamp / Vet Clin Exot Anim 6 (2003) 689–725

707

Fig. 16. Looking in a coronal direction from the apical opening of an extracted tusk that had partially recovered from a complicated fractured. Several small dentin spicules are attached to the tusk wall (A). Several large dentin structures (B) were produced in an attempt to wall off the infection.

Paraformaldehyde, usually used as formocresol, has been used with apparent success since 1930. Formocresol fixes the pulp which creates a mass of necrotic tissue and rapidly loses its antibacterial effect. Formocresol is usually used in higher concentrations than the 10% used to fix pathologic specimens. Its volatile vapors are antimicrobial. It is mutagenic, carcinogenic, and toxic; therefore, this product is not a good choice and should not be used [105]. Twenty-one juvenile elephants were endodontically treated for molar abscessation. Three of these cases, in which formocresol and zinc oxideeugenol (ZOE) were used as filling material, failed. The other eighteen individuals were treated with ZOE and calcium hydroxide (CaOH) with more acceptable results [106]. Zinc-oxide eugenol has been used extensively for indirect pulp cappings, endodontics, cementation of bridges and inlays, and as a base material and temporary restorative in humans [101]. The free eugenol in the product has local anesthetic properties. Unfortunately, ZOE is cytotoxic and its value is questioned when used on deep cavities or directly on pulp [103– 105]. It does, however, have antibacterial properties; further research is needed to determine the extent to which the cytotoxicity may negatively impact the large pulp of elodont teeth. Calcium hydroxide paste is currently the product of choice for treating exposed pulp in humans. This is only true for the paste form, because there is no proof that the hard setting compounds readily dissociate into the calcium (Ca) and hydroxide (OH) ions, that give the product its high pH and makes it effective. The alkaline pH of calcium hydroxide also makes it a good antibacterial product. Calcium hydroxide paste causes necrosis of a thin layer of tissue and stimulates a pulpal reaction

ZOE + formocresol

Gauze

3% hypochloride + saline

None

Dental plaster

Water

Zoe + (Oxytetracycline/ hydrocortisone)

None

Hydrogen peroxide + saline None

Tub and tile sealer + brass crown

Plaster

ZOE

Composite + fast curing epoxy chrome-cobalt (Vitallium) crown

Abscess, cellulitis formation, filling loosened

Daily flushings, no growth after 2 years

Crown and filling lost in 2 weeks

Changed weekly initially and then every second week - Tusk growing

15 days postoperative filling dropped out

Tusk growing

Filling lost in 1 day

Dropsin + Omniflex

Glass ionemer + chemical cure composite

Filling lost in 11 days

African elephant Hydrogen peroxide + saline ZOE

Asian elephant

No infection and filling in place 2 months post-operative

Outcome

First part of two step pulpotomy procedure ZOE + Formocresol Extraction

Does not say

Coronal filing materials

CaO + Type III, low viscosity Nonirritating epoxy (PC7) polysulfide (Omniflex)

CaOH (Dropsin)

African elephant None

None

Formocresol

African elephant 0.9% NaCl + povidone-iodine Sterile distilled water

Pulp dressing

Paraformaldehyde + ZOE

Flushing agent

African elephant Does not say

Species treated

[56]

[56]

[56]

[48]

[48]

[49]

[49]

[49]

[99]

[102]

Reference

Table 2 Partial pulpectomy procedures as described in the literature. Species and outcome of various treatment regimes are included. Success is taken as a growing tusk; however this does not indicate histologic response to treatment (ie, hard bridge formation (secondary dentin bridge)) 708 G. Steenkamp / Vet Clin Exot Anim 6 (2003) 689–725

None

None

Saline

Elephants

Indian elephant

BIP

Iodine + Chloramphenicol + BIP

None

None

None

No resolution

Filling lost 26 days postoperation

Filling lost in 12 hours

De Puy synthetic casting Pencillin, hemostatic powder and Gelocast R-impregnated tape (Tuff Stuff R) + metal crown gauze

None

Tuff Stuff R + chrome steel plate

Filling lost 35 days postoperatively

[100]

[100]

[100]

[100]

[97]

[107]

[58,98,131]

[57]

[58]

[56]

(continued on next page)

Tusk growing 10 weeks postoperatively

Penicillin, hemostatic powder De Puy synthetic casting and Gelocast R-impregnated tape (Tuff Stuff R) + gauze crown

Glass ionemer

None given

Composite lost, tusk growing

Tusk growing, 22 months postoperatively

Tusk growing

Tooth exfoliated after approximately 4 years and 8 months of treatment

African elephant None

CaOH (Pulpdent)

CaOH (Dycal)

African elephant None

Composite restorative + crown Glass ionemer + composite

Cork

Iodoform gauze soaked in Chloramphenicol

African elephant Hydrogen peroxide + iodine

None

Set screw + steel impregnated epoxy, nickel-crucible

None

African elephant 1:10 dilution of povidine iodine-Chloromycetin sodium succinate Penicillin G

10% hypochloride, 10% betadine/hydrogen peroxide

G. Steenkamp / Vet Clin Exot Anim 6 (2003) 689–725 709

Table 2 (continued )

None

Irrigation in a lateral direction, no drugs mentioned

Lactated Ringer’s solution

Lactated Ringer’s solution

African elephant

Asian elephant

African elephant (2)

Babirusa

CaOH powder

Compomer (Dyract)

Intermediate restorative material placed. Undercuts made

Nylon or Delrin rod

Dacron membrane impregnated with Whitehead’s varnish and CaOH

CaOH powder

Composite

Glass ionomer + composite + amalgam + Aluminium crown

Polyoxymethylene bolt

None

Coronal filing materials

Gentamycin antibiotic ointment + Bioglass synthetic bone graft particulate

Topical antibacterial + CaOH (Dycal)

Abbreviations: CaOH, calcium hydroxide; ZOE, zinc oxide eugenol.

None

Malaysian elephant

Sterile polyester gauze

Pine tar and oakum

None

Saline + 10% povidone iodine

Pulp dressing

Flushing agent

Babirusa

Species treated

Author’s unpublished data

Author’s unpublished data

Tusks growing 6 months postoperative Filling lost 14 months postoperative, tusk growing

[62,106]

[98]

[108]

[67]

[100]

Reference

Tusk growing

Tusk growth 4 weeks postoperatively

Tusk growing 18 months postoperatively

Tusk growing

Tusk growing at constant rate, but no dentinal bridge formation

Outcome

710 G. Steenkamp / Vet Clin Exot Anim 6 (2003) 689–725

G. Steenkamp / Vet Clin Exot Anim 6 (2003) 689–725

711

that leads to the formation of a hard tissue barrier in adjacent vital tissue [105]. Recently, the author used Ca(OH)2 powder as a dressing agent while successfully performing a partial pulpectomy on a bull African elephant and a babirusa (Figs. 17, 18). At 3 weeks postsurgery the elephant was unwell and there was concern that there may be a septic pulpitis. On re-entering the pulp canal, it was clean and a hard tissue bridge was already developing so the dressing was replaced and the tooth was resealed.

Fig. 17. (A) A shortened tusk, after a pulpectomy procedure was performed on a 12-year-old African elephant bull. The tusk suffered an oblique fracture with the fracture line extending below the gingival margin (arrows). The fracture line did not involve the pulp cavity at the level of the partial pulpectomy and pulp dressing. (B) At 15 months of follow-up there is loss of the obliquely fractured fragment, correlating to where the fracture line extended below the gingival margin. Subsequent to the tooth fragment loss and tusk abrasion, the coronal filling was also lost. The pulp had closed by production of reparatory dentin before the filling was lost.

712

G. Steenkamp / Vet Clin Exot Anim 6 (2003) 689–725

Fig. 18. (A) An 8-year-old babirusa boar suffered a complicated fracture of his right mandibular tusk. A partial pulpectomy procedure was performed. The maxillary tusks are being shortened using a cutting disc to reduce the risk of these being fractured. (B) Fourteen months later the mandibular tusk has continued to erupt and the patient seemed to have no discomfort.

The final stage of the partial pulpectomy procedure is to obturate the coronal opening with a tight-sealing filling material. Many different sealing techniques have been used with success in the past (Table 2). An ideal filling material for elodont teeth should be one that gives a good tight seal and wears away at the same rate as normal tooth when subject to attrition, is easy to use, and cost effective. The simplest measure of success is the continued normal growth of the treated tusk and exposure of normal-looking dentin when the coronal filling material has been worn away, or is lost. Histopathologic studies confirming the normality of such teeth are lacking.

G. Steenkamp / Vet Clin Exot Anim 6 (2003) 689–725

713

Currently, there is no field technique for determining whether pulp exposure is likely to have occurred when an elephant tusk fractures; most exposures are too small to detect from a distance. Robinson and Schmidt [32] attempted this by using the length from the tusk sulcus to the eye as a basis for the calculation of pulp length in erupted tusks of adult animals [25]; this is deemed inaccurate for the Asian elephant cow [83]. This method is unsuitable for juvenile and subadult animals; these do not have a coronal tusk that is of this described length and the author disputes its suitability for adult African elephants as well (Fig. 19). Research is ongoing to find a suitable model for the determination of likely pulp exposure. Extractions The indications for tusk extractions are varied. This procedure is mostly performed on tusks that have complicated fractures that carry a poor prognosis (see references (see references [17,54,83,96,107]) or where the pulp has been exposed because of abrasion (see references [65,66,108]. In the South Pacific Islands, maxillary tusk extractions on boars are performed for cultural reasons [2]. Disarming of domestic pigs that are kept as pets, is another reason for extracting teeth. These animals are strong and playful; while they are equipped with razor sharp tusks there is a serious risk of injury to their owners and other animals. In the past, regular trimming of these tusks was done [109]. The author has been approached by an owner to remove such a pig’s tusks after it had caused damage to their horse for the second time. Complete tusk extraction by the animal itself, has been

Fig. 19. Two African elephants. Note that the distance from the tusk sulcus to the eyes is less than the length of the exposed tusks. Adult cow (A) and juvenile (B).

714

G. Steenkamp / Vet Clin Exot Anim 6 (2003) 689–725

documented in wild African elephants [110]. Recently, another such case was reported; a bull African elephant lost a complete tusk, possibly because of fighting, in the Addo Elephant Park in South Africa (Dr. Markus Hofmeyer, personal communication, 2002). Surgical extraction techniques have been developed to deal with tusks. A standard surgical extraction through an alveolotomy approach can be used [111], but tends to be excessively traumatic. This has been described for various species (Fig. 20). Extracting tusks is not a procedure to be undertaken without serious consideration because specialized instrumentation is often needed to perform this type of surgery (see references [17,32,112,113,130]). The internal collapsing technique is a novel way of extracting tusks (see references [17,96,112]). The technique is based on the principle of creating a thin-walled, hollow tube. After the tusk is adequately hollowed out, longitudinal sections are made at the coronal opening, which divides the tusk into four or five segments. A protected chisel is used to extend the cuts into full-length splits that terminate at the apex of the tooth. Each segment can then be separated from the alveolar bone, with the aid of purpose-made elevators, and folded into the hollow space where it can then be extracted [17,96,113].

Fig. 20. Surgical exposure of the right mandibular tusk in a domestic pig. The tusk was extracted using a combination of alveolotomy and internal collapsing techniques.

G. Steenkamp / Vet Clin Exot Anim 6 (2003) 689–725

715

Steiner et al [114] recently presented a unique method for extracting an elephant’s tusk with the aid of elastic bands. The use of elastic bands was first used in humans who suffered from hemophilia. Elastic bands are placed around the tooth and were forced apically as far as they would go. This procedure was repeated every second day and more elastics were added. The combination of damage to the periodontal ligament, together with lateral traction daily on the tusk resulted in its exfoliation 3 weeks after the onset of treatment. Walrus tusks have a folded wall. These folds make the use of the internal collapsing technique difficult in this species, but it can be used in selected cases [67]. After the offending tusk is extracted, the empty alveolus should be cleaned of all debris. Because these teeth are elodont, curetting the apical area of the alveolus is imperative to remove or destroy any remaining germinal tissues. Failure to do so will result in regrowth of a tooth or toothlike structure [81,115]. The technique for walrus extraction, described by Cornell and Antrim [108] does not address this crucial issue.

Miscellaneous oral and dental conditions unrelated to tusks Partial anodontia Congenitally missing teeth have been recorded for the hippopotamus and the suids, especially the domestic pig [10,115,117]. This can be due to premature loss, impaction, or failure to erupt, as well as true agenesis. In the hippopotamus, partial anodontia was described in a first mandibular molar [10]. Bodegom and van der Linden [116] described the agenesis of the first lower premolars in three miniature pigs. The first premolar tooth in the pig is small and will frequently be lost. This may explain the high incidence of missing first premolars in the suids [10,117]. Missing incisors in suids are uncommon; however, an incidence of 4% was reported for this phenomenon in two small groups [117]. It is speculated that in both groups this could be as a consequence of inbreeding because of their separation from other populations [117]. Supernumerary teeth Supernumerary premolars and premolar roots were described in the Hippopotamidae [10]. This anomaly is also present in the suids but is uncommon [10,117]. In two wild populations of African elephants, the incidence of supernumerary molars was 6.1% [41]. Dento-alveolar abscesses Abscessation that is due to trauma to the incisors, premolars, and molars has been reported in the domestic pig [118,119,132]. The reasons for this are

716

G. Steenkamp / Vet Clin Exot Anim 6 (2003) 689–725

unclear, but the habit of stone chewing and bar biting has a detrimental effect on the premolars [120]. Clipping of tusks in piglets is described as a contributing factor to osteomyelitis in these animals [121]. In a herd of 85 elephants, 21 developed mandibular abscessation that was due to occlusal table perforation of the second molar [106]. In a survey of 60 North American zoos, only 35 out of 375 dental disorders were related to the molars [50]. Caries, which may lead to dento-alveolar abscessation, has been documented in the suids (see references [10,116,119,122]) and hyrax (Procavia capensis) [123]. Caries in the hyrax is associated with a refined carbohydrate diet because only captive animals were seen with this disease [123]. In the domestic pig, swill feeding may contribute to the formation of caries. Even so, the incidence of caries in suids is low, ranging from less than 0.4% [119] to less than 3.8% [117]. Impaction The Indian elephant seems to be more prone to molar impaction than the African elephant. Impaction of the molar teeth has led to weight loss,

Fig. 21. Palatal view of a collared peccary skull. There is loss of a second molar on the left (P). The palatal borders (arrows) extend medially and are rounded consistent with loss of the tooth through localized periodontal disease. Alveolar bone loss is also evident on the mesio–distal surface of the first molar’s distal root.

G. Steenkamp / Vet Clin Exot Anim 6 (2003) 689–725

717

undigested/poorly digested roughage in the feces, and even signs of colic [17,40,124,125]. It is important to give elephants a diet of good quality roughage that is abrasive enough to help with molar wear and exfoliation [45]. The high incidence of silicate phytoliths in certain diets may cause excessive wear and pulp exposure in molar teeth [17]. In the warthog, the third molar tooth continues to erupt for 3 to 4 years. In its rostral progression, this tooth compresses onto the second and first molar teeth [14,64]. This should not be mistaken for impaction. Periodontitis Periodontitis is common in the domestic and wild pigs. In two studies the incidence ranged between 6% and 24% [117,119]. In suids, periodontitis is commonly associated with the fourth premolar and first molar teeth. One collared peccary skull from the Transvaal Museum, Pretoria, South Africa showed tooth loss of the left maxillary second molar, presumably due to periodontal disease (Fig. 21). Food, bedding straw, or foil tops of discarded containers have often been found trapped between, or around the molar teeth (see references [28,119,120,125]). Canine and incisor teeth were free from periodontal disease [28,125]. It has been speculated that animals in captivity suffer more from periodontal disease than wild populations; however, Samuel and Woodall [126] found no statistical difference between a wild and domestic group of pigs. Their domestic group of pigs consisted of skulls that came from an abattoir; therefore the group was made up of young animals. This may explain the lower than expected incidence of periodontal disease in this group. The incidence of periodontal disease is

Fig. 22. African elephant bull in left lateral recumbency. The mass (M) that protrudes from the oral cavity measured nearly 40 cm in length. The tongue (T) lies ventral to the mass in this photograph. (Courtesy of Q. Otto, BVSc, Nelspruit, Mpumulanga, South Africa).

718

G. Steenkamp / Vet Clin Exot Anim 6 (2003) 689–725

Fig. 23. Skull of the African elephant in Fig. 22, showing the displacement of the maxillary molar because of the maxillary tumor. The base of the tumor was approximately 8 cm in diameter as delineated on the photograph.

9% in the warthog and is 14% the bushpig [20]. Samuel and Woodall [126] found a significantly lower incidence of periodontal disease only in the warthog. The reasons for this could be the more abrasive diet of the warthogs, as well as the fact that the third molar continues to erupt rostrally, and replaces the first two molars. Periodontal disease in elephants is usually associated with impacted molar teeth. Food gets trapped between the molars and creates a favorable environment for periodontal disease [17]. Periodontal disease may also occur around tusks if the elephant packs the sulcus with debris. This may happen when the animal is suffering from chronic irritation of the sulcus, like from sharp tooth fragments after an uncomplicated tusk fracture [127]. Tumors Tumors in the oral cavity of wild animals seems to be uncommon. Mikota et al [50] found 18 tumors in their study population of 379 individuals. None of these tumors was related to the oral cavity or dentition. Raubenheimer et al [128] were the first to describe an odontoma in an African elephant. In this case, the sixth mandibular molar was prevented from erupting. Lindeque [129] reported an abscess in one of the mandibles he used for ageing the elephants in the Etosha National Park, in Namibia. On further investigation by the author, this seems to be another odontoma; histology is currently underway to confirm this. An African elephant was recently shot because of an oral tumor. The individual was 15 to 18 years old and presented with a mass approximately

G. Steenkamp / Vet Clin Exot Anim 6 (2003) 689–725

719

40 cm long which the ranger described as looking like an extra tongue (Fig. 22). Unfortunately, no biopsy was obtained so the diagnosis cannot be confirmed. The author examined the skull after learning of the incident. This mass had originated from an 8-cm diameter base, rostro–buccal to the right maxillary molar tooth. The tumor displaced the maxillary molar in a palatal direction (Fig. 23) which produced a malocclusion with the mandibular molar. This, in turn, led to decreased wear on the mandibular molar which resulted in a crown that was higher than the contra-lateral molar. Summary Tusked mammals can be terrestrial or aquatic. Many of these magnificent animals are kept in captivity all over the world. Functions of tusks vary as much as the species in which they occur. Dental anomalies and disorders of tusks and the rest of the dentition in these mammals were discussed, with an emphasis on the elephant. The tusk anatomy, with its large, conicallyshaped pulp, makes it an ideal tooth for partial pulpectomy treatment in trauma cases where the pulp is exposed. Surgical techniques for tusks have been developed and were discussed. Oral tumors occur, but are rare.

Acknowledgments The author would like to acknowledge the significant contribution from our Library staff at Onderstepoort. They were exceptional in finding articles from around the world. Furthermore, the support from Drs. Venter and Espie, the veterinarians of the National Zoological Gardens, Pretoria, is greatly appreciated. A final word of thanks to Theresa from the Transvaal Museum for finding all sorts of interesting skulls for me to look at and photograph. References [1] Bland Sutton J. The disease of elephants’ tusks in relation to billiard balls. Lancet 1910;Nov. 26:1534–7. [2] Sperber GH. Tusks. J Can Dent Assoc 1976;5:257–68. [3] Gro¨ning K, Saller M. The ‘white gold’ trade. In: Gro¨ning K, editor. Elephants, a cultural and natural history. Gu¨tersloh, Germany: Ko¨nemann Verlagsgesellschaft mbH; 1999. p. 364–81. [4] Neufeldt V, Guralnik DB. Webster’s new world dictionary of American English. 3rd college edition. New York: Webster’s New World Dictionaries; 1988. [5] Little W, Fowler HW, Coulson J. The shorter Oxford English dictionary on historical principles, 3rd edition, Vol I. Oxford (UK): Clarendon Press; 1973. [6] Little W, Fowler HW, Coulson J. The Shorter Oxford English dictionary on historical principles, 3rd edition, Vol II. Oxford (UK): Clarendon Press; 1973. [7] Shoshani J. General information on elephants with emphasis on tusks. Elephant 1978;1:20–34.

720

G. Steenkamp / Vet Clin Exot Anim 6 (2003) 689–725

[8] Raubenheimer EJ, van Heerden WFP, van Niekerk PJ, et al. Morphology of the deciduous tusk (tush) of the African elephant (Loxodonta africana). Arch Oral Biol 1995;40(6):571–6. [9] Raubenheimer EJ, Bosman MC, Vorster R, et al. Histogenesis of the chequered pattern of ivory of the African elephant (Loxodonta africana). Arch Oral Biol 1998;43:969–77. [10] Miles AW, Grigson C. The ungulates. In: Colyer’s variations and diseases of the teeth of animals, revised edition. Cambridge, UK: Cambridge University Press; 1990. p. 106–29. [11] King JE. Dentition, age determination and longevity. In: King JE, editor. Seals of the world. Oxford, UK: Oxford University Press; 1983. p. 163–9. [12] Laws RM. Dentition and ageing of the hippopotamus. E Afr Wildl J 1968;6:19–52. [13] Johnston NW. Atraumatic malocclusion in two pygmy hippos. J Vet Dent 2002;19(3):144–7. [14] Mason DR. Dentition and age determination of the warthog Phacochoerus aethiopicus in Zululand, South Africa. Koedoe 1984;27:79–119. [15] Carwardine M, Camm M. Beaked whales. In: Carwardine M, editor. Whales, dolphins and porpoises. The visual guide to all the world’s cetaceans. London: Dorling Kindersley; 1995. p. 100–43. [16] Gro¨ning K, Saller M. Primeval wanderer. In: Gro¨ning K, editor. Elephants, a cultural and natural history. Gu¨tersloh: Ko¨nemann Verlagsgesellschaft mbH; 1999. p. 12–25. [17] Kertesz P. Dental disease and their treatment in captive wild animals. In: A colour atlas of veterinary dentistry and oral surgery. Aylesbury: Wolfe Publishing; 1993. p. 215–81. [18] Sikes SK. The African elephant and its health. In: The natural history of the African elephant. London: Weidenfeld & Nicholson; 1971. p. 185–223. [19] Huffman B. Babirusa (Babyrousa babyrussa). Available at: http://www.ultimateungulate. com/babirusa.html. Accessed November 7, 2002. [20] Gro¨ning K, Saller M. The elephant in the wild. In: Gro¨ning K, editor. Elephants, a cultural and natural history. Gu¨tersloh: Ko¨nemann Verlagsgesellschaft mbH; 1999. p. 80–107. [21] Brear K, Currey JD, Pond CM, et al. The mechanical properties of the dentine and cement of the tusk of the Narwahl Monodon monoceros compared with those of other mineralised tissue. Arch Oral Biol 1990;35(8):615–21. [22] Sperber GH, MacQuarrie E. The skull and tusk of a narwhal (Monodon monoceros). Med Biol Illus 1973;23:86. [23] Kertesz P. Comparative odontology. In: A colour atlas of veterinary dentistry and oral surgery. Aylesbury, Great Britain: Wolfe Publishing; 1993. p. 35–50. [24] King JE. Walrus. In: Seals of the world. Oxford, UK: Oxford University Press; 1983. p. 65–72. [25] Tiedermann R. Sexual selection in Asian elephants. Science 1997;278(5343):1550–1. [26] Kurt F, Hartl GB, Tiedemann R. Tuskless bulls in Asian elephant Elephas maximus. History and population genetics of a man made phenomenon. Acta Theriol (Warsz) 1995;3:125–43. [27] Bagla P. Longer tusks are healthy signs. Science 1997;276(5321):1972. [28] Woodall PF. Periodontal disease in Southern African bushpigs (Potamochoerus porcus) and warthogs (Phacochoerus aethiopicus). J Wildl Dis 1989;25(1):66–9. [29] Somers MJ. Warthog (Phacochoerus aethiopicus). In: Mills G, Hes L, editors. The complete book of Southern African mammals. Cape Town (South Africa): Struik Publishers; 1997. p. 247. [30] Bowland JM, Bowland AE. Bushpig (Potamochoerus porcus). In: Mills G, Hes L, editors. The complete book of Southern African mammals. Cape Town (South Africa): Struik Publishers; 1997. p. 245. [31] MacLeod CD. Species recognition as a possible function for variations in position and shape of the sexually dimorphic tusks of Mesoplodon whales. Evolution 2000;54(6):2171–3. [32] Robinson PT, Schmidt M. Dentistry in zoo animals: dental diseases of elephants and hippos. In: Fowler ME, editor. Zoo and wild animal medicine. 2nd edition. Philadelphia: WB Saunders Co.; 1986. p. 534–47.

G. Steenkamp / Vet Clin Exot Anim 6 (2003) 689–725

721

[33] MacDonald AA. The babirusa (Babyrousa babyrussa). In: Oliver WLR, editor. Status survey and conservation action plan: pigs, peccaries and hippos. Gland (Switzerland): IUCN; 1993. p. 161–71. [34] Koffler B. Peccary (Collared Paeccary: Tayassu tajacu). Available at: http://www.csam. montclair.edu/ceterms/mammals/peccary.html. Accessed November 17, 2002. [35] Carwardine M, Camm M. Narwhal and beluga. In: Carwardine M, editor. Whales, dolphins and porpoises. The visual guide to all the world’s cetaceans. London: Dorling Kindersley; 1995. p. 90–9. [36] King JE. Walrus. In: King JE, editor. Seals of the world. Oxford, UK: Oxford University Press; 1983. p. 65–72. [37] Kroese M. Order Sirenia. In: Mills G, Hes L, editors. The complete book of Southern African mammals. Cape Town (South Africa): Struik Publishers; 1997. p. 330. [38] Bloomer P. Order Hyracoidea. In: Mills G, Hes L, editors. The complete book of Southern African mammals. Cape Town (South Africa): Struik Publishers; 1997. p. 228. [39] Davie R. Family Procaviidae. In: Mills G, Hes L, editors. The complete book of Southern African mammals. Cape Town (South Africa): Struik Publishers; 1997. p. 229. [40] Fagan DA, Oosterhuis JE, Roocroft A. Captivity disorders in elephants: impacted molars and broken tusks. Zool Garten NF 2001;71(5):281–303. [41] Laws RM. Age criteria for the African elephant Loxodonta a. africana. E Afr Wildl J 1966;4:1–37. [42] Hooijer DA. Remarks upon the dentition and tooth replacement in elephants. Netherlands J Zool 1980;30(3):510–5. [43] Krumrey WA, Buss IO. Age estimation, growth and relationships between body dimensions of the female African elephant. J Mammol 1968;49(1):22–31. [44] Sikes SK. The African elephant, Loxodonta africana: a field method for the estimation of age. J Zool London 1967;154:235–48. [45] Sikes SK. The energy exchange systems of the body: I. In: The natural history of the African elephant. London: Weidenfeld & Nicholson; 1971. p. 76–112. [46] Miles AW, Grigson C. Variations and disturbances of eruption. In: Colyer’s variations and diseases of the teeth of animals, Revised edition. Cambridge, UK: Cambridge University Press; 1990. p. 331–54. [47] Hanks J. Growth of the African elephant (Loxodonta africana). E Afr Wildl J 1972;10:251–72. [48] Weatherford HL. Some observations on the tusks of an Indian elephant - the innervation of the pulp. Anat Rec 1940;76(1 Suppl):81–93. [49] Fagan DA, Benirschke K, Simon JHS, et al. Elephant dental pulp tissue: where are the nerves? J Vet Dent 1999;16(4):169–72. [50] Mikota SK, Lee Seargeant E, Ranglack GS, et al. Dentistry. In: Mikota SK, Lee Seargeant E, Ranglack GS, editors. Medical management of the elephant. West Bloomfield, Michigan, MI: Indira Publishing House; 1994. p. 87–94. [51] Kwon S-w., Hwang B-T, Lee G-h., et al. Repair of a fractured tusk in an Asian elephant by pulp capping. Korean J Vet Clin Med 1996;13(2):208–11. [52] Reichard T, Heinrichs P, Lentz T. African elephant tusk repair. In: Proceedings of the 1989 Exotic Animal Dentistry Conference. Milwaukee, WI; 1986, p. 79–81. [53] Korneewa W, Chromow W. Tusk prosthesis for an elephant. Erkrankgunender Zootiere 1988;30:349–51. [54] Steenkamp G, Hornsveld M. Elephant tusks-clinical anatomy/embryology and treatment options: a literature review. In: Proceedings of the Sixth World Veterinary Dental Congress. Hobart; 1999. [55] Stringer BG. Case report. The removal of a tusk in an African elephant. In: Proceedings of the Annual Meeting of the American Association of Zoo Veterinarians. 1972. p. 271–2. [56] Wallace C, Woodle K, Doyle C, et al. Making cast metal bands for an Asian elephant’s (Elephas maximus) tusks. In: Proceedings of the American Association of Zoo Veterinarians. Calgary, p. 6–8.

722

G. Steenkamp / Vet Clin Exot Anim 6 (2003) 689–725

[57] McGavin MD, Walker MS, Schroeder EC, et al. Death of an African elephant from probable toxemia attributed to chronic pulpitis. J Am Vet Med Assoc 1983;183: 1262–73. [58] Braswell LD, McManamon R. Tusk fracture in a young African elephant. In: Proceedings of the 1989 Exotic Animal Dentistry Conference. Milwaukee: 1986. p. 35–7. [59] Wagner RA, Bentz GH. An African Elephant tusk pulpotomy: a conservative approach. In: Proceedings of the American Association of Zoo Veterinarians. Calgary: 1991, p. 1–5. [60] Bush M, Heese D, Gray C, et al. Surgical repair of tusk injury (pulpectomy) in an adult male forest elephant (Loxodonta cyclotis). J Am Dent Assoc 1976;93:372–5. [61] Wyatt JD. Medical treatment of tusk pulpitis in an African elephant. J Am Vet Med Assoc 1986;189(9):1193. [62] Reichardt T, Lantz T, Heinrichs P. Update on 1986 African elephant tusk repair at Toledo zoo. In: Proceedings of the 1989 Exotic Animal Dentistry Conference. Milwaukee, WI; 1989. p. 85. [63] McCrae D. Cooper lab technician tackles a titanic tooth problem. Dent Lab Rev 1984;May:23–4. [64] Scheels JL. Treatment of dental injuries in a warthog. J Vet Dent 1999;16(2):82. [65] Bartsch RC, Frueh RJ. Alveolitis and pulpitis of a canine tooth in a walrus. JAVMA 1971;159(5):575–7. [66] Willis GJ, Proudfoot J, Ramer J. Placement of protective metal crowns on the tusks of captive pacific walrus (Odobenus rosmarus divergens). In: Proceedings of the American Association of Zoo Veterinarians Zoo Dentistry Symposium. Milwaukee, 2002. [67] Kertesz P, Harrison JD. The treatment of infected tusks in a collection of pacific walrus (Odobenus rosmarus). In: Proceedings of the American Association of Zoo Veterinarians Zoo Dentistry Symposium. Milwaukee, 2002. [68] King JE. Pathology and pollution. In: King JE, editor. Seals of the world. Oxford, UK: Oxford University Press; 1983. p. 205–7. [69] Schaftenaar W. Treatment of a fractured tusk in a male babirusa (Babyrousa babyrussa) using a polyoxymethylene bolt. J Zoo Wildl Med 1991;22(3):364–6. [70] Gro¨ning K, Saller M. Anatomy of an ancient giant. In: Gro¨ning K, editor. Elephants, a cultural and natural history. Gu¨tersloh: Ko¨nemann Verlagsgesellschaft mbH; 1999. p. 56–79. [71] Raubenheimer EJ. Development of the tush and tusk and tusklessness in African elephant (Loxodonta africana). Koedoe 2000;43(2):57–64. [72] Jachman H, Berry PSM, Imae H. Tusklessness in African elephants: a future trend. Afr J Ecol 1995;33:230–5. [73] Owen-Smith N. The incidence of tuskless elephant in Mana Pools game reserve. Afr Wildl 1966;20:69–73. [74] Janssen J. Eruption of an impacted tusk of a female African elephant. In: Proceedings of the 1989 Exotic Animal Dentistry Conference. Philadelphia, 1989. [75] Gass H. Komplikation beim Stobzahndurchbruch bei einem Afrikanischen elefanten (Loxodonta africana). Kleintierpraxis 1987;32:387–8. [76] Miles AW, Grigson C. Overgrowth of teeth. In: Colyer’s variations and diseases of the teeth of animals, revised edition. Cambridge (UK): Cambridge University Press; 1990. p. 355–69. [77] Miles AW, Grigson C. Injuries of the teeth. In: Colyer’s variations and diseases of the teeth of animals, Revised edition. Cambridge (UK): Cambridge University Press; 1990. p. 394–436. [78] Taylor RMS. Dental evidence of survived calamities in wild animals. J Dent Assoc S Afr 1988;43:553–6. [79] Colyer F. The pathology of the teeth of elephants. The Dental Record 1926;46(1):1–15. [80] Miller WD. Studies on the anatomy and pathology of the tusks of the elephant. The Dental Cosmos 1890;32(7):505–26.

G. Steenkamp / Vet Clin Exot Anim 6 (2003) 689–725

723

[81] Cook RA, Klein L, Welsch BB, et al. Tusk regrowth following surgical removal in a female pacific walrus (Odobenus rosmarus divergens). In: Proceedings of the 1989 Exotic Animal Dentistry Conference. Milwaukee, 1989. [82] Miles AW, Grigson C. Orders Pinnipedia and Cetacea. In: Colyer’s variations and diseases of the teeth of animals, revised edition. Cambridge (UK): Cambridge University Press; 1990. p. 95–105. [83] Wiggs RB, Lobprise H. Exotic animal oral disease and dentistry. In: Wiggs RB, Lobprise H, editors. Veterinary dentistry: Principles & Practice. Philadelpia: Lippencot-Raven; 1997. p. 538–58. [84] James SB, Cook RA, Raphael BL, et al. Immobilization of babirusa (Babyrousa bybyrussa). J Zoo Wildl Med 1999;30(4):521–5. [85] Brown DH, Asper ED. Further observations on the Pacific walrus (Odobenus rosmarus divergens) in captivity. International Zoo Yearbook 1962;6:78–82. [86] Hagenbeck C-H. Notes on walruses, Odobenus rosmarus, in captivity. International Zoo Yearbook 1962;4:24–5. [87] Brown DH. The health problems of walrus calves, and remarks on their general progress in captivity. International Zoo Yearbook 1962;4:13–23. [88] Miles AEW. Healed injuries of elephant tusks. BDJ 1972;133:395–400. [89] Von Metnitz J. Osteodentine, vasodentine and abscess cavities in dentine. Quart Circ 1903;Sept.:289–304. [90] Humphreys HF. Particulars relating to the broken tusk of wild Indian elephant. BDJ 1926;47:1400–1. [91] Cohen S. Diagnostic procedures. In: Cohen S, Burns RC, editors. Pathways of the pulp, 7th edition. Mosby, MO: St Louis; 1998. p. 1–19. [92] Kuntze A. Oral and nasal disorders of elephants. In: Fowler ME, Miller RE, editors. Zoo and wild animal medicine - Current therapy 4. Philadelphia: WB Saunders Company; 1999. p. 544–6. [93] Briggs M, Schmidt M, Black D, et al. Extraction of an infected tusk in an adult African elephant. JAVMA 1988;192(10):1455–6. [94] Colyer F, Miles AEW. Injury to and rate of growth of an elephant tusk. J Mammal 1957;38(2):243–7. [95] Miller WD. Studies on the anatomy and pathology of the tusks of the elephant. The Dental Cosmos 1891;33(6):421–40. [96] Kertesz P. The principles of elephant tusk therapy. In: Proceedings of the Fifth World Veterinary Dental Congress. Birmingham; 1997. p. 195–8. [97] Legendre LFJ. Vital pulpotomy of the broken tusk of an Indian elephant. J Vet Dent 1993;10(4):10–1. [98] Willis GJ, Proudfoot J, Ramer J. Pulpal treatment and restoration of a fractured tusk of an African elephant (Loxodonta africana). In: Proceedings of the American Association of Zoo Veterinarians Zoo Dentistry Symposium. Milwaukee, 2002. [99] Reichardt T, Red Fox D, Shellabarger W, et al. Medical and surgical treatment of tusk pulpitis in an African elephant. J Vet Dent 1989;6(3):20. [100] Allen JL, Welsch B, Jacobson ER, Turner TA, Tabeling H. Medical and surgical management of a fractured tusk in an African elephant. JAVMA 1984;185(11): 1447–9. [101] Van Foreest A. Considerations in the clinical application of dental adhesive materials/ techniques in zoo animals. In: Proceedings of the American Association of Zoo Veterinarians. Calgary: 1991. p. 15–8. [102] Gardner HM, Barr JW, Spellmire TJ. Fractured tusk on a male African forest elephant. In: Proceedings of the 1989 Exotic Animal Dentistry Conference. Milwaukee, 1986. p. 56–60. [103] Clark TJ. Successful application and outcome of a direct pulp cap in a Malaysian elephant. In: Proceedings of the American Association of Zoo Veterinarians Zoo Dentistry Symposium. Milwaukee: 2002.

724

G. Steenkamp / Vet Clin Exot Anim 6 (2003) 689–725

[104] Zoodent International. Recent cases, case 2: Asian Bull Elephant - Kiev Zoo 1998. Available at: http://www.zoodent.com/cases2.htm. Accessed October 8, 1998. [105] Spa˚ngberg LSW. Instruments, materials and devices. In: Cohen S, Burns RC, editors. Pathways of the pulp, 7th edition. St Louis: 1998, p. 476–531. [106] Welsch B. Dental problems in young African elephants. In: Proceedings of the 1986 Exotic Animal Dentistry Conference. Milwaukee: 1986, p. 53–5. [107] Welsch BB. Tusk extraction simplified. In: The 1989 Exotic Animal Dentistry Conference. Milwaukee: 1989, p. 22, 23. [108] Cornell LH, Antrim JE. Anesthesia and tusk extraction in walrus. J Zoo Ann Med 1987;18(1):3–6. [109] Harvey CE, Penny RHC. Oral and dental disease in pigs. In: Harvey CE, editor. Veterinary dentistry. Philadelphia: WB saunders company; 1985. p. 272–80. [110] Stannus HS. Diseases of elephant tusks. Lancet 1911;March 4:617. [111] Wiggs RB, Lobprise H. Oral surgery. In: Wiggs RB, Lobprise H, editors. Veterinary dentistry: principles and practice. Philadelpia: Lippencot-Raven; 1997. p. 232–58. [112] Lateur N, Kusse G, van der Velden M, et al. Extraction of an infected tusk in a male Indian elephant. Presented at the 25th Anniversary Symposium of the British Veterinary Biological Society. April 18–20, 1986. [113] Welsch B, Jacobson ER, Kollias G, et al. Tusk extraction in the African elephant (Loxodonta africana). J Zoo Wildl Med 1989;20(4):446–53. [114] Steiner M, Gould AR, Clark TJ, et al. Elephant tusk removal. In: Proceedings of the American Association of Zoo Veterinarians Zoo Dentistry Symposium. Milwaukee: 2002. [115] Steenkamp G, Crossley DA. Incisor tooth regrowth in a rabbit following complete extraction. Vet Rec 1999;16(2):65–8. [116] Bodegom JC, van der Linden PGM. Tooth formation and eruption in the miniature pig. Am J Orthod 1969;56(6):622–3. [117] Horkwitz LK, Davidovitz G. Dental pathology of wild pigs (Sus scrofa) from Israel. Isr J Zool 1992;38:111–23. [118] Miles AW, Grigson C. Dento-alveolar abscess. In: Colyer’s variations and diseases of the teeth of animals, revised edition. Cambridge, UK: Cambridge University Press; 1990. p. 506–20. [119] Penny RC, Mullen PA. Atrophic rhinitis of pigs: abattoir studies. Vet Rec 1975;96:518–21. [120] Davies ZE, Guise HJ, Penny RH, et al. Effects of stone chewing by outdoor sows on their teeth and stomachs. Vet Rec 2001;149:9–11. [121] Barker IA, van Dreumel AA, Palmer N. The alimentary system. In: Jubb KVF, Kennedy PC, Palmer N, editors. Pathology of the domestic animals, 4th edition, Vol. 2. San Diego (CA): Academic Press Inc; 1991:1–30. [122] Andrews AH. Dental caries in an experimental domestic pig. Vet Rec 1973;94:257–8. [123] Miles AW, Grigson C. Caries of the teeth. In: Colyer’s variations and diseases of the teeth of animals, Revised edition. Cambridge: Cambridge University Press; 1990. p. 455–85. [124] Schaler K. Delayed dentition of an Indian elephant causing obstipation and colic. Dtsch tiera¨rztl Wschr; 88:393–448. [125] Reichard TA, Ullrey DE, Robinson PT. Nutritional implications of dental problems in elephants. In: Proceedings of the American Association of Zoo Veterinarians 1982. p. 73–4. [126] Samuel JL, Woodall PF. Periodontal disease in feral pigs (Sus scrofa) from Queensland, Australia. J Wildl Dis 1988;24(2):201–6. [127] Van Foreest. Veterinary dentistry in zoo and wild animals. In: Fowler ME, editor. Zoo and wildlife medicine. 3rd edition. Philadelphia: WB Saunders Co.; 1993. p. 263–8. [128] Raubenheimer EJ, van Heerden WFP, Turner ML, et al. Odontoma in an African elephant. J S Afr Vet Assoc 1989;60(3):149–50. [129] Lindeque M. Dentition and age estimation of elephants in the Etosha National Park, Namibia. Madoqua 1991;18(1):17–25.

G. Steenkamp / Vet Clin Exot Anim 6 (2003) 689–725

725

[130] Lateur N, Kusse G, van der Velden M, Stolk P. Surgical management of traumatic pulpitis of the tusks in a male Indian elephant. In: Proceedings of the American Association for Zoo Veterinarians. 1985; p. 125–6. [131] McManamon R, Braswell L. Tusk fracture in a young African elephant. J Vet Dent 1989;6(3):18. [132] Nowotny F. Ein durch zahnverlagerung verursachter abseb imcavum nasi eines schweines. In: Kongresse und wissenschaftliche Organisationen. Wien: 1965. p. 867–70.