Nonhuman Primate Dental Care

Topics in Medicine and Surgery

Nonhuman Primate Dental Care Cathy A. Johnson-Delaney, DVM, Dip. ABVP (Avian)

Abstract Nonhuman primates require, at minimum, annual dental examination, cleaning, and prophylactic care. Sedation is necessary for examination and may be extended into full anesthesia should dental conditions require oral surgery. Because there is a potential zoonotic disease risk during dental procedures, personal protective equipment should include masks, double gloving, face shields, and goggles. Dental disease commonly treated in nonhuman primates includes tartar and calculus, gingivitis, fractures and caries, periodontal disease, abscesses, and osteomyelitis. Ethical considerations of canine tooth reduction will also be discussed. Copyright 2008 Elsevier Inc. All rights reserved. Key words: monkey; primate; dental disease; dental prophylaxis; calculus; gingivitis; abscess; fistula; caries

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onhuman primates (NHPs) present a challenge to the clinician not only in regard to the different dentition between species of primate, but also because of potential zoonotic disease and safety issues inherent to oral procedures. The dental formula for New World monkeys (Cebidae) is 2(I2/2, C1/1, P3/3, M3/3).1 The formula for Old World monkeys is 2(I2/2, C1/1, P2/2, M3/3) (Fig 1, Table 1).1 Normal times for tooth eruption of selected primates are presented in Table 2.2-4 NHPs rarely allow dental examination without sedation, which may be extended into general anesthesia and analgesia, especially if immediate procedures are required.5 Dental disease presentations are similar to those encountered in traditional pet practice, and include accumulation of tartar and calculus, gingivitis, fractures and caries, periodontal disease, abscesses, and osteomyelitis (Fig 2). The periodontal bone in the Callitrichidae (e.g., marmosets, tamarins) is highly sensitive to generalized metabolic changes such as metabolic bone disease.5,6 Diagnosis and treatment regimens also follow dental plans used in most carnivore/omnivore species and can be easily adapted to the different dentition. Follow-up home care is problematic, therefore the NHP patient requires at least annual preventive dental examination and cleaning.

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Oral Health Considerations NHPs kept in private settings occasionally present for treatment of dental disease and prophylaxis. However, a more common request is for removal of teeth in an effort to reduce human injury from monkey bites. The canine teeth of many male NHP species are as large as and even sharper than the canine teeth in large-breed dogs (Fig 3). NHPs are nondomesticated animals and use biting as one method of asserting social rank. Unfortunately, humans do not have the thick skin characteristic of most monkeys and do not use biting as a method to determine hierarchy. Consequently, such behavior from monkeys to humans is extremely undesirable and dangerous. The potential for infliction of severe From the Eastside Avian and Exotic Animal Medical Center, Kirkland, WA USA. Address correspondence to: Cathy A. Johnson-Delaney, DVM, Dip. ABVP (Avian), Eastside Avian and Exotic Animal Medical Center, 13603 100th Ave NE, Kirkland, WA 98034. E-mail: [email protected]. © 2008 Elsevier Inc. All rights reserved. 1557-5063/08/1702-$30.00 doi:10.1053/j.jepm.2008.03.012

Journal of Exotic Pet Medicine, Vol 17, No 2 (April), 2008: pp 138 –143

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Figure 1. Dental chart of teeth in Old World NHPs (author drawn).

bite wounds is a primary reason for the unsuitability of primates as pets. This author’s rule: monkeys bite, they bite quickly and hard, and they will always bite even if their owners swear they do not. Extraction of healthy teeth to prevent injury from monkey bites is not recommended. The American Veterinary Medical Association (AVMA) has recently published a Dental Surgery Position Statement for captive NHPs or exotic and wild (indigenous) carnivores: The AVMA is opposed to removal or reduction of canine teeth except when required for medical treatment or scientific research approved by an institutional animal care and use committee. The primate mouth also contains many types of bacteria that may cause infection in humans.7,8 Care must be taken during oral examination and dental procedures to protect the clinical staff from potential zoonotic disease, most notably B virus (Cercopithecine herpesvirus 1, Herpes B) in macaques. In the macaque, shedding is intermittent and frequently occurs without evidence of typical lesions

(e.g., canker sores, oral ulcers, conjunctivitis, “cold sores” on lips). Serologic testing in macaques is not a reliable indicator of carrier status, although culture of oral and conjunctival swabs may indicate whether the virus is being shed at the time of sampling. Positive identification of carrier status usually requires viral isolation from the dorsal root ganglia or trigeminal or facial nerve, which is not possible on a live animal. Practitioners should consider all macaques to be B-virus positive and use appropriate protective clothing and procedures to protect themselves and staff from potential exposure. Should a bite, scratch, or splash of bodily fluids onto mucous membranes of a human occur, the guidelines issued by the National B-virus Resource Center (www2.gsu.edu/ ⬃wwwvir) should be followed. These are listed in Table 3. Shigella infection may manifest as severe gingivitis with or without diarrhea.7,8 NHPs require vitamin C in their diets. Those fed commercial primate biscuits used within the expiration dates and supplemented with fresh produce will rarely have gingival inflammation with hemorrhage and loosening of the teeth due to deficiencies. However, some pet monkeys may have various nutritional deficiencies, and vitamin C deficiency should be considered when oral lesions consistent with scurvy are present.8,9

Prophylactic Care Ideally, for an NHP, an annual dental examination and prophylaxis should be performed.9 The author recommends wearing a moisture-resistant mask (8710 Dust & Mist Respirator; 3M, Corp., St. Paul, MN USA), eye protection, face shield, and double gloves when performing dental procedures in NHPs. A complete dental workup should include radiographs, preferably with intraoral techniques. However, full head radiographs with oblique angles chosen to highlight tooth roots are acceptable. The NHP dental examination should include an evalua-

Table 1. Dental formulas of different species of primates.1-3 All formulas are 2ⴛ(n) Primates

Incisors

Canines

Premolars

Molars

Total Teeth

Lemuridae (lemurs) Cebidae (New World monkeys) Callitrichidae (New World; marmosets, tamarins) Cercopithecidae (Old World monkeys) Pongidae (great apes)

2/2 2/2 2/2

1/1 1/1 1/1

3/3 3/3 3/3

3/3 3/3 2/2

36 36 32

2/3 2/2

1/1 1/1

2/2 2/2

3/3 3/3

34 32

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Table 2. Age in years by permanent tooth eruption in 3 species of macaques and the common baboon1-3

Tooth First molar Central incisor Lateral incisor Second molar First premolar Second premolar Canine Third molar

Macaca fascicularis Max Man

M. mulatta Max Man

M. nemestrina Max Man

Papio cynocephalus Max Man

1.7 2.8 3.4 3.8 4.3 4.4 5.3 6.8

1.5 2.5 2.8 3.4 3.7 3.8 4.2 5.8

1.4 2.25 2.5 3.1 3.8 3.8 3.3 5.3

1.6 2.6 3.1 3.5 3.6 3.8 3.9 6.1

1.7 2.7 2.9 3.8 4.6 4.6 4.8 6.2

1.4 2.5 2.6 3.2 3.9 3.8 4.0 5.5

1.4 2.25 2.5 3.1 3.7 3.8 3.2 5.3

1.5 2.6 2.8 3.3 3.9 3.8 3.8 6.0

Macaca fasicularis (common names: Longtailed, Crab-eating, Java, or Cynomolgus), Macaca mulatta (common name: Rhesus), Macaca nemestrina (common name: Pigtail), Papio cynocephalus (common name: Savannah baboon). Abbreviations: Max ⫽ maxillary; Man ⫽ mandibular.

tion of each tooth, and periodontal and gingival assessment with a dental probe to determine depth of the periodontal pocket (Fig 4). Prophylaxis should include the removal of tartar, stain, plaque, treatment of caries, and polishing of tooth surfaces and fluoride treatment to repair and strengthen the enamel. The author prefers hand-scaling of the teeth with manual root planing. Ultrasonic scaling can aerosolize oral pathogens and is not recommended. Treatment of caries is straightforward. Areas of tooth necrosis are removed with high-speed dental equipment, dried, and prepared with a commercial veterinary composite restoration kit.

Figure 2. Adult female macaque (Macaca fascicularis) with calculus, gingivitis, fractured incisors, and excessive wear of both premolars and premolars.

Dental Procedures Elective Coronal Reduction of Canine Teeth Coronal reduction or “blunting” of the canine teeth in males is an acceptable procedure to reduce the severity of injury to humans or other monkeys and is still a common laboratory animal procedure. However, it must be understood that blunting in no way

Figure 3. Adult male macaque (Macaca fascicularis) mouth. Note mandibular canines have been cut and pulpotomy performed.

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Table 3. B virus incident protocol A. Bite or scratch from any potential B-virus–carrying monkey (most commonly macaques) Human: Scrub the wound for 15 min with a soft brush or paper towel and copious amounts of water. If the wound is bleeding profusely, direct pressure should be applied and emergency medical care sought. Inform the medical professionals that the wound was inflicted by a macaque, and that B virus protocol should be followed. The B virus laboratory can be consulted for care of the serious wound. After cleaning the wound, it should be swabbed for viral culture and submitted along with a serum sample at the time of the incident, and again in 2 weeks. Macaque: The macaque should have 3 swabs taken for viral culture: 1 from each conjunctival pouch and 1 from the buccal surfaces of the mouth. A serum sample should be submitted with the culture swabs to the B virus lab, along with a follow-up serum sample in 2 weeks. B. Splash of any macaque body fluids into eyes, nose, mouth (mucous membrane exposure) Human: Flush mucosal surface with saline solution for 15 min, then report to a medical facility for sampling as above. Macaque: Samples (culture and serology) as listed above. Contact B-virus Resource Center (www2.gsu.edu/⬃wwwvir) for instructions and testing submission forms.

prevents a monkey from biting. Simple blunting can be accomplished in the anesthetized and intubated monkey with a finishing cone on a low-speed dental drill. Care must be taken to keep the tooth tip cool to prevent thermal damage to the pulp. The canine teeth of many male monkeys will not remain blunt after coronal reduction: normal occlusion of the canines acts to sharpen the teeth, and repeated procedures are often required. It should also be noted that as the male ages, the canine teeth become smaller in diameter from repeated wearing and selfsharpening.

Figure 4. Dental probe is used to check periodontal pockets and gums. This is an adult male Celebes macaque (Macaca nigra).

Primate canine teeth are similar to those in carnivores in structure, in that the root is often as large as the visible crown. Any reduction of the primate canine teeth that results in exposure of the pulp cavity may result in pathologic dental disease and pain. If pathologic dental disease takes place, additional procedures such as pulpotomy, root canal, or extraction will be required. An alternative technique to simple coronal reduction is amputation with pulpotomy, which effectively eliminates the potential for resharpening of canine teeth. The tooth surface should be cleansed with a dilute chlorhexidine rinse (Chlorhexidine Oral Rinse; Henry Schein Inc., Melville, NY USA). The tooth is amputated with a dental disk at approximately the occlusal surface level of the incisors and premolars (Fig 5, A). Vital pulp is then drilled with a high-speed cylindrical diamond burr (#557-7, Star Diamond; Henry Schein, Inc.) to approximately the depth of the bur itself, or approximately 3 to 5 mm (depending on the size of the tooth) (Fig 5, B). Care must be taken to keep the pulp and tooth cool. This procedure creates a pulpal access cavity within the pulp chamber (Fig 5, C). The drilled cavity should be air-blown dry to remove any debris. Sterile dental points are inserted to further dry the pulp cavity and stop hemorrhage (Fig 5, D). A small amount of calcium hydroxide (calcium hydroxide paste, Henry Schein, Inc.) is then packed into the pulp cavity (Fig 5, E). Excess paste is removed with a no. 35 inverted cone-shaped diamond burr (#805-018, Henry Schein, Inc.). This leaves a base of approximately 1 to 2 mm over the pulp (Fig 5, F). The no. 35 burr is

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Figure 5. Elective coronal reduction of the right maxillary canine tooth in adult male Macaca nemestrina. A, Note the protective welder’s glove used to prevent punctures from the instrument and intact canine teeth. B, Drilling the pulp and measuring depth of drilling. C, Open pulp cavity after drilling. D, Sterile paper points inserted to stop bleeding of pulp cavity. E, Calcium hydroxide paste applied to dried pulp cavity. F, Filled pulp cavity with ceramic composite. G, Finished tooth after polishing of surface.

then used to undercut the walls of the pulpal access cavity slightly to allow retention of the ceramic. The cavity is then filled with a ceramic dental filling material (many types available) and allowed to cure according to manufacturer’s instructions. The surface is then gently polished to smooth the material (Fig 5, G). Radiographs can be taken at the completion of the procedure to evaluate and document the periapical region of the filled teeth. Annual dental radiographs should be taken to evaluate the teeth and viability of the roots. Pulpotomy of the healthy canine tooth is currently under debate, because over time many of these teeth eventually require root canal or extraction because of inadvertent damage to pulp during the procedure.10 Other endodontic procedures in NHPs are similar to those in other species. Dental burrs and materials suitable for large-breed dogs are usually sufficient to complete the endodontic procedure. Anesthetic blocking of the tooth root or area is recommended in addition to systemic analgesics and anesthesia.

calculus are discussed above under prophylactic care.

Dental Abscesses Tooth root abscesses may present with swelling of the cheek or jaw, and are treated similarly to those encountered in canine and feline patients. Maxillary abscesses also may involve the sinuses and nasal tissues (Figs 6 and 7). Treatment involves lancing the abscess and removing purulent material and necrotic tissue, flushing of the site and irrigating fistulous tracts if present, removing diseased teeth and bone, and administration of systemic antibiotics.

Treatment of Gingivitis and Periodontal Disease Gingivitis, periodontal disease, and dental abscesses present as they do in other species. Caries are common, particularly if animals are fed human foods that are high in sugars. Plaque and calculus are also common. In many species, the incisors tend to accumulate plaque and calculus at a greater rate than the premolars and molars. Treatment of plaque and

Figure 6. Abscessed canine tooth. Injection of saline solution into the open central cavity produced drainage of exudates at the gum line.

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Figure 7. A, Male Macaca nemestrina with a draining facial fistula (arrow) from a necrotic canine tooth that had been cut and left open without filling. B, Flushing of the fistula with saline solution to illustrate patency.

Extraction of Diseased Teeth For the extraction of a diseased tooth, local anesthetic blocking of the tooth root area is performed, followed by gingivectomy. The periodontal ligaments are severed. In cases where there is accompanying osteomyelitis and/or infection, the surrounding bone may be adherent to the tooth structures and will require gentle and patient manipulation to loosen the tooth. Care needs to be taken not to damage surrounding tooth roots. When loosened, the tooth should be elevated and extracted. Because there is usually a large space remaining after the tooth is extracted, use of matrix material such as Consil Bioglass (Nutramax Laboratories, Baltimore, MD USA) can be packed into the cavity.11 The gums are then sutured loosely over the cavity to not only hold the material in, but prevent accumulation of food debris. Because osteomyelitis is often present, treatment for inflammation must be added to the antimicrobial regimen. Nonsteroidal antiinflammatory medications such as meloxicam (Metacam; Boerhinger Ingleheim, Ridgefield, CT USA) at 0.2 mg/kg orally once daily not only decrease inflammation, but also provide analgesia.

Preventive Care The maintenance of healthy teeth may include the use of monkey chow that incorporates sodium hexametaphosphate (PMI Dental Primate Chow; PMI Feeds, St Louis, MO USA) or the regular provision of tartar-control products manufactured as treats for dogs and coated with sodium hexametaphosphate.12 Toys designed for dogs to decrease plaque accumulation are also helpful for NHPs when chewed. Some

NHPs can be taught to use a toothbrush and will brush their teeth like humans. When that is not possible, a good diet and twice yearly dental cleaning are recommended to keep the mouth healthy.

References 1. 2. 3. 4. 5. 6. 7. 8. 9. 10.

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Wiggs RB, Hall B: Nonhuman primate dentistry. Vet Clin Exotic Anim 6:661-687, 2003 Swindler DR: Primate Dentition: An Introduction to the Teeth of Non-Human Primates. New York, NY, Cambridge University Press, 2002, pp xv-296 Swindler DR: Dentition of Living Primates. New York, NY, Academic Press, 1976, pp xvii-308 Hurme VO: Estimation of monkey age by dental formula. Ann N Y Acad Sci 85:795-799, 1960 Williams CSF: Nonhuman primates, in Williams CSF (ed): Practical Guide to Laboratory Animals. St Louis, MO, CV Mosby Co, 1976, pp 129-141 Potkay S: Diseases of the Callitrichidae. A review. J Med Primatol 21:190-236, 1992 Whitney RA, Johnson DJ, Cole WC: Laboratory Primate Handbook. New York, NY, Academic Press, 1973 Ruch TC: Diseases of the mouth and teeth, in Ruch TC (ed), Diseases of Laboratory Primates. Philadelphia, PA, WB Saunders, 1959, pp 42-75 Johnson-Delaney CA: Primates. Vet Clin North Am Small Anim Pract 24(1):121-156, 1994 Coman JL, Fortman JD, Alves ME, Bunte RM, Bennett BT: Assessment of a canine crown reduction technique in nonhuman primates. Contemp Top Lab Anim Sci 37(4):67-72, 1998 Wilson J, Low SB: Bioactive ceramics for periodontal treatment: comparative studies in the patus monkey. J Applied Biomaterials 3:123-129, 1992 Emerson CL, Johnson-Delaney C, Persson R: Effects of sodium hexametaphosphate on dental calculus formation in Cynomolgus macaques (Macaca fascicularis). Lab Animal Sci 47(4):451, 1997