Periodontal disease (PD) is one of the most common problems in oral pathology of Equidae around the world, with prevalence reported from 13 to 76%. The objective of this article is to describe oral clinical findings and estimate risk factors (diet, breed, age, and presence of maloclussions). 89 horses of four different breeds (Chilean pure breed:36; Arabians:7; Jumpers:39 and Thoroughbreds:7) were subjected to dental examinations by one single veterinarian and separated in two groups (43 healthy; 46 periodontitis). Oral examinations were performed under sedation (Detomidine 0,1 mg/Kg), full mouth speculum (Millenium), mirror and periodontal probes. Dental pathologies were registered and considered like quantitative variables (depth and width of periodontal pockets), discrete quantitative variables (most frequent diastema location) and qualitative variables (peripheral cementum staining, gingival appearance, requirement of radiographic exams, and presence of other dental pathologies). All data were analyzed through central trend statistics and OR (Odds ratio). The most frequent diastema location was observed in between dental element 310 (with 311 or 309). The most relevant clinical oral findings in PD group were peripheral cementum staining (78%), diastema presence (36%) and peripheral caries (21%). 26 horses (56,5%) were classified as mild periodontitis (Grade 1). 8 horses (17,4%) were recommended for dental radiographs in this study.
The Odds value (Risk factors) for each variable shows significance for age (p=0,001), breed (p=0.024), and diastema presence (0,0016) in periodontitis group. Diet was not statistically significant (p=0.78). Breed data were statistically significant, jumping breeds (p=0,019), arabians (p=0,024) and racehorses (p=0,019), show low risk compared to Chilean pure breed. Like a conclusion Chilean horses have similar PD oral clinical findings to other studies, and it was possible to identified risk factors like age, breed, and diastema presence. We need soon larger horse population studies to achieve better understanding of diet involvement in periodontal disease.
Keywords
Horses, equine dentistry, periodontal disease, diastemas, risk factors.
Introduction
Periodontal disease (PD) affects most likely horses from 10 years and upward, and there is with few studies about his etiology, most likely associated to entrapment of food between cheek teeth, that differs of the tartar accumulation and immune response in humans and companion animals 6. Reports on the prevalence of PD in horses have shown 60% of prevalence in some parts of the world1. Other reports in the UK have shown a prevalence ranged between 13,9-38,6% 3,4. In Australia there is 22,3% of periodontal pockets and 13% of diastemas in molars17 .In South America, few studies have reported prevalence of PD, one in Chilean Pure Breed Horse, which is a small size breed specialized in rodeo and reining in Chile and some South American countries , with an estimate of 7% 2 and 11% 19 .In the criollo Colombian horse, there is one report of 1,3%24 , and in criollo horses in Brazil there is a report of 37% of gingivitis in incisors25 . In other Equidae like donkeys, PD can reach up to 76% of prevalence5
Periodontal disease can be one of the most painful conditions and can directly influence the body score condition, performance, and general health of equids13. The etiopathogenesis is associated with feed packed into interdental spaces (diastemas) , which can lead to inflammation of the gingiva and periodontal surrounding tissues by the action of acids and enzymes produced by anaerobic bacteria, some of them already described and isolated from horses 6. Diastemas development has been associated with primary dental problems (developmental, like rotation or misalignment of dental elements) and secondary (acquired, like malocclusions type I) 7.
To date, only a few reports have described the risk factors of PD, showing that increasing in age (p<0.001) and diastema presence (p<0.001) were associated with PD lessions4. Other reports have been researched into a positive association with peripheral caries12,27, and others have shown no association 4, no current studies have researched for the roles of breed and diet on periodontal disease in horses. In this study, the objective was to described PD lesions in horses of different breeds in Chile and to identify risk factors associated with PD.
Materials and method
Dental examinations were performed by one veterinarian in 89 (N:487; C:95%; α:0.005) horses
(40 females; 49 males) of four different breeds (Chilean pure breed:36; Arabians:7; Jumpers:39 and Thoroughbreds:7), between June 2021 and June 2023 in Metropolitan Central Region of Chile.
Two groups were created based on PD presence (46 Healthy and 43 Periodontal Disease group). Inclusion criteria considered horses over ten years of age and without receiving previous dental treatment. Oral examinations were performed under sedation (Detomidine 0,1 mg/Kg), full mouth speculum (Millenium), mirror and periodontal probes. Dental pathologies and PD grades were registered8,9. Later quantitative variables (Depth and width of periodontal pockets), discrete quantitative variables (Most frequent diastema location) and qualitative variables (Peripheral cementum staining, Gingival appearance, requirement of radiographic exams, PD grades and other dental pathologies) were analyzed trough central trend statistics. In the case of quantitative variables, normality was estimated through Shapiro-Wilk test10. Accordingly, to this median, rank, minimal and maximal value, kurtosis, and asymmetry (with confidence intervals) were stimated10.
The association between the dependent variable (PD or Periodontal disease) with the independents were estimated through logistic regression (OR α≤0,05) 10,11, based on PD is a dichotomic variable, and the independents are qualitative (dichotomic) and quantitative (continuous). The degree of association was measured by AIC (Akaike information criterion) and R2 value (Nagelkerke).
Results
From the total of 89 horses, gender was not statistically significant (p=0.78). The results of the clinical aspects in PD horses were detailed in Table 1, the distribution of Peripheral cementum staining, gingivitis, requirement of radiographic exams, PD grades and other dental pathologies. Periodontal pockets measures were between 8 and 3mm (Depth and width), which minimal and maximal values start from 5 to 18mm (Depth) and 1 to 8mm (width). Both values, symmetry (1,27 mm; SDe=0.35) and kurtosis (1,21; SDe=0.68) are far from cero and were normal value distribution, so they are representative for this study. About the distribution of most frequent diastema location, it was observed in 310 (with 311 or 309).
In table 2 are showing the results of the logistic regression that was applied for the risk factors, then R2 value (Nagelkerke) was 0,28 which means that independent variable can explain 28 % of the variance involving the PD (dependent variable), and AIC (Akaike information criterion) was 105,26. The Odds value for each variable shows significance for age (p=0,001) and breed (p=0.024), diet was not significant (p=0.78), and the presence of maloclussions was a constant (present in most of the horses studied).
Table 1 | Distribution of frequencies and percentages (central trend statistics) of peripheral cementum staining, gingivitis, requirement for dental radiographs, grades of periodontal disease, and other dental problems observed in the periodontal group horses.
1 grade 0 not included (no disease, less than 5mm of pocket depth), 1 (mild disease, 5 to 9mm),
2 (moderate disease 10 to 14mm) and 3 (Severe disease, more than 15mm) 9
2 Mal 1: malocclusion type 1 (focal overgrowths)
Table 2 | Results from the stimate of risk factors trough logistic regression (OR), for diet, age and breed (independent variables)
1 A: Alfalfa; A+C: Alfalfa plus concentrate; H: Wheat flour; H+A: Wheat flour plus alfalfa
2 CO: Continuous variable (years) between 10 and 22 (average 13,4)
3 CH: Chilean pure breed; ARA: Arabians; FSC: Thoroughbreds; SA: Jumping breeds
4 OR: Odds ratio
5 R2 0.2824133 (28%)
6 AIC= 105.26
*Significatives
Discussion
About the measures of periodontal pockets, matches with the degree 1 of periodontal disease (5 to 9mm of Depth), in which most of the cases undergo without clinical signs, that also was observed in this study13. Other studies consider it like “grade 0” or incipient disease (Gingivitis)4. In table 2 it also shows that PD grade 1 was the most frequent in the 46 horses. About the most frequent location, it was found in the mandibular arcade triadan 310/309, which agrees as well with other studies 4,6,7. Probably due to feed stasis by gravity in lower arcades, and more force during mastication cycles in caudal cheek teeth1. The clinical aspect of the gingiva and cementum it’s also matches with the degree of PD reported in this study like gingivitis and peripheral cementum staining (most brown or dark brown color) , this last one, nevertheless must be differentiated from peripheral caries, because some reports suggest a possible association with PD12,26. In our study was not observed, with only 10 from 46 horses with peripheral caries (21%), recent studies in UK has the same results4 . Diastemas was found in 17 horses of the PD group (37%), much higher to reports in Australia with 13%17 and 8,7% in UK highly associated to periodontal injury4, nevertheless there is other reports with more prevalence 38,6%3. The requirement for radiographic studies (Table 1) was suggested in 8 of 46 cases (17,4%), all grade 3 and some grade 2 PD. The most frequent radiographic finding was enlarged periodontal space (6 horses) and periapical lysis/sclerosis (2 horses). This also agrees with other reports that suggest the use of radiographs for more severe cases8,13, probably a good focus for future studies is to consider radiographical changes of interproximal and crestal bone in PD horses (authors opinion). About other dental pathologies present in the PD group was malocclusion type I, this has been widely researched as one of the most important possible risk factors, nevertheless in this study was a constant (84% Table 1, and with other dental abnormalities 100%). This agrees with several other reports6,8,9,23. The most frequent malocclusions type 1 were focal overgrowths (Sharp enamel points, hooks, and excessive transverse ridges). About the risk factors, diet was not statistically significant (p=0.23), and included two different categories: wheat flour alone plus wheat flour/alfalfa hay (H+H/A) with alfalfa hay alone plus alfalfa hay/concentrate (A+A/C). These are initial data, and must be understood like a projection of a large population study, other reports has been postulated that forage stasis and entrapment (alfalfa hay in this study) in diastemas could be the source of irritation and gum inflammation9, which later goes to fermentation and decomposition, participating like a mechanical damage, but also permitting the proliferation of gram negative anaerobe bacteria7, who increase the periodontium damage, this last action is very well researched in humans and small animals14,15. Age was statistically significant. The results show that when horse get one year older, increase1,4 times the possibility to develop PD (P=0,0010). This has been reported in other studies4, about 60% of the horses over 10 years can have PD16,17. In Chile 26% of the horses over 18 years can have PD, compared with a young horse’s group (between 4 and 9 years) that can obtain 2%2. Studies in donkeys over 30 years of age report prevalence of 76%5. This situation can be explained by the continuing eruption of horse’s teeth (Hypsodonts) and his eventual separation once the horse gets old (geriatric diastemas)17. This situation has been studied experimentally in horses over 15 years old, concluding that as less crown the horse has, higher loads in the periodontal ligament were detected18. Another theory that is not proven yet could be a lower local immune response at older ages, this situation was not researched in this study, but can be a good way for future projects, in this same context only has been reported the presence of toll-like receptors and interleukins (IL-1) in gingival tissue of PD horses7. Breed data were statistically significant. Jumping breeds (p=0,019), arabians (p=0,024) and racehorses (p=0,019), show low risk compared to Chilean pure breed. In a study of 456 Chilean pure breed horses, it was found 7% PD prevalence2. Other study in Chile found a 11% of gingivitis in incisors19. There is a study in Colombia were Criollo horses show 1,3% of PD and 5% of diastemas in incisors 24, found it at oral exam of 400 horses. There were no other reports published of PD prevalence in South America according to this author. Comparing data with other latitudes it means a low prevalence, just close to 13,9% reported in a study in UK4. This low risk of other breeds compare to Chilean pure breed horse (also known as Chilean rodeo horse) could be due to differences in management and stabling and low or lack grazing at pastures, nevertheless, must be understood like a possibility that need to be verified in large populations studies. It has been theorized that green grass pastures could help to show lower PD lesions, because of the potential of producing more salivation and more protective local factors in the oral cavity, condition that could affect Chilean pure breed horse, especially in Central Region21,20,22. Like a conclusion Chilean horses have similar PD oral clinical findings to other studies, and it was possible to identified risk factors like age, breed, and diastema presence. We need soon larger horse population studies to get better understanding of diet involvement in periodontal disease.
References
1. Dixon P, Barakzai S, Collins, et al. Treatment of equine cheek teeth by mechanical widening of diastemata in 60 horses (2000 – 2006), Equine Veterinary Journal 2008; 40 (1), 22–28
2. Guerra S, Pineda M, De Negri L, et al. Frequency of dental disorders in Chilean Rodeo Horses between 2010 and 2013, Sustainability, Agri, Food and Environmental Research (SAFER) 2016; 4(3), 37-43 ISSN: 0719-3726
3. Lee L, Reardon R, Dixon P. A post-mortem study on the prevalence of peripheral dental caries in Scottish horses. Equine Vet. Educ. 2019; 31, 96–101
4. Nuttall H, Ravenhill P. Prevalence & analysis of equine periodontal disease, diastemata, & peripheral caries in a first-opinion horse population in the UK. The Veterinary Journal 2019; 246, 98–102
5. Du Toit N, Burden FA, Baedt LG, et al. Dimensions of diastemata and associated periodontal food pockets in donkey cheek teeth. J Vet Dent. 2009;26(1):10-14.
6. Kennedy R, Dixon P. The aetiopathogenesis of equine periodontal disease – a fresh perspective. Equine vet. Educ. 2018; 30 (3) 161-168
7. Kennedy R, Lappin D, Dixon P et al. The microbiome associated with equine periodontitis and oral health. Vet Res 2016; 47:49
8. Klugh D. Equine periodontal disease. Clin Tech Equine Pract. 2005;4(2):135-147.
9. Cox A., Dixon P.M., Smith, S. Histopathological lesions associated with equine periodontal disease. Vet. J. 2012; 194, 386-391.
10. Díaz-Narváez VP. Metodología de la Investigación Científica y Bioestadística para Profesionales y Estudiantes de Ciencias de la Salud. Editorial Universidad Evangélica del Salvador (UEES) y Universidad Andrés Bello de Chile (UNAB). San Salvador de El Salvador y Santiago de Chile. 2019.
11. Díaz-Narváez VP, Calzadilla-Núñez A, Reyes-Reyes A. Reflexión acerca de la regresión logística y las decisiones Clínicas. Rev. Méd. Rosario 84: 35-40, 2018
12. Borkent, D. and Dixon, P.M. Equine peripheral and infundibular dental caries: a review and proposals for its investigation. Equine Vet. Educ. 2017; 29, 621-628.
13. Dixon P. Periodontal Disease Research and Treatment – UK Experiences. Paper presented at: AAEP Focus on Dentistry, September 18-20, 2011, Albuquerque, NM, USA.
14. Niemic B. Periodontal Disease, Topical Review. Topics in companion animal medicine. 2008; 23, 2
15. Loesche W, Grossmann N. Periodontal Disesease as a specific, albeit Chronic, Infection: Diagnosis and Treatment. Clinical Microbiology Reviews 2001; 727-752.
16. Baker, G.J. Some aspects of equine dental disease. Equine Vet J 1970; 2, 105-110.
17. Chinkangsadarn T, GJ Wilson, RM Greer et al. An abattoir survey of equine dental abnormalities in Queensland, Australia. Australian Veterinary Journal 2015; 93; 189;194
18. Cordes V, Gardemin M, Lupke M, et al. Finite element analysis in 3-D models of equine cheek teeth. The Veterinary Journal 2012 193, 391 – 396.
19. Muñoz L, F Vidal , O Sepulveda, et al. Patologías dentales en incisivos, caninos y primer premolar en caballos chilenos adultos. Arch Med Vet, 2010; 42, 85-90.
20. Casey M. A new understanding of oral and dental pathology of equine check teeth. Vet Clinic Equine 2013; 29, 301-324.
21. O’Neill H, Keen, J, Dumbell L, et al. A comparison of the occurrence of common dental abnormalities in stabled and free-grazing horse Animal 2010; 4 (10), 1697-1701
22. Pearce C. ‘What’s new in treatment for diastema in cheek teeth’. Paper presented at: Toothfest 2015, Coffs Harbour, NSW, Australia, March 2-6, 2015
23. Jackson K, Weber L, Tennant M. A Retrospective Study of the Effectiveness of Four Different Treatments of Periodontal Disease in Equine Cheek Teeth. Journal of Veterinary Dentistry 2016;33(2), 83-89
24. Cruz J, Sanchez J, Vera L, Caracterización y prevalencia de las enfermedades orales en el caballo criollo, departamento de Caldas, Colombia 2012. Revista Medicina Veterinaria 23, Junio 2012Scielo issn:0122-9354
25. Leite CT, Duarte CA, Mozzaquatro FD, Mistieri ML, Machado IR, Porciuncula ML, Leon IS, Dowich G, Goss GC, Santini AP, Pereira EP. Survey of dental diseases in crioulo breed horses reared in an extensive farming system. Arq. Bras. Med. Vet. Zootec. v.71, n.1, p.21-27, 2019.
26. Jackson K, Kelty E, Stazsyk C, Tennant M., 2019. Peripheral caries and diseases of the periodontium in Western Australian horses: An epidemiological, anatomical and histopathological assesment. Equine Vet Journal. 51, 617-624