Equine Odontoclastic Tooth Resorption and Hypercementosis (EOTRH) is a painful and progressive dental disease, which affects the incisor and canine teeth of senior horses.1 According to Vlaminck et al,2 Icelandic horses appear to be more susceptible to EOTRH. In Germany, the prevalence is estimated to be over 50% in older horses.3 So far, the occurrence of EOTRH has not been evaluated specifically for Icelandic horses.
The etiology and pathologic process of EOTRH are not known yet. A multifactorial genesis, including mechanical stress of the periodontal ligament as well as involvement of red complex bacteria (Treponema and Tannerella spp) are taken into consideration.4,5 EOTRH could also be related to age, breed, and sex.6,7 The influence of horse husbandry and feeding is a much-discussed topic but remains uncertain. Moreover, genetic linkage and systemic factors such as hypervitaminosis A, hypocalcemia, and hyperparathyroidism might cause EOTRH.8 Tooth resorption is also described in other species such as cats8 (feline odontoclastic resorptive lesion), dogs9,10 (canine odontoclastic resorptive lesion), and humans.11
Clinical signs can vary between nearly asymptomatic to gingivitis, gingival recession, and subgingival swelling with variable severity.12–14 Furthermore, the (eating) behavior may be altered.
In addition to these clinical findings, EOTRH diagnosis is based on typical radiographic findings, such as variable levels of dental resorption and bulbous enlargement of the intra-alveolar tooth aspects.1,12,15
At present, extraction of affected painful teeth is the only effective treatment.13 Preventive therapies may result from a better understanding of the etiology of EOTRH and how it is influenced by various anamnestic factors such as horse husbandry and feeding.
The initial aim of the study was to detect the prevalence of EOTRH in the selected population of Icelandic horses in Northern Germany. The studied population was divided into 2 groups: orally healthy horses and horses affected by EOTRH. Comparison of both groups allowed us to identify risk factors for the development of EOTRH. We hypothesized that an intensive diet rich in carbohydrates and acids would favor the development of EOTRH.
Methods
Horses
The examinations were conducted on an outpatient basis, in Lower Saxony, Germany. Only purebred Icelandic horses over 15 years of age were examined. The population consisted of EOTRH-affected and -nonaffected horses. At least 1 healthy horse and 1 horse suffering from EOTRH were examined per stable to allow a comparison of “EOTRH diseased” and “EOTRH healthy” at the same location. The preliminary dental health report relied on the owners' statement. Study participants were recruited from the client base of a local veterinary practice and via a press release.
The owners indicated in advance whether a veterinarian or dentist had already suspected or diagnosed the disease.
A written anamnesis using a standardized questionnaire was obtained in advance and evaluated (Supplementary Table S1). The animal's environment had to be consistent during the previous year. Horses that had changed from, for example, 24-hour grazing to stabling within the previous 12 months were excluded from the study.
Examinations
All horses were clinically examined according to a standardized examination protocol. Stopping criteria were established in advance to ensure that only generally healthy animals were included in the further examinations (Supplementary Table S2).
The subsequent examination of the anterior oral cavity and the intraoral x-rays were performed under sedation using an α-2 opiate combination (detomidine [Cepesedan], 0.012 to 0.03 mg/kg, IV, once and butorphanol [Butorgesic], 0.025 to 0.04 mg/kg, IV, once).
The clinical appearance of the rostral oral cavity was documented and evaluated according to a standardized protocol and score (Supplementary Table S3). A minimum of 2 intraoral radiographs were taken per horse, 1 of the maxilla and 1 of the mandible (0°/+45° and 0°/–80° projection). The radiographs were evaluated independently by 3 veterinarians using a standardized score (Supplementary Table S4). The median was formed from the total scores of all 3 observers and was transferred to an adjusted radiologic staging system based on Hüls et al16 and Rehrl et al3 that classified horses into 5 groups: “no EOTRH” (stage 0), “suspicious” (stage 1), “mild” (stage 2), “moderate” (stage 3), or “severe” (stage 4; Table 1).
Adjusted radiologic staging system (based on Hüls et al16 and Rehrl et al3).
| Stage | Score | ||
|---|---|---|---|
| Normal | 0 | 0 | No radiological findings |
| Suspicious | 1 | 1–2 | Tooth shape preserved but sporadic deviations, slightly blunted root tip, surface irregular or rough, slightly altered tooth structure |
| Mild | 2 | 3–5 | Tooth shape preserved, slightly blunted root tip, surface irregular or rough, slightly altered tooth structure |
| Moderate | 3 | 6–9 | Tooth shape largely preserved, intra-alveolar tooth part is not wider than the clinical crown, obviously blunted root tip, surface irregular or rough, moderately altered tooth structure |
| Severe | 4 | > 10 | Loss of tooth shape, intra-alveolar tooth part is wider than the clinical crown, surface obviously irregular or rough, severely altered tooth structure |
Statistical analysis
Descriptive statistics were calculated and reported as mean or median. Frequency distributions were reported as percentages or numbers. The effects of age, sex, animal husbandry, and feeding on the acquired EOTRH stage were investigated with logistic regression analysis. A significance threshold of P < .05 was used. Statistical analysis was performed with standard software (EG version 7.15; SAS Institute Inc; and Excel version 2304; Microsoft Corp).
Results
A total of 154 horses were examined. Three horses were excluded from the study, resulting in 151 horses being evaluated. EOTRH was diagnosed in 72.2% (109/151) cases. Further distribution is provided (Figure 1).
Flow chart of study population. Number of horses with and without Equine Odontoclastic Tooth Resorption and Hypercementosis (EOTRH) and its severity. The findings of 3 horses (P095, P143, and P147) had to be excluded due to lack of x-rays.
Citation: Journal of the American Veterinary Medical Association 261, S2; 10.2460/javma.23.05.0301
Age and sex
Overall, the study population consisted of 87 geldings, 1 stallion, and 63 mares that ranged in age from 15 to 31 years, with an average age of 20.1 years. Horses with EOTRH were significantly (P = .004) older (median age, 20.7 years; range, 15 to 30 years) than horses without this dental disease (median age, 18.8 years; range, 15 to 31).
There was a total of 42.7% females and 58.3% males. The frequencies of EOTRH in male and female horses are summarized (Figure 2). A significant sex predilection for males to develop EOTRH is given (P = .03).
Occurrence of EOTRH in male and female horses. EOTRH (stage ≥ 2) = Radiographic findings of EOTRH at least stage 2 (mild). Healthy (stage 0) = No radiographic findings. Suspicious (stage 1) = Unclear x-ray findings, not excluding EOTRH.
Citation: Journal of the American Veterinary Medical Association 261, S2; 10.2460/javma.23.05.0301
Origin and import
A total of 29 of 151 (19.9%) horses were imported from Iceland (n = 18), Denmark (6), the Netherlands (4), and the US (1). A total of 117 horses were bred in Germany. For 5 horses the information about the place of birth was missing.
No x-ray findings were documented for 27.6% (8/29) of the imported horses. These horses ranged in age from 3 to 15 years with an average age of 7.1 years at the time of import. The average age of importation was 14.1 years.
A total of 58.6% (17/29) of the imported horses were diagnosed with EOTRH. On average, the imported horses had lived in Germany for 18.3 years. The average age of EOTRH-affected, imported horses was 5.9 years with a range of 1 to 10 years (data refer to the time of import). The remaining 4 horses could not be clearly identified as EOTRH affected or healthy (stage 1). Horses born in Germany seemed to have a higher risk of developing EOTRH (P = .02). There was a significant correlation between Germany as the place of birth and the risk of contracting EOTRH (P = .02). Thus, 75.2% (88/117) of the horses bred in Germany had EOTRH, while 6.8% (8/117) were classified as stage 0.
Animal husbandry and feeding
The majority of the horses studied (87.4% [132/151]) were kept in open stables offering direct access to pasture. Only a small percentage lived in open stalls without pasture (5.3% [8/151]) or on pasture (3.3% [5/151]). A total of 4% (6/151) of the horses were reported to be kept in stables. EOTRH-diseased and healthy horses did not differ in husbandry.
Being the main source of roughage, haylage was fed to 87% (20/23) of the EOTRH-healthy horses (stage 0) and 80.7% (88/109) of the EOTRH-affected horses (stage ≥ 2). Other roughage sources included hay, hay cobs, and silage as well as a combination of the above and were fed to horses with stages 0 to 4. No predilection for EOTRH development was shown in horses fed ensiled roughage (P = .51).
Horses in stage 0 (no x-ray findings) were fed from hayracks in 60.9% (14/23) of cases. These were covered with hay nets in 21.7% (5/23) of cases, whereas 39.1% (9/23) of EOTRH-healthy horses were fed from the ground. The ability to ingest sand while feeding was reported in 13% (3/23) of cases.
A total of 81.7% (89/109) of EOTRH-affected horses (stage ≥ 2) were fed from hayracks. In 21.1% (23/109) of cases, the hayracks were covered with hay nets. A total of 16.5% of horses with EOTRH were fed from the ground partly in combination with hay nets (2.8% [3/109]) or hayracks (2.8% [3/109]). Another 2.8% (3/109) were fed from hay nets. For 1 horse, it was reported that it may have ingested sand while eating.
However, there was no significant influence of feeding methods on horses developing EOTRH (P[hayracks] = .5249); P[hay nets] = .91).
Concentrates were fed to 95.7% (22/23) of the stage 0 horses and 86.9% (89/109) of the EOTRH-affected horses. These included premixed horse muesli (stage 0, 68.2% and stage ≥ 2, 57%), cereals (stage 0, 22.7% and stage ≥ 2, 24.7%), pellets (stage 0, 0% and stage ≥ 2, 9.7%) and mash (stage 0, 0% and stage ≥ 2, 6.5%). These feeds were given either individually or in combination. The frequency and quantity of concentrates are shown (Figure 3). There were no significant differences detected between stage 0 and stage ≥ 2 in feeding with concentrates (P = .22).
Frequency and quantity of horses being fed concentrates. Occasionally = Concentrates were given sporadically, (eg, after exercises).
Citation: Journal of the American Veterinary Medical Association 261, S2; 10.2460/javma.23.05.0301
Supplementary feeds were administered very individually. Mineral feed was given to about half of the horses in both groups (stage 0, 52.2% [12/23] and stage ≥ 2, 55.2% [58/105]) with no significant impact (P = .72). Furthermore, the feeding of selenium, medicinal mushrooms, and various other products was indicated. Selenium was fed more frequently to stage 0 horses (21.7%) than to EOTRH-affected horses (8.6%). The administration of selenium also had no significant effect (P = .216). Only 30.4% (stage 0) and 28.6% (stage ≥ 2) of the horses received no supplementary feed.
The horses had access to a tap water supply or well water. Among both EOTRH-healthy and EOTRH-diseased horses, nearly half of the animals drank tap water and half drank well water (P = .05).
Suspicion of EOTRH and other abnormal findings by the owner
EOTRH was not suspected by the owners in 90 of the 151 horses. In 44 horses, EOTRH was diagnosed in advance of the study and the disease was suspected in 12 horses. A total of 5 owners did not provide any information.
A total of 4 owners of stage 0 horses (n = 23) reported that their horses showed abnormalities such as conspicuously quiet behavior and weight loss (horse 1), eating slowly (horse 2), increased salivation (horse 3), and coat change disorder (horse 4).
A total of 60 of the 109 horses diagnosed with EOTRH (55.1%) were described as asymptomatic beforehand. Reported symptoms (not classified by stages) are listed (Supplementary Table S5).
Routine dental examination and treatment
Half of the horses, both EOTRH-diseased and -healthy animals, received annual dental treatment. Whereas EOTRH-healthy horses are presented to a veterinarian/dentist for dental treatment irregularly (52.2%), only 1.9% of EOTRH-affected horses received dental treatment infrequently. Detailed frequencies are summarized (Figure 4).
Frequency of dental treatment (owner information). Irregular = Horses are only presented for dental treatment in case of abnormalities. Regular (no constant interval) = Regular treatment, but interval not specified by the owner.
Citation: Journal of the American Veterinary Medical Association 261, S2; 10.2460/javma.23.05.0301
Discussion
EOTRH is described as a disease of middle-aged horses,4,7,12,13,17 which has only been investigated in a few studies with a larger number of cases.18,19 In fact, in our study population, age was declared to have a significant influence on horses developing EOTRH. Moreover, horses classified in a higher stage (stage ≥ 3) had a higher average age. It should be considered to what extent this phenomenon can be explained by a progression of EOTRH over time. The phenomenon of age-related progression was recently confirmed by Rehrl et al.18 In that study, a close correlation between age and severity of radiographic findings was demonstrated. However, it should be noted that the x-ray findings in our study were made independent of age, so that age-related changes were also scored. This may contribute to a higher score in older animals. Therefore, for practical purposes, it should be considered whether the limits of the individual stages of the radiologic staging system should be adjusted upward for older horses. At present, there are no methods to differentiate between age-related processes and mild pathologic changes due to EOTRH in radiographs. Nevertheless, statistics in our study demonstrated that a horse had about 1.2 times the expected risk compared to a horse 1 year younger.
As other studies4,7 have suggested, it has been confirmed that male horses are more susceptible to EOTRH. Even though the present study included more male horses, the comparison within the sex clearly shows this fact: 61.9% of the mares were diseased, while 80.7% of the males were affected. However, the reason for this predilection remains unclear.
Icelandic horses bred in Germany as well as imported horses are likely to develop EOTRH. Nevertheless, the percentage of horses affected was 16.6% lower among imported horses. In addition, horses imported at an older age had less EOTRH later on, which could indicate that the horses lived in Iceland for a longer time under more optimal conditions and may therefore be less prone to develop EOTRH. Horses born in Germany seem to have a higher risk of developing EOTRH (P = .02). Thus, it should be considered that there are factors in Germany that predispose horses to this disease. The more extensive horse husbandry in other countries such as Iceland as well as a different climate may have an impact. There, the horses spend a large part of their life on poor pastures, whereas in the studied German horse population, grazing was severely restricted. In addition, the pastures in Germany are usually fertilized and sown in areas with higher yields. This assumption is supported by the fact that the incidence of tooth resorption in wild cats is also lower than in domestic cats.20–22 Likewise, access to pasture throughout the year leads to a lower risk of developing peripheral caries.23 Although this affects the cheek teeth, it could influence the entire oral cavity. Compared to eating from a trough, the horses eat continuously in a low head position. It could be possible that the different mechanical forces on the incisors and the increased salivation during grazing have a positive effect on the incisors.
Furthermore, no significant influence of horse feeding and husbandry on the development of EOTRH could be demonstrated. Ensiled roughage was fed to 87% of the EOTRH-healthy horses and 80% of the EOTRH-affected horses. Therefore, the hypothesis that higher acid feeds such as haylage or silage encourage the development of EOTRH is disproved. In this context, it should also be mentioned that the use of hay nets has no predisposing effect even if it were expected due to the changed biomechanics of horses when eating hay from nets. At this point, it should be noted that the only data collected were whether horses ate from nets or not. Other factors such as height and material of the net and mesh size were not considered.
A large percentage of the horses received concentrates regardless of the stage (Figure 3). The administration of concentrated feed did not correlate with the occurrence of EOTRH. Thus, the theory of carbohydrate-rich feed as a predisposing factor for EOTRH is refuted.
The high prevalence of EOTRH in the studied population (109/151) should be emphasized, although the owners described only a few symptoms. The reason for this could be the high pain tolerance of the Icelandic horse, which is a robust breed. Besides, it can be assumed that EOTRH is still underdiagnosed.
The study also had significant limitations. These included the imbalance in the size of the control group (stage 0) and EOTRH-affected group (stage ≥ 2) and the fact that the information given was provided by the owner. As a result, horses presented in the preliminary report as EOTRH-healthy were often officially diagnosed as affected later on.
The study took place in a mobile veterinary practice setting rather than an ideal “clinical trial” setting, which sometimes compromised x-ray image quality. Nevertheless, diagnosis and severity could be determined. Stage 1 was introduced for ambiguous cases to keep the probability of misinterpretation low.
In conclusion, our study suggested that aged and male horses were more prone to EOTRH. The same applies to the country of birth of horses: Icelandic horses bred in Germany are more susceptible to EOTRH, leading to the assumption that general living conditions could influence the development of EOTRH. Nevertheless, the results of this study suggest that there are other predisposing factors, possibly mechanical stress of the periodontal ligament, or metabolic diseases such as pituitary pars intermedia dysfunction along with certain age and sex.
Supplementary Materials
Supplementary materials are posted online at the journal website: avmajournals.avma.org.
Acknowledgments
The authors thank the owners of the horses and the Tierarztpraxis für Pferde, Eyendorf, Germany for providing a mobile x-ray system.
Disclosures
The sedatives used in the study were provided by cp-Pharma GmbH, Burgdorf, Germany.
Funding
This study received financial support from the Stiftung Pro Pferd, Zurich, Switzerland. Funding sources did not have any involvement in the study design, data analysis, and interpretation or writing and publication of the manuscript.
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