Reasons for performing study: Although clinical disorders of equine maxillary cheek teeth (CT) infundibula are common, anatomical knowledge of these structures is poor.
Hypothesis: Anatomical examinations of sectioned CT infundibula will better define their shapes and sizes and allow identification of infundibular cemental variations and changes.
Material and methods: Cheek teeth were extracted post mortem from 33 horses, aged 3–30 years, without a clinical history of dental disease. The CT were sectioned longitudinally in the bucco-palatal plane through the widest aspects of both infundibula. The infundibular surfaces were then assessed morphologically, including by measurements of areas of cemental variations and changes. Specimens from selected teeth were examined histologically.
Results: Infundibular length and infundibular surface area, and infundibular length as a proportion of dental crown length progressively decreased with age, e.g. infundibular length was up to 89 mm after eruption to 2 mm in one older horse. Triadan 06 and 09 positions had significantly shorter CT and therefore infundibula, than the other 4 Triadan positions. Only 11.7% of infundibula were filled completely with normal appearing cementum, 8.2% of infundibula (especially the 09 position) had complete cemental caries; 22.6% of infundibula had areas with cemental hypoplasia and the remaining 57.5% of infundibulae had a variety of other cemental appearances, including the presence of central defects, localised occlusal caries and cemental discolourations. Histology showed the presence of an apical blood supply to infundibular cement in younger horses.
Conclusions: Anatomical variations of CT infundibular cement are very common and some changes, such as areas of localised cemental hypoplasia, may predispose to the development of infundibular caries.
Potential relevance: This more complete description and quantification of CT infundibular anatomy should allow more rational assessment and treatment of equine CT infundibular disorders.
An infundibulum is a cup or funnel shaped invagination of enamel from the occlusal surface of equine incisor and maxillary cheek teeth (CT). Disorders of equine maxillary CT infundibula include developmental, incomplete filling with cement(um) (i.e. cemental hypoplasia), which is reported to occur in up to 65% of equine maxillary CT (Baker 1979; Kilic et al. 1997). Cemental hypoplasia may predispose affected CT to infundibular caries, a disorder whose prevalence increases with increasing age (Honma et al. 1962; Miles and Grigson 1990; Crabill and Schumacher 1998; du Toit et al. 2008). The consequences of advanced infundibular caries include the development of midline sagittal fractures (Dacre et al. 2007) as well as pulpal and thus apical infections (Dacre et al. 2008).
Despite the apparent high prevalence of equine CT infundibular disorders, knowledge of CT infundibular anatomy is incomplete, although newer imaging techniques are improving knowledge of this structure (Windley et al. 2009a,b). Establishing the prevalence and quantifying the extent of cemental hypoplasia and other cemental changes is a prerequisite to understanding infundibular disorders more fully. There is increasing interest in prophylactic endodontic-type treatment of CT infundibular caries (Klugh et al. 2001; Johnson and Porter 2004), although few objective data are yet available on the value of these interventions (Galloway and Easley 2009); but a comprehensive understanding of infundibular anatomy is a prerequisite to performing any such intrainfundibular restorations. The aims of this study were to examine equine maxillary CT infundibula from horses of differing ages to determine the gross dimensions and shapes of infundibula in CT that were sectioned longitudinally through the rostral and caudal infundibula in the bucco-palatal (latero-medial) plane; and grossly to assess the prevalence and extent of hypoplasia, caries and other defects and variations of infundibular cement. Some limited histological examination of cementum was also performed.
Materials and methods
Source and handling of teeth
Skulls were obtained post mortem from 33 horses (median age 10 years; range 3–30), mainly Thoroughbred crosses, Thoroughbredsand larger, cob-type horses that were subjected to euthanasia on humane grounds for reasons unrelated to dentition at Edinburgh University Veterinary School. Teeth were not examined prior to selection of any skulls. Skulls were chosen initially at random, but the latter 11 were selected on an age basis, to include a wide age-range in the study. After disarticulating the skulls, all maxillary cheek teeth were extracted intact using a hammer and osteotome. The individual teeth were then sectioned using a 99-TS230M water-cooled tile saw1 with an 20.3 cm diameter, 8.1 mm thick, continuous-rim, diamond-tipped blade2. Teeth were sectioned in standardised, longitudinal, palatal (medial) to buccal (lateral) planes to reveal the internal structures of both rostral and caudal infundibula. The central occlusal opening in the infundibular cementum (remnants of previous central vasculature) that was present in most teeth was used as a reference point. In CT where this central opening was not visible, infundibula were sectioned in the middle of their rostrocaudal length. Additional sectioning, or grinding of teeth on the saw blade was required to expose the full length of curved infundibula in some CT. Some sections of cementum had decalcified histology performed as described by du Toit et al. (2008).
Digital images were obtained of each sectioned infundibula with a metric ruler included as a measurement reference, for both longitudinal measurements and also for later analyses of infundibular surface areas using an Image-Pro Plus program3. The surface areas of the whole infundibulum, and of areas of cemental hypoplasia, caries or other cemental defects, and the lengths of the rostral and caudal infundibula and dental crown were measured for each tooth. Dental crown length was defined as the distance between the occlusal surface of the tooth and the apical limit of the enamel (i.e. excluded the roots that are of variable lengths and composed solely of cementum and dentine).
After performing pilot studies, the following gross descriptions of infundibular cementum were used:
Grossly normal infundibula: Complete filling of infundibulum with grossly normal cementum (Fig 1a).
Cemental hypoplasia: Areas of developmental, complete absence of infundibular cementum, with the underlying infundibular enamel exposed. These defects often contained thin folds of soft tissue (Fig 1b).
Complete cemental caries: Infundibula with characteristic dark, carious destruction of their cementum that extended through the full length of the infundibulum (with or without extension of caries into the underlying enamel) (Fig 1c).
Other cemental defect: Any other cemental abnormality, including localised areas of central cemental caries at the occlusal surface, prominent, centrally located linear defects (probable sites of previous central infundibular vasculature), or pale brown or red discoloured, or porous appearing areas of intact infundibular cementum (Fig 1d).
Horses were divided into 4 age groups for statistical analyses, i.e. 3–5 years; 6–11 years; 12–20 and >20 years. Data were not normally distributed, and so Chi-squared analyses were used to determine possible associations between the assessed variables. Friedman tests were used to quantify and establish if the observations from selected age groups differed, and regression analysis was used to ascertain if there was a dependent relationship between 2 selected variables. Statistical analyses were performed using Minitab 14 and a value of P<0.05 taken as statistically significant.
A total of 396 maxillary cheek teeth were extracted from the 33 horses; n = 5 age 3–5 years; n = 13 age 6–11 years; n = 12 age 12–18 years; and n = 3 age >20 years. Following CT sectioning, 786 infundibular sites (393 rostral and 393 caudal infundibula) were exposed for examination and measurements. Six infundibula in 3 CT (08, 09, 11) that were damaged iatrogenically during sectioning were treated as missing values. The 3 oldest horses (age 21, 23 and 30 years) had a total of 26 infundibula absent from their (short) maxillary cheek teeth, (both infundibula in 12 CT, and 2 caudal infundibula), which were assumed to be due to normal, age-related dental attrition and these were also were treated as missing values. No apically infected or sagittally fractured maxillary CT were present in any skull.
Infundibular length (median 41 mm) ranged from 89 mm in a 210 from a 4-year-old to 2 mm in a 208 from a 30-year-old horse (Fig 2, Table 1). Infundibular length was associated significantly with age (P<0.001). Infundibular length was also assessed as a proportion of the dental crown (median value 82%) and ranged from 99% in a Triadan 111 from a 4-year-old to 7% in a 110 from a 16-year-old horse, and this feature was also significantly associated with age (P<0.001) (Fig 3).
Table 1. Median length and surface areas of CT infundibula in the 6 Triadan positions
Median infundibular length (mm)
Median infundibular surface area (mm2)
06 (n = 129)
07 (n = 129)
08 (n = 130)
09 (n = 122)
10 (n = 128)
11 (n = 122)
There was no significant difference (P = 0.86) between the lengths of the rostral and caudal infundibula in any age group. However, infundibular lengths were significantly different (P<0.001) between teeth in different Triadan positions, with Triadan positions 06 and 09 consistently having the shortest infundibula and 08 having the greatest median infundibular length (Table 1).
Infundibular surface area
Infundibular surface area (median value 179 mm2), as assessed on single, longitudinal, bucco-palatal section, ranged from 610 mm2 in the 210 of a 4-year-old to 7 mm2 in the 208 of a 30-year-old horse. Infundibular surface area was also significantly associated with both age (P<0.001) and Triadan position (P<0.001), with the 06s and 09s having the smallest and the 08s the largest surface area (Table 1). There was no significant difference in the infundibular surface area between rostral or caudal infundibula (P = 0.86).
Grossly normal infundibula
Only 11.7% (89/760) of infundibula were completely filled with grossly normal cementum (Fig 1a) on the sections examined (Table 2). Grossly normal cementum completely filled 7.5% of infundibula in the 3–5 year age group; 5.6% in the 6–10 year age group; 16.7% in the 12–20 year age group; and 32.6% of (the remaining) infundibula in the >20 year age group.
Table 2. Number (and %) of infundibula with: grossly normal cementum; cemental hypoplasia; complete cemental caries and other cemental change in each Triadan position
Grossly normal (n = 89)
Cemental hypoplasia (n = 172)
Complete caries (n = 62)
Other changes (n = 437)
06 (n = 129)
07 (n = 129)
08 (n = 130)
09 (n = 122)
10 (n = 128)
11 (n = 122)
In grossly normal infundibula, there was no significant difference (P = 0.74) in the median surface area between rostral (median 135 mm2) and caudal (median 108 mm2) infundibula. There was a significant association of grossly normal infundibula with Triadan position (P = 0.02), with notably only 3.3% of infundibula in the 09 position being completely filled with normal cementum (Table 2).
Infundibular cemental hypoplasia
Well defined local areas of complete cemental hypoplasia (with cementum present in the remaining part of the infundibulum) were present in 22.6% of the infundibula (172/760), including in 24.4% of rostral and 20.8% of caudal infundibula. These areas were often located near the apical region (Figs 1b, 4), but occasionally more occlusally. Cemental hypoplasia was present in 29.2% of infundibula in horses in the 3–5 year age group; 27.1% in the 6–11 year group and 18.8% in the 12–20 year age group, but was not present in the infundibula of horses age >20 years. There was no significant difference in the percentage of infundibular surface area affected with cemental hypoplasia between caudal and rostral infundibula (P = 0.23). The surface area of hypoplastic infundibular cement (as a proportion of total infundibular surface area) ranged from 1% (108 of a 9-year-old horse) to 35% (207 of a 14-year-old horse) with a median value of 7%. Cemental hypoplasia was most commonly observed in the Triadan 11 position (40% affected) and least commonly in the 09 position (13.9% affected) and this difference between Triadan positions was statistically significant (P<0.001).
Complete infundibular caries
Caries affecting the full length of the examined infundibular surface and that always communicated with the occlusal surface was present in 8.2% (62/760) of infundibula, with a prevalence of 7.3 and 9%, respectively, in the rostral and caudal infundibula (Figs 1c, 5). There was a significant difference in the prevalence of completely carious infundibula between the different Triadan positions (P<0.001; Table 2). The 09s were the most commonly affected position (22.3% of infundibula in the 09 position were fully carious), i.e. 30 times more frequently than infundibula in the Triadan 11 position (0.8% fully carious). The surface area of completely carious infundibula ranged from 7 mm2 in the 208 of a 30-year-old to 395 mm2 in the 109 of a 7-year-old (median 91 mm2). There was also an age-related difference in the prevalence of complete infundibular caries, i.e. 3–5-year-old horses had none; 6–11-year-old horses had 3.3%; 12–18-year-old horses had 11.5% and horses aged >20 years had 41.4% of their infundibula affected with complete caries. There was no significant difference in the surface area of rostral and caudal fully carious infundibula (P = 0.43).
Miscellaneous infundibular cemental changes
Other cemental changes including localised caries (dark brown to black defective cementum), especially centrally near the occlusal surface, linear central infundibular defects (likely sites of previous central vasculature) or intact areas of cementum that were pale brown or red coloured, or of a porous appearance or often combinations of these features were present in the remaining 437 infundibula. The percentage of surface areas having such variations and changes ranged from 1% in a 210 of an 8-year-old to 74% in the 106 from a 24-year-old (median 11%). Horses in the 3–5 year age group had 63.3%; those in 6–11 year age group had 59.8%; those in the 2–18 year age group had 58.7% and horses aged >20 years had 19.6% of infundibular surface area having these miscellaneous cemental changes. There was no significant difference in the proportion of surface area having miscellaneous cemental changes between the rostral and caudal infundibula (P = 0.87).
Miscellaneous cemental changes were most commonly present in the Triadan 10 (69.5%) and 06 position (65.1%) and least commonly in the 11 position (41%) (Table 2), with a significant difference present in the distribution of these cemental defects between Triadan positions (P = 0.003). This group of cemental changes included infundibula that had red-tinged cement situated apically, that were recognised in horses aged ≤11 years (Fig 6). Histology in 12 of these CT showed that 3 CT (210, 110 and 109 from two 3-year-old horses) had viable endothelial cells and red blood cells in the apical infundibular cementum, in addition to apparently viable cementocytes within cemental lacunae (Figs 7, 8). In a previous study, transverse sections of young maxillary CT showed the apex of some infundibula to be perforated by vascularised tissue (Fig 9) (G. Beresford and P.M. Dixon, unpublished data).
As expected, this study showed infundibular length (maximum 89 mm and minimum 2 mm long) to decrease with age (Fig 9) with some infundibula fully worn away in horses aged >20 years. Infundibular length as a proportion of dental crown length also significantly decreased with age, from up to 99% in recently erupted CT to 7% of crown length in aged CT (median of 82% of crown length in all age groups). Infundibular length also varied significantly between different Triadan positions, with the 06 and 09 positions having the shortest CT and therefore the shortest infundibula (i.e. their infundibula were typically 45 and 28% shorter, respectively, than the mean infundibular length of the 4 other Triadan positions). The surface area of infundibula reflected infundibular length, with the Triadan 06 and 09 positions having the smallest areas. Although all surface areas were measured on a single longitudinal section in the bucco-palatal plane from what was believed to be the widest aspect of each infundibulum in that plane, these sections will have variation depending on the plane of the section because infundibula are not always straight or completely perpendicular to the occlusal surface and this is a limitation with this study.
Only 11.7% of equine infundibula were completely filled with normal cementum on the sections examined and as later discussed, it is likely that some of the other variations in cemental morphology, should be considered to be within the normal range of infundibular cemental appearance. Similarly, a recent study of 126 CT using computer tomography found that 90% of infundibula had some apparent defects, with all teeth with a dental age of >6 years having infundibula incompletely filled with cementum (Windley et al. 2009b).
Caries involving the full length of the infundibula (that always communicated with the occlusal surface) was present in 8.2% of infundibula, most commonly in horses 12–20 years old. Inexplicably, CT in the Triadan 09 position were most commonly affected with extensive caries (i.e. 30 times more commonly than those in the Triadan 11 position) and conversely, the 09s also had the lowest level (3.3%) of grossly normal infundibula in this study. The maxillary 09 position is the most common site for idiopathic CT fractures to develop (Dacre et al. 2007), which would support the role of caries in the aetiopathogenesis of these fractures. However, idiopathic fractures were most commonly observed in horses aged 9–10 years (Dacre et al. 2007), whereas in this study complete infundibular caries was more common in older horses (age 12–20 years). The 09 position is also commonly involved in apical infections (in horses of median age 8 years) (Dixon et al. 2000) and an extension of infundibular caries has recently been shown to cause 16% of maxillary CT apical infections (Dacre et al. 2008). Infundibular caries is reported to be rare or nonexistent in wild horses (Miles and Grigson 1990) and cemental hypoplasia has not been described in wild equids to date, suggesting that the domestication of horses has contributed to the aetiopathogenesis of CT infundibular disorders.
Infundibular cemental hypoplasia was grossly observed in 22% of all infundibula, which is less than the 65% prevalence observed ultrastructurally by Kilic et al. (1997), but is certain that the latter technique detected more subtle cemental changes. It is also probable that some cementum classified as having miscellaneous cemental changes in this study, had in fact lower grade cemental hypoplasia. Cemental hypoplasia, being a developmental defect was as expected, most commonly found in the younger age groups (29.2% in age 3–5 years and 27.1% in 6–11 year groups). The mechanisms that cause cemental hypoplasia are unclear, but disruption of occlusal blood supply by premature removal of deciduous CT (‘caps’) cannot cause cemental hypoplasia of the molars (Triadan 09–11) that do not have a deciduous precursor, and in this study, the Triadan 11 position had the highest prevalence of cemental hypoplasia.
The finding of viable vasculature and cementocytes in apically located cementum proves the presence of an active apical blood supply in some infundibula that persists for many years after eruption, i.e. that infundibular cementum is nourished from both apical and occlusal aspects until eruption and thereafter from apical aspect only in some infundibula. Accordingly, the infundibulum – and consequently the infundibular dental organ – needs to be perforated by blood vessels as seen in Figure 9. This finding contradicts the current concepts for the development of infundibula in hypsodont tooth and needs to be addressed in further studies.
Many areas of hypoplastic cementum were situated apically, suggesting that loss of vascular supply from this aspect of infundibula may have compromised cemental formation. In any case, the consequences of such apically located infundibular defects may not appear until later life, when these defects first become exposed occlusally and infected by oral bacteria (Crabill and Schumacher 1998). The relationship of cemental hypoplasia to cemental caries was not obvious in this study, but may be because areas of cemental hypoplasia with communications to the occlusal surface became infected and so were carious at the time of our examinations.
Many defects were observed deep in infundibula, additionally many infundibula were curved in younger horses and some infundibula had dilations, including at their apical aspects. These anatomical features would make effective intraoral restorations of such deeply situated infundibular defects technically very difficult.
The majority of infundibula (58%) had gross infundibular features other than complete filling with normal appearing cementum; cemental caries of full length of infundibulum or areas of cemental hypoplasia, and were classified separately. This heterogeneous group often had a centrally located defect at site of former vasculature (Fig 5) and these areas had darker localised areas of caries or food staining when they were exposed occlusally. Other teeth had areas of apparently more porous cementum, that was dark if connected to the occlusal surface. As noted, it is probable that some of these cemental variations are within the normal range of appearance and they may have been classified differently by other workers. A systematic histological study of large number of infundibula in different aged horses is required to more fully understand infundibular cementum variations and to more accurately determine what may be considered to be within the normal range.
In conclusion, this study has described the gross anatomical and histological findings of maxillary CT infundibula in different horses of differing ages. The majority (88%) of infundibula are not completely filled with normal appearing cementum, and some of these variations in cemental appearance may be normal findings. However, 8% of infundibula in clinically normal horses had severe infundibular caries, preferentially in the Triadan 09 position. This study also confirmed the presence of an apical blood supply to infundibula in younger horses.
This study was partly funded by The Donkey Sanctuary, Sidmouth Devon. Nicole du Toit was supported by a Donkey Sanctuary Scholarship. We thank Darren Shaw for statistical advice and Carsten Staszyk for helpful comments to manuscript.
1 Buehler, Coventry, UK.
2 Malvern Lapidary, Malvern, Worcestershire, UK.
3 Media Cybernectics, Silver Spring, Maryland, USA.
Author contributions All authors contributed to the initiation, conception, planning, writing and statistics for this study. Its execution was by C.F.