The Nasolacrimal Duct of the Mule: Anatomy and Clinical Considerations M

636 EQUINE VETERINARY EDUCATION / AE / DECEMBER 2013

Original Article The nasolacrimal duct of the mule: Anatomy and clinical considerations M. F. Adams*, J. R. Castro, F. Morandi†, R. E. Reese and R. B. Reed‡ Departments of Large Animal Clinical Sciences, †Small Animal Clinical Sciences, and ‡Biomedical and Diagnostic Sciences, College of Veterinary Medicine, University of Tennessee, USA. *Corresponding author email: [email protected]

Keywords: horse; mule; nasolacrimal duct; donkey; anatomy; computed tomography; dacryocystography

Summary Mules were administered detomidine hydrochloride 1 This study investigated the location of the nasolacrimal orifice (Dormosedan) (0.015 mg/kg bwt i.v.) to facilitate (NLO) and course of the nasolacrimal duct in the mule examination. Each nasal vestibule was examined to using visual examination, gross dissection and computed determine the location of the NLO. The nasolacrimal duct of 9 tomography (dacryocystography [CT-DCG]) and concluded mules was lavaged using a technique previously described for 2 that the location of the NLO is distinct from that described for the horse (Michau 2005). Lidocaine hydrochloride gel was horses and donkeys and is easily located, by visual applied to the NLO prior to inserting a 14 cm (5.5 inch), 3.5 Fr, 3 examination alone, within the internal cutaneous tissue of the open-end, tomcat catheter . Once catheterised, the duct lateral wall of the external nares. The course of the was occluded with digital pressure and lavaged in retrograde 4 nasolacrimal duct caudal to the nasal vestibule is similar to fashion with 6–10 ml of sterile, eye irrigating solution injected that of the horse. slowly until the solution flowed from the medial canthus.

Introduction Computed tomography - dacryocystography The 4 university owned mules were subjected to euthanasia The equine lacrimal system consists of both secretory and immediately before CT-DCG and the heads removed at drainage portions and is composed of the lacrimal gland, 2 the atlanto-occipital joint. The specimens were positioned lacrimal puncta, 2 canaliculi, a lacrimal sac, the nasolacrimal on the CT table in ventral recumbency and CT-DCG was duct and NLO (Latimer et al. 1984). The anatomy of the performed using a previously published technique (Nykamp nasolacrimal duct of the horse and the donkey has been et al. 2004), which entailed inserting a 14 cm (5.5 inch), 3.5 Fr, previously described (Said et al. 1977; Latimer et al. 1984) and open-end, tomcat catheter3 into the NLO of the right and left several variations exist, most notably the location of the nares and injecting a radiographic contrast medium (Optiray nasolacrimal orifice (NLO). The NLO of the horse is located on 350; Ioversol 350 mg/ml organically bound iodine)5 into the floor of the nasal vestibule near the mucocutaneous the nasolacrimal duct until it exited the lacrimal puncta. junction (Latimer et al. 1984), whereas the NLO of the donkey The volume of contrast medium injected depended on the is located in cutaneous tissue in the dorsal external nares (Said size of the head and ranged from 1.0 ml (6-month-old, et al. 1977). Anecdotally, the location of the NLO of the mule miniature mule) to 5.5 ml (7-year-old, gaited-horse mule). Thin (Equus asinus x caballus) has been described as highly section, transverse images were obtained before and variable and difficult to locate visually. The aims of this study immediately after injecting the contrast medium using a were to determine the location of the NLO in a population of 40 slice multidetector CT scanner (DS Brilliance 40 Hybrid mules, to describe landmarks for locating the NLO, and to CT system)6 and the following imaging parameters: 40 × determine the course of the nasolacrimal duct of the mule 0.625 mm collimation, 0.474 pitch, 0.5 s rotation time, 120 kV, using gross dissection and CT-DCG. 2509 mAs/slice. Data were reconstructed using edge enhancing and standard algorithms. Edge enhancing was Materials and methods used to optimise evaluation of osseous structures and standard algorithms were used to optimise evaluation of soft tissues. Visual examination and nasolacrimal lavage Results were displayed with bone windows (window width: The left and right external nares of 40 mules were examined to 2600, window level: 660) and with soft tissue windows (window establish the location of the NLO and determine if retrograde width: 350, window level: 50). Images were evaluated using a lavage of the nasolacrimal duct was possible. Thirty-six mules dedicated workstation (Philips Extended Brilliance Workspace were privately owned and the cohort included mules 4.5) and multiplanar and 3D images were reformatted, as of varying age, sex and breed (gaited-horse mules, needed, from the transverse thin section data. Measurements nongaited-horse mules and draught mules). The remaining 4 were obtained on transverse images oriented 90° to the hard mules were university owned, including a 6-month-old, palate. miniature mule, one yearling mule and two 7-year-old gaited-horse mules. All mules were in good body condition, had no evidence of ocular or respiratory disease and Gross dissection appeared clinically healthy. All procedures performed on The tomcat catheter3 was left in place following CT-DCG and mules were approved by the University of Tennessee’s the left and right nasolacrimal ducts of each of the 4 heads Institutional Animal Care and Use Committee. were injected retrograde with red latex casting material7 until

Fig 1: Left naris of mule showing placement of hand prior to eversion of naris. The NLO is located opposite the tip of the index finger within the nasal vestibule. Fig 2: Everted left naris of mule demonstrating the NLO (arrow) in Location A. observed to flow from the lacrimal puncta. The lacrimal puncta and NLOs were clamped with haemostats to prevent loss of casting material prior to polymerisation. The specimens caudomedial from the lateral edge of the naris (Fig 2). In 4/40 were injected with 10% formalin via the common carotid mules (10%), the NLO was observed on the floor of the nasal arteries, submerged in 10% formalin and refrigerated at 7°C for vestibule (Location B). One mule (2.5%) had a NLO in Location 7 days to allow the latex to solidify. The specimens were A and in Location B in both nares. hemisected longitudinally on the median plane using an Catheterisation and retrograde lavage of the nasolacrimal electric band saw before dissecting the nasolacrimal duct duct was performed in 9 mules. In these mules, including 3 with < from either a medial or lateral approach. The rostral and a NLO 1 mm, the tomcat catheter was inserted easily and caudal maxillary sinuses of 2 specimens were trephined using a with little resistance (Figs 3 and 4) and lavage was performed 2.54 cm (1 inch) Galt trephine8 using previously published without difficulty. landmarks for sinusotomy in the horse (Perkins et al. 2009). Multiple NLOs were identified in 5/40 mules (12.5%). In 4 of the 5 mules, 2 orifices, approximately 5–10 mm apart, were found bilaterally, although not always bilaterally symmetrical in Results location or in size. Of the 4 mules, 2 mules had double orifices Visual examination and nasolacrimal lavage in Location A and 2 mules had double orifices in Location B (Fig 5). In one of these mules, a Jones Test (passage of The NLO of the mule was easily located with visual fluorescein stain to the NLO after topical application to the examination in all 40 mules (36 live and 4 cadaver specimens). eye) was performed to evaluate patency and produced stain The average diameter of the NLO was about 1 mm but varied from both orifices of the right naris in approximately 5–6 min. between 0.25 and 4 mm. The most common location One mule had one orifice in Location A and one in Location B observed in 35/40 mules (87.5%) was in the internal cutaneous in both external nares. In this mule, catheterisation of both tissue of the lateral wall of the external nares. This location orifices revealed communication with each other and the (Location A) was easily visualised when the thumb was placed main nasolacrimal duct, allowing for retrograde lavage of the in the most dorsal aspect of the external naris, the index finger duct via either of the NLOs. was placed 6 cm in a caudolateral direction from the thumb towards the direction of the caudal border of the false nostril and the internal surface of the naris was everted (Fig 1). The Gross dissection orifice was found at the level of the tip of the index finger in the The right and left NLO of all 4 heads were found within the internal cutaneous tissue at the junction where the lateral wall cutaneous tissue of the lateral wall of the external naris (i.e. curved to meet the floor of the nostril, approximately 3.5–5 cm Location A). Within the tissue of the external naris, the duct was

Fig 3: Nasolacrimal catheterisation of the left naris using 5.5 inch 3.5 Fr tomcat catheter. Note the lateral location of the NLO in the cutaneous tissue of the external naris.

Fig 5: Double NLO (arrows) observed in Location A of right naris of mule.

to be visualised. When the duct reached the level of the caudal maxillary sinus, it entered the lacrimal bone where it was encased in a substantial amount of bone preventing its visualisation without further dissection. While passing through the dorsolateral aspect of the maxillary sinus, the nasolacrimal duct is located dorsal to the recommended site of maxillary sinus trephination in the horse (Fig 8). After entering the lacrimal bone, the duct passed caudally through the continuation of the lacrimal canal to enter the lacrimal fossa where it terminated in a dilatation, the lacrimal sac.

Computed tomography - dacryocystography Fig 4: Nasolacrimal catheter in place demonstrating caudomedial The morphology of the nasolacrimal duct was similar in all course of initial portion of duct. mules. The duct travelled in a caudal and medial direction from the NLO, arching dorsally over the caudal aspect of the flattened dorsoventrally and difficult to dissect from the incisive bone. A saccular dilation of the duct was present at surrounding tissue. The duct continued caudally and medially the level of the diastema between the corner incisor (Triadan along the floor of the nasal vestibule passing dorsal to the 103 or 203) and the second premolar (Triadan 106 or 206) caudal portion of the incisive bone (Fig 6). At this point it (Fig 9). Maximum diameter of the duct observed at this level entered the basal fold of the ventral nasal concha where it ranged from 7.5 to 9.8 mm (Fig 10a). The portion of the attained its closest proximity to the median plane. Passing nasolacrimal duct within the lacrimal sulcus of the maxillary through the basal fold, the duct coursed ventrally to a lateral bone, at the level of the premolar and molar teeth, was the extension of the medial accessory nasal cartilage as it entered narrowest (range: 1.3–1.7 mm) (Fig 10b). The most caudal the ventral concha. After passing ventral to the cartilage, the aspect of the duct, which was encased in the lacrimal bone, duct exited the lateral aspect of the ventral concha into the extended from the level of the first or second molar (Triadan floor of the ventral nasal meatus. The nasolacrimal duct 109/110 or 209/110) to the lacrimal sac (Fig 10c). immediately coursed laterally onto the lateral aspect of the middle nasal meatus where it continued to pass caudally and Discussion dorsally in a slightly dorsally arched fashion (Fig 7). At this Historically, the mule has been considered a poor research location, it lay within the lacrimal sulcus, covered by nasal subject due to the variability of its genetic make-up (Burnham mucosa. At the level of the maxillary fourth premolar (Triadan 2002) and lack of scientific literature often mandates 108 and 208), the duct passed lateral to a ridge of bone, the extrapolation from either the horse or the donkey when rostral terminus of the lacrimal canal, to enter the dorsolateral diagnosing and treating clinical disease of the mule. In this aspect of the rostral maxillary sinus. Upon entering this sinus, the study population, 87.5% of mules displayed NLOs at a site nasolacrimal duct passed dorsocaudally into the maxillary which has not previously been described in horses or donkeys. portion of the lacrimal canal through which the latex was able In only 10% of mules, the NLO was in close proximity to the

Fig 8: Left Lateral view of 7-year-old mule head depicting sinus trephination sites over the rostral and caudal maxillary sinuses in relation to the left nasolacrimal duct which is visible by removal of overlying maxillary bone (some latex has been inadvertently removed with saw blade). Nasolacrimal duct (A); opening into rostral maxillary sinus (B); opening into caudal maxillary sinus (C); facial crest (D); medial canthus (E); infraorbital foramen (F) and incisive notch (G).

or in those with extremely small orifices. In our experience, many orifices, especially those 1 mm and less, had more of a ‘slit-like’ appearance than the ovoid shape more commonly observed in the horse. Knowledge of the typical location of the NLO of the mule was instrumental in finding the NLO in Fig 6: Right naris of mule (dorsal aspect of naris has been these cases, as the orifice would have easily been overlooked removed): Initial caudomedial course of nasolacrimal duct. NLO or mistaken for debris because of its smaller than expected (arrow). Lateral edge of naris (arrowheads). diameter and unexpected location in the lateral wall of the naris. A spot of moisture or a mucoid plug, reported to be present at most NLOs of horses (Lavach 1990), was present at the NLO of most mules and aided in identification of the orifice. In the mules with NLO observed near to the location described for horses (Location B), there was more variation rostrocaudally and/or mediolaterally (up to 4 cm lateral to the mucocutaneous junction in one mule) than is typically observed in the horse, in our experience. Interestingly, the mules that had a NLO at Location B were all female. These individuals were not of common ancestry and different breeds were represented (e.g. one draught mule, 4 horse mules born to mares of different breeds). As no mules displayed NLO in the location of the mule’s sire, these findings suggest that the location of the NLO may be determined by sex-linked inheritance but our study population was too small to conclude the mode of inheritance or even if the location is Fig 7: Mid-sagittal section of 1-year-old mule head. Nasolacrimal heritable. duct has been injected with red latex casting material. It has been previously reported that horses and mules may have multiple NLOs, some of which may end as blind pouches while others may communicate with the main nasolacrimal location established for horses (Location B) and none of the 40 duct (Lavach 1990). In our study, 5/40 mules (12.5%) had mules were observed to have a NLO near the location multiple NLOs. All NLOs of 2 of these 5 mules were patent and described in the donkey (Fig 11). These findings demonstrate communicated with the main nasolacrimal duct, but the that the location of the NLO of the mule is typically different patency of the other 3 individuals was not investigated. The from that of the horse and the donkey and extrapolation from variability in location and number of NLOs reported in this study other equids in regard to the location of the NLO of the mule seems greater than that expected to be found in a horse is not reliable. population of similar size, but we can find no previous studies The NLO was found by visual examination alone in all that describe the variability in location and number of distal mules, although visualisation was slightly more difficult in black orifices among horses. These findings prompted us to survey a mules, light-coloured mules with spots of pigment on the nares, random group of clinically healthy university horses for

Fig 9: Dorsal oblique maximum intensity projection (MIP) CT image outlining the right nasolacrimal duct in a 7-year-old mule. The portion of the duct located medial to the premandible at the level of the diastema is the largest (arrows), a consistent finding in all specimens. Notice the tomcat catheter (open arrows) and contrast extravasation rostral to the duct opening (open arrowheads). Asterisk: first maxillary premolar. comparison purposes and we found 24/24 horses to have NLO in the established location for the horse and only 1/24 (4%) of these horses had multiple orifices (bilaterally), as compared to 12.5% of the mules in our study cohort. The nasolacrimal drainage apparatus of the horse is a common source of clinical problems, most often from obstruction (Freestone and Seahorn 1993). Obstruction of the nasolacrimal drainage system may be caused by congenital atresia or, more commonly, may be an acquired condition. Acquired obstruction is often secondary to dacryocystitis Fig 10: Representative transverse cross-sectional CT images of the arising from a number of causes, such as foreign bodies, nasolacrimal ducts at the level of diastema (a), fourth maxillary trauma, dacryoliths, rhinitis or neoplasia (Freestone and premolar (b) and second maxillary molar (c). Notice the Seahorn 1993). Recently, dacryocystitis has been reported to symmetric appearance of the ducts, which are largest in the rostral occur secondary to suture exostoses (Carslake 2009) and to portion (arrows, a), smaller and in close apposition to the bone margins at the level of the premolars (arrows, b) and contained periapical dental infection in both the horse and donkey within the lacrimal canal caudally (arrows, c). (Ramzan and Payne 2005; Cleary et al. 2011). Clinical signs of nasolacrimal obstruction include epiphora, mucoid ocular discharge and conjunctivitis of the affected side. A negative When disorders of the nasolacrimal apparatus are Jones test (failure of fluorescein stain applied to the eye to suspected, methods of diagnosis (e.g. endoscopy and appear at the NLO) is suggestive of obstruction which can be CT-DCG) and treatment (e.g. catheterisation and lavage) are confirmed with failure of normograde or retrograde lavage more easily performed by accessing the nasolacrimal duct (Carslake 2009). through the NLO because catheterisation of the lacrimal

(Fig 7). Anatomic landmarks for sinusotomy of the rostral and caudal maxillary sinuses of the horse were reliable when used for sinusotomy of the 2 mule heads and based on observations of the course of the nasolacrimal duct of the 4 cadaver heads, sinusotomy performed ventral to a line drawn from the medial canthus of the eye to the infraorbital foramen should not interfere with the nasolacrimal duct of the mule. Computed tomography is superior to radiography when evaluating the skull and CT-DCG has proven superior to radiographic dacryocystorhinography in the evaluation of the nasolacrimal apparatus for the presence of disease (Nykamp et al. 2004; Cleary et al. 2011; Rached et al. 2011). In this study, the morphology of the ducts was similar in all mules and appeared to be normal. Parasagittal and dorsal oblique reconstructions were especially useful because they allowed the entire length of the nasolacrimal duct to be evaluated in one image. Three-dimensional reconstructions were of limited use, because the mid-portion of the duct could not be clearly separated from the underlying bone margin. The variation in diameter observed along the course of the duct was a consistent finding in all mules. In this study, in order to avoid personnel exposure to ionising radiation, CT acquisition was performed immediately at the end of and not during contrast injection. It is possible that if the acquisition was performed during injection, additional distention of the duct, especially in its mid-portion, could be achieved. Although CT-DCG in mules is easy to perform and provides consistently good images of the nasolacrimal duct, it does require dedicated equipment (e.g. a large animal table) and general anaesthesia in live animals, which limit its widespread application.

Fig 11: Right naris of donkey showing the dorsal location of the Conclusion nasolacrimal orifice (arrow). Asterisk: Alar fold. The NLO and rostral portion of the nasolacrimal duct of the mule are anatomically different from that of the horse and punctum is more difficult and often requires heavy sedation or donkey. The NLO of the mule is typically located in the internal general anaesthesia (Carslake 2009). Knowledge of the cutaneous tissue of the lateral wall of the external nares and is variations in location of the NLO among species of equids is easily located by visual examination alone. Knowledge of the important when performing these procedures. Catheterisation anatomy of the nasolacrimal duct in the mule and especially of the nasolacrimal duct of the mule is easy to perform when the location of the NLO is essential for treatment of certain using a small diameter catheter (circa 3.5 Fr) and the duct can ocular diseases or disorders of the nasolacrimal system and the be flushed effectively in retrograde fashion, eliminating the location of the NLO should be established prior to performing need for cannulation of the lacrimal punctum in many cases. some surgical procedures of the head to avoid iatrogenic Endoscopy of the nasolacrimal duct, as previously described damage. for the horse (Spadari et al. 2011), may be difficult to perform in the mule because the diameter of the NLO is small in many cases and the flattened and tortuous path of the duct in the Authors’ declaration of interests tissue of the external naris may prevent introduction of the No conflicts of interest have been declared. endoscope in retrograde fashion. The anatomy of the nasolacrimal apparatus of the equid Source of funding must be considered before performing common surgical Funding for this project was provided by an internal grant from procedures of the head (e.g. repairing nasal lacerations, the Department of Large Animal Clinical Sciences, College of resection of redundant alar folds and sinusotomy). Lacerations Veterinary Medicine, University of Tennessee, Knoxville, of the external naris are common in equids (Hendrickson 2006), Tennessee. and a laceration of the external naris of the donkey and mule, unlike that of the horse, can be associated with damage to Acknowledgements the nasolacrimal duct. Failure to locate the NLO of a donkey or mule preoperatively before suturing a laceration of an Reese Brothers Mule Company with special thanks to Rufus, external naris or before resecting flaccid or redundant alar Vivian and Richard Reese, Mrs Kathy Pinkston, Drs Claude folds, could result in iatrogenic damage to the nasolacrimal Ragle, James Schumacher and Melissa Hines. duct. Gross dissection of the 4 cadaver heads confirmed that, except for the size and location of the NLO and the first few Manufacturers’ addresses centimetres of the nasolacrimal duct, the course of the 1Pfizer Animal Health, New York, New York, USA. nasolacrimal duct of the mule resembled that of the horse 2Akorn Pharmaceuticals, Lake Forest, Illinois, USA.

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