Mammomonogamus auris infection in the middle ear of a domestic cat in Saipan,Northern Mariana Islands,USA

Abstract

A 2-year-old female domestic shorthair cat on the island of Saipan was presented to a local veterinarian for headshaking. Otoscopic examination showed mild erythema of the right tympanic membrane, but was otherwise unremarkable. Headshaking resolved with topical gentamicin/betamethasone/clotrimazole therapy; however, erythema persisted. Further otoscopy revealed movement of the erythematous region, which was in fact the red-colored strongylid nematode, Mammomonogamus auris, residing within the middle ear. Myringotomy and a saline flush were performed under heavy sedation. A silastic tube was inserted into the incision and the worms were retrieved by applying negative pressure. Follow-up treatment included topical thiabendazole/dexamethasone/neomycin ointment as well as selamectin. Mammomonogamus auris has previously been documented only three times, once each in China, Sri Lanka and Japan. This is the first report of M auris in cats from Saipan.

A 2-year-old, spayed, indoor/outdoor, domestic shorthair cat presented to the Paradise Island Animal Hospital on the island of Saipan with a complaint of headshaking. Routine otic examination with a Welch Allen otoscope revealed erythema of the right tympanic membrane. No signs of otitis externa were present. The cat was discharged with topical gentamicin/betamethasone/clotrimazole ointment (Otomax; Schering-Plough), to be applied twice a day in both ears for 10 days. On recheck examination 10 days later, the headshaking had resolved but erythema of the tympanum persisted. Closer otoscopic examination revealed movement of the erythematous region. Myringotomy was performed with the cat under tiletamine sedation (Telazol; Wyeth) to retrieve the moving object. Silastic tubing, attached to a 3 cc syringe, was passed through the incision. The middle ear was flushed with saline, after which application of negative pressure with the syringe allowed for the retrieval of two red vermiform organisms, approximately 10 mm in length. Smaller pinkish-white organisms, approximately 2.5 mm in length, were also detected and removed. The cat recovered without incident; it has not returned to the clinic for the recommended follow-up examinations. Later examination of the parasitic organisms established them to be Mammomonogamus auris, with the large worms being females and the small worms being detached males.

The strongylid nematode M auris (formerly Syngamus auris) was first reported by Faust and Tang (1934) in Fuzhou, China. The same species was later identified in Kandy District, Sri Lanka by Seneviratne (1954) and in Saitama prefecture in Tokyo, Japan by Sugiyama et al (1982). This paper represents the fourth report of this parasite to date, and is the first from Saipan, one of the Northern Mariana Islands southeast of Japan. M auris has also recently been found during the examination of a cat from the neighboring Mariana island of Rota, 45 miles away. It has not been reported from the US Territory of Guam, some 120 miles south of Saipan.

Since this first case, the parasite has been detected many times during routine otoscopic examinations at the Paradise Island Animal Hospital. A video-otoscope (Endoskope and Veterinary Camera System; Karl Storz) was acquired to capture images of the worms living and moving behind the tympanum (Fig 1, plus the associated Supplementary data video found at doi:10.1016/j.jfms.2008.02.007). Approximately 10 out of 1440 cats examined per year at this hospital have been found to be infected with M auris. These animals range from 9 months to 12 years of age, and are indoor/outdoor pets or live strictly outdoors. Most cats are asymptomatic for infection. Typically only one pair of worms is found unilaterally, although several cats have had bilateral involvement with up to four worms in the middle ear. Up to eight pairs of worms have been reported previously in a single ear (Sugiyama et al 1982).

Fig 1.

Video-otoscopic image of a female Mammomonogamus auris as viewed through the intact tympanic membrane. Water has been instilled in the outer ear to improve image clarity. The bright red female can be seen in the center of the image, with its pink ovarian tubules and uteri clearly visible. The manubrium of the malleus is seen directly in front of and dorsal to the worm.

Typical physical examination findings include apparent erythema of the tympanic membrane – which is actually the scarlet worm being seen through the tympanum – with no signs of aural disease. No clinical signs aside from headshaking have been associated with M auris infection. Diagnosis is made by observing movement of the worms during otoscopic examination, or by detection of M auris eggs on fecal centrifugation flotation (Faust and Tang 1934).

Ryzhikov (1948) created the genus Mammomonogamus to distinguish the worms in mammals from a similar genus in birds, Syngamus. In both genera, the adult male and female worms are found permanently in copula, with the bursa of the male appressed tightly to the female over the area of the vulva (Fig 2). One marked difference, however, is the lack of an operculum on the Mammomonogamus species egg. During life, the M auris female is bright red and measures 14–30 mm in length, while the male is orange red and markedly smaller, measuring between 3.3 and 8.1 mm (Faust and Tang 1934). Four female specimens were retrieved intact from cats in Saipan and fixed in 10% formalin. These averaged 17.6 mm (range: 16.0–18.5 mm) in length and 0.85 mm (range: 0.7–0.9 mm) in width. Six intact males averaged a length of 5.0 mm (range: 3.8–6.0 mm) and a width of 0.46 mm (range: 0.4–0.5 mm) [Specimens submitted to the US National Parasite Collection, Beltsville, MD, Accession number: USNPC 100477].

Fig 2.

Adult male and female Mammomonogamus auris worms after 10% formalin fixation (white bar=3.0 mm). The smaller white-colored male (5.4 mm) is permanently joined in copula to the larger brown-colored female (18.5 mm), whose vulva is located one third of the body distance from the anterior end. Note that the posterior end of the female narrows abruptly into a sharp point. Inset: The four-celled stage of an M auris egg, collected from the formalin vial containing the adult specimens (black bar=50 μm).

M auris lives in the middle ear of the feline host and can often be seen through the tympanic membrane. Eggs are passed down the Eustachian tube into the nasopharynx where they are swallowed and then shed in the feces. They are laid in the four- to eight-celled morula stage with a thick, transparent, sculptured shell, and are typically found in feces in the eight-celled stage (Sugiyama et al 1982). Free eggs recovered from the vial of preserved worms from Saipan measured 85–108 μm in length and 50–68 μm in width (Fig 2 inset).

Other Mammomonogamus species have been described (Sugiyama et al 1982). Species in the domestic cat include M ierei from the nasal cavity in the Caribbean islands, and M mcgaughei from the frontal sinus, nasal cavity, and pharynx in Sri Lanka. Species from wild felids include M dispar from the trachea of a puma in Brazil, and M felis from the bronchi of a tiger in Malaysia. The type species M laryngeus and a number of other species have been described from cattle, other ruminants, elephants, hippopotami, okapi, and orangutans (Foitová et al 2007). People have, on occasion, been infected with M laryngeus, mainly from tropical America (Nosanchuk et al 1995).

The life-cycle of M auris after fecal egg shedding has yet to be elucidated. It is unknown how infection is propagated and how the adult worms reach the middle ear. The tympanum is intact in all cats examined, and, therefore, it is unlikely that the worms enter through the outer ear. The requirement for an intermediate host in the life-cycle has been postulated for other Mammomonogamus species. Buckley (1934) introduced M ierei larvae into the oropharynx of two cats and two kittens, but none developed patent infections. One of the non-inoculated control cats, however, did begin shedding Mammomonogamus eggs. The lack of infection after direct inoculation suggests that larvae cannot develop without an intermediate host. After initiation of infection in the cat, the worms mature either in the trachea, larynx, nasal sinuses, or middle ear and are able to move between these locations via the Eustachian tube, nasopharynx, and laryngopharynx. This assumption is based on observation of worms in situ, and the ability of pairs of M auris to disappear from the middle ear into the Eustachian tube during examinations.

M auris infections can be treated with myringotomy and worm retrieval. Alternatively, instead of using a silastic tube to remove the worms, an endoscopic cytology brush can be advanced into the middle ear to entangle the worms, allowing for easy removal. Myringotomy may not be necessary in all cases. When saline solution is instilled in the external ear canal to improve video-otoscopic image clarity, worms sometimes disappear from the middle ear. They are subsequently found in the oropharynx, esophagus, or expelled from the nares during a sneeze, and can, therefore, be non-invasively removed.

Follow-up medications prescribed empirically for all cases to date have included an otic preparation of thiabendazole/dexamethasone/neomycin (Tresaderm; Merial) twice daily for 10 days and a single application of topical selamectin (Revolution; Pfizer). Otoscopic examinations are regularly performed post-treatment to verify that neither further worms nor worm movements are seen behind the tympanum. Two cases of re-infection have been observed in cats from households with multiple infected cats; these were also outdoor cats with access to the nearby jungle.

Mammomonogamus auris is a strongylid nematode that lives in the middle ear of domestic cats. Though it was discovered over 70 years ago, knowledge of its complete life-cycle is still lacking. To date, this species has only been found in Asia, and reports of infection have been few. The low number of cases in a few limited geographic foci may be due to under-diagnosis from the lack of clinical signs associated with infection, or may be related to environmental, host or parasite factors as yet unknown. Once infection has been diagnosed, myringotomy or saline ear flush in combination with topical medications appears sufficient to completely remove the parasites. Re-infection appears to be associated with lifestyle factors, such as outdoor access and living in a multiple cat household, perhaps because the likelihood of re-exposure is increased.

Appendix. Supplementary material

Supplementary material associated with this article can be found in the online version, at doi:10.1016/j.jfms.2008.02.007.