Rabbit Fur Mite (Listrophorus gibbus) Infestation of New Zealand White Rabbits

MAREK A. NIEKRASZ, DVM, JAMES L. CURL, DVM, AND JOAN S. CURL, PHD

Abstract ͉ The prevalence of Listrophorus gibbus infestation in seven groups of New Zealand White female rabbits that were purchased from the same source was determined by microscopic examination of hair tufts collected from affected rabbits. Thirty- nine of 52 (75%) rabbits were infested, although there was variation in the degree of infestation for each group (ranging from 0 to 100%). The infestation did not spread to other rabbits that had been housed in the same room for 72 h. Infested rabbits were treated with a commercially available carbamate-based acaricide, which effectively eliminated infestation with one application ( 3 groups) or two applications at a 5 to 7-day interval (4 groups). Cross-infestation was prevented by use of strict isolation, and eradication was easily accomplished with the use of available acaricides.

Rabbit fur mites (Listrophorus gibbus) were first described by to 21.1ЊC), relative humidity was 20 to 31%, and a 14-h light:10- Pagenstecher in 1862 as a fur mite of wild Oryctolagus cuniculus h dark cycle was used. Rabbits were housed in stainless-steel cages, in Austria (1). They are commonly found in India (2) and have fed a commercially available diet (Teklad Rabbit Diet, Harlan been reported in Great Britain (3), Puerto Rico (4), France, Sprague Dawley, Inc., Indianapolis, IN), and received water via Germany (5), Eastern Europe (6), Australia, and New Zealand an automatic system. (7). They also have been found on domestic Oryctolagus spp. in Examination and Treatment: Mites were not detected during two commercial rabbit facilities in the state of New York (8). the initial physical examination of the first group of rabbits. Three Mites have been found on wild and domestic as well as albino days after the Group 1 rabbits arrived, the investigators noticed and pigmented Oryctolagus rabbits (Champagne, Checker, Dutch tiny dark specks on the pelage of the tail of one of the rabbits Belted, Hare Brown, New Zealand White, New Zealand Red, and and notified the attending veterinarian. All six rabbits were im- Sable) (8) and wild Lepus rabbits and hares in the United States mediately examined, and hair samples were collected by means (5). Mites are difficult to detect, because they are small and do of plucking. A sufficient amount of hair was collected to cover not produce overt disease (5,8). Therefore, their incidence may the clear (non-frosted) portion (25 x 56 mm) of a standard 25 x be greater than reported. Because clinical disease has not been 75-mm glass slide with a layer approximately 1 to 5 hair shafts in associated with even heavy infestations (8), L. gibbus is consid- thickness. When personnel could readily see the mites on the ered a nonpathogenic obligate parasite (6,8,9). However, Bull rabbits, hair samples were collected from two areas. When mites (7) reported thinning of hair in wild rabbits infested with a large were not readily observed on the rabbits, hair samples were col- number of mites. lected from five to seven locations on each rabbit. The best Adult and larval stages of this non-burrowing parasite (10) anatomic location to pluck hairs for examination was the ven- may be encountered on a single rabbit host (5), where they re- tral aspect of the tail. main attached to hair shafts and feed on sebaceous secretions Hair samples were examined by using a light microscope (mag- and epithelial scales (1,3,9). Mites may complete their life cycle nification of 40 to 100X). Mineral oil was used to keep hair samples on a single host (5). Listrophorus gibbus has not been recognized on the glass slides and allowed us to use cover slips. Mites were as a vector or the primary cause of diseases specific to rabbits or collected and stored in a solution of 70% isopropyl alcohol. Group any zoonotic disease (9). 1 rabbits were not removed from the room, even though they were housed with non-infested rabbits, because the infested rabbits al- Materials and Methods ready had been there exposing the non-infested rabbits to mites Animals: We purchased 52 female New Zealand White rabbits for 72 h. Also, we wanted to investigate whether the infestation from a USDA-licensed rabbit facility during February through would be transmitted using conventional housing conditions. December. Only old (> 36 months) female rabbits were purchased However, all Group 1 rabbits were treated with a commercially because of the inability to secure a reliable supply of males of this available powder used to treat flea and tick infestations (Flea & age. A few young rabbits were used as control subjects. Rabbits Tick Powder, Carbaryl [1-Naphthyl N-methylcarbamate 5%], Vet- arrived in seven shipments, and each shipment was designated as Kem/Sandoz Ltd., Dallas, TX]. Rabbits received treatment as soon a group as follows: Group 1, n = 6; Group 2, n = 13; Group 3, n = 7; as the infestation was detected (72 h after initial contact with non- Group 4, n = 12; Group 5, n = 4; Group 6, n = 4; and Group 7, n = infested rabbits in the same room). Treatment was administered 6. All rabbits in Groups 2, 4, 5, 6, and 7 as well as four rabbits in on the basis of the manufacturer’s recommendation. The acari- Group 3 were greater than 36 months old. Three rabbits in Group cide was liberally sprinkled on the fur about 1.5 cm on each side of 3 and three in Group 1 were 3 months old, two rabbits in Group 1 the dorsal midline from the external occipital protuberance to were two months old, and one rabbit in Group 1 was more than 30 the base of the tail as well as on the entire tail. It was then gently months old. Body weight ranged from 1.65 to 5.10 kg. rubbed into the fur until it was no longer visible. Animal husbandry: Rabbits were housed in conventional rooms Special isolation procedures were not instituted. Rabbits were of an AAALAC, International-accredited facility and cared for frequently monitored to detect signs of toxicosis for 3 to 5 h according to the principles outlined in the Guide for the Care and after application of the acaricide, and then daily by three mem- Use of Laboratory Animals. Rooms had more than 10 air changes/ bers of the veterinary staff. Rabbits were re-examined 5 to 7 days hour, ambient temperature was maintained at 67 to 70ЊF (19.4 after initial treatment. The vendor was notified of the problem, but did not treat sub- Center for Experimental Animal Resources, Northwestern University, Chicago, IL sequent rabbits for mites. During initial examination, one of the

Volume 37, No. 4 / July 1998 CONTEMPORARY TOPICS © 1998 by the American Association for Laboratory Animal Science 73 rabbits in the next shipment (Group 2) had Table 1. Results of examinations and treatment of rabbits infested with Listrophorus gibbus mites; therefore, all Group 2 rabbits were iso- Group lated, treated, and scheduled for another examination. For isolation procedures, the 1234567a caretaker and investigative staff wore dispos- Variable (6) (13) (7) (12) (4) (4) (6) able outer garments, shoe covers, and gloves Exams 1,8,12,20 1,6,10,14,21 1,7,13,21 1,6,10,14,21 1,6,10,84 1,6 1,7,41 while in that room. Furthermore, that room was the last to be entered each day. Mites were (day) found on all Group 2 rabbits at the examina- Treatments 1 1, 6 7 1, 6 1, 6 1 7a tion 6 days after the initial treatment, and all (day) received a second treatment of acaricide. Live mites +- - - ++- - - -+- - ++- - - ++- - - - +- - Rabbits in subsequent shipments (Groups 3 through 7) were isolated on arrival, visually Dead mites ++- - ++- - -+- - +++- - ++- - - - ++- checked for mites, and hair samples were aRabbits treated by vendor on the day before delivery. Numbers in parentheses No. of rabbits. plucked, as previously described, for exami- + = mites detected during examination. - = mites not detected. nation by means of light microscopy. All rabbits in these groups were treated with acaracide and exam- 5 of 6 rabbits in Group 1 had mites. However, mites were found ined 5 to 7 days later. When rabbits were found to be infested on only 2 of 4 rabbits in Group 5 and 1 of 7 rabbits in Group 3, with mites at the second examination, they were given a second and mites were not found on any of the 4 rabbits in Group 6. treatment of acaricide. One application of acaricide to rabbits of Groups 1, 3 and 6 Investigators used one rabbit in Group 3 in a study two days eradicated the mites. Rabbits in the other four Groups (2, 4, 5 after arrival and another Group 1 rabbit four days after arrival. and 7) required a second application 5 to 7 days later to achieve The remaining five rabbits in Group 1 were re-examined on day eradication of the mites. Four rabbits from Group 5 and five 7 after arrival. Shortly after re-examination (1 or 2 days), two rabbits from Group 7 were examined 84 and 41 days, respec- additional rabbits were used in that study, and only three re- tively, after arrival, and mites were not found. mained for further monitoring of mite infestation. One rabbit in Group 1 died 3 days after treatment for mites. The vendor was notified of the continuing problem and advised Upon necropsy it was discovered that it had developed aspira- of eradication methods. Rabbits in Group 7 were treated with aca- tion pneumonia most likely related to anesthesia and surgery ricide by the vendor one day before shipment. Because there were that had been performed two days prior to treatment for the live mites on them when they arrived, these rabbits were also iso- mites. Another rabbit in Group 4 was treated with enrofloxacin lated and scheduled for another examination 5 to 7 days later. for respiratory infection and died on day 8 of treatment. It had Two shipments of rabbits from this vendor were not included developed purulent pericarditis and pneumonia. Three rabbits as part of the data. One shipment (five rabbits) was used for in Group 2 were also concurrently treated with enrofloxacin for experiments within 48 h after arrival and was housed in isola- different degrees of mastitis. tion facilities, but these rabbits were not examined or treated Using conventional housing conditions, mites did not readily for mites. Another shipment (four rabbits) was inadvertently infest other rabbits. Mites were not found on rabbits from other placed in a conventional room with rabbits from other vendors. vendors that were housed in the same room for 72 h or rabbits Two of these rabbits remained in the room for 1 week, another cared for by the same caretaker in adjacent rooms. Similarly, for about 2 weeks, and the fourth for approximately 4 weeks. the cats and guinea pigs did not become infested with mites. None of these rabbits were examined or treated for mites. Hair loss was not observed. Rabbits consumed typical amounts Non-infested rabbits: We examined 20 rabbits (all purchased of food and water. Fecal and urine quality and quantity were within from a different vendor) that had been housed for 72 h in the expected limits. Excessive grooming or scratching was not observed. same room as the Group 1 rabbits. Some of these rabbits were Small (0.2 to 0.5 mm in length) brown specks attached to hair housed on the rack immediately adjacent to infested Group 1 shafts were observed during examinations of rabbits. Parasites were rabbits. We also examined 20 rabbits located closest to the door always found on or near the tail. In heavy infestations, they were of a room used to house rabbits obtained from a third vendor. also found on the medial and lateral aspect of both thighs and the That room was approximately 15 m from the room used to house caudal portion of the abdomen. Most parasites were attached to the infested Group 1 rabbits. The same caretaker provided care the distal or middle third of the hair shaft. We did not find para- for both rooms of rabbits. Special precautions, such as use of sites on the head, neck, forelimbs, or thoracic area. Younger rabbits gloves, shoe covers, disposable garments, or acaricidal agents, to appeared to be less heavily infested than older rabbits, although prevent transmission were not taken by the caretaker during the we did not attempt to quantify this observation. initial 72 h. Microscopic examination revealed parasites that appeared After the Group 2 rabbits were used by the investigators, the brown, ovoid, and slightly compressed laterally. In adult mites, room in which they had been housed was sanitized (NPD, Calgon four pairs of short legs and a dorsal protuberance of chitin pro- Vestal, St. Louis, MO). Ten cats were placed in the room, and jecting over their mouthparts were evident. Female mites were they were examined 7 days later for mites. Guinea pigs (a total slightly larger than male mites, which had a large caudal clasp- of 20; 10 each for two periods) housed in a room 18.5 m from ing organ (Figure 1). Larval forms at various developmental the room used to house mite-infested rabbits were also checked stages with three pairs of legs were also found, but we did not for mites. The same caretaker provided care for the Group 2 detect any eggs. Most parasites were found attached to the hair rabbits and the guinea pigs. shafts by means of two chitinous lips; dead mites often had their legs clasped around the hair shafts. The movement of live mites Results was expressed mainly through moving their legs (particularly Results of examination and treatment of rabbits were recorded the second, third and fourth pairs). (Table 1). Thirty-nine of 52 (75%) rabbits from a single vendor were infested with L. gibbus. The degree of infestation among Discussion shipments was variable. All the rabbits in Groups 2, 4, and 7 and Listrophorus gibbus has not been reported frequently in the

74 CONTEMPORARY TOPICS © 1998 by the American Association for Laboratory Animal Science Volume 37, No. 4 / July 1998 roof rats (8). As a point of interest, we examined two non-lago- morph species (guinea pigs and cats) that were possibly exposed. In each case, we did not detect evidence of transmission. These findings do not prove that cross-species or within species infesta- tion under laboratory conditions is impossible. However, we concluded that it does not readily take place even when using conventional housing conditions, and transmission can be eas- ily prevented by use of standard isolation techniques. Because L. gibbus apparently spend their entire life cycle on the host, a combination of isolation and use of available acaricides easily accomplishes eradication. We treated the rabbits with a flea and tick powder that proved to be highly effective. One ap- plication of powder eradicated mites in 3 groups of rabbits, and a second treatment eradicated mites from the other four groups. Mites were not found during follow-up examinations of Group 5 and 7 rabbits 84 or 41 days after initial treatment. Rabbits were frequently observed after application of acaricide, and none of the rabbits exhibited signs of toxicosis. We closely monitored rab- bits in groups 1 through 4 for a period of three weeks. We concluded that two applications of acaricide were sufficient to eradi- cate mite infestations and that the treated rabbits (regardless of the degree of infestation) could be safely introduced into a popu- lation of non-infested rabbits 7 days after the second treatment. Taxonomy experts claim that the proper generic name for this mite is Leporacarus (11), despite widely used Listrophorus.

Acknowledgments The authors thank Ms. Amy L. Schmudde, Ms. Young J. Rhee, and Ms. Janet Martinez for their technical assistance with the study, Ms. Sheila Macomber for the art work, and Dr. Douglas B. Larsen for language translation.

References 1. Pagenstecher, H. A. 1862. Listrophorus gibbus. Nebst FIG. 1. (a) Ventral and (b) lateral view of an adult female Listrophorus Nachtraglichen Bemerkungen uber Listrophorus leuckarti. Z. gibbus. (c) Ventral and (d) lateral view of an adult male L. gibbus. Wiss. Zool. 11:156–161. 2. Flynn, J. R. 1973. Mites, p. 425–492. In Flynn, J. R. (ed.), United States. Reports are especially rare for rabbits housed in Parasites of laboratory animals. 1st ed. Iowa State Univer- laboratory animal facilities. Mites are difficult to detect because sity Press, Ames, Iowa. of the lack of clinical signs, lack of movement on the fur, and 3. Mead-Briggs, A. R. and A. M. Hughes. 1965. Records of mites the preferred site of attachment on the underside of the tail. and lice from wild rabbits collected throughout Great Brit- Even after observing mites on Group 1 rabbits, investigators failed ain. Annu. Mag. Naturist. 8:695–708. to identify mites on 12 of 13 rabbits during the initial exam of 4. Tamsitt, J. R. and I. Fox. 1970. Mites of the family Group 2. Thus, this parasite may have a substantially higher inci- Listrophoridae in Puerto Rico. Can. J. Zool. 48:398–399. dence in rabbits in laboratories than is appreciated (8). This 5. Kraus, A. L. 1974. Arthropod parasites, p. 287–315. In may be true for small vendors whose preventive health programs Weisbroth, S. H., R. E. Flatt, and A. L. Kraus (eds.), The for animals may be less rigorous than large commercial vendors. biology of the laboratory rabbit. Academic Press, Inc., New The vendor from which we obtained the rabbits described here York, NY. has supplied our institution with rabbits for several years and 6. Wasylik, A. 1965. Studies on the European Hare. VIII. Dy- was able to provide rabbits of the required age, whereas other namics of occurrence of Listrophorus gibbus Pagenstecher, vendors could not supply us with our requested rabbits. The ven- 1862. Acta Theriol. 10:27–54. dor was contacted several times in an attempt to find the source 7. Bull, P. C. 1953. Parasites of the wild rabbit, Oryctolagus cu- of mites and to assist in eradication efforts. However, the vendor niculus (L) in New Zealand. N. Z. J. Sci. Technol. 34:341–372. was unable to help in identifying the source of infestation. The 8. Weisbroth, S. H. and S. Scher. 1971. Listrophorus gibbus (Aca- vendor’s facility reportedly is well isolated from wild rabbits and rina: Listrophoridae). An unusual parasitic mite from uses a closed breeding program. The vendor’s veterinarian did laboratory rabbits (Oryctolagus cuniculus) in the United not find mites; however, only two rabbits were examined. States. J. Parasitol. 57:438–440. The parasites do not appear to be easily transmissible when 9. Hofing, G. L. and A. L. Kraus. 1994. Arthropod and helm- conventional laboratory animal conditions are used. Rabbits from inth parasites, p. 231–257. In Manning, P. J., D. H. Ringler, another vendor that were housed for 72 h in a cage immediately and C. E. Newcomer (eds.), The biology of the laboratory adjacent to the rack of infested rabbits did not become infested. rabbit. 2nd ed. Academic Press, Inc., San Diego, CA. Additionally, rabbits in an adjacent room also did not become 10. Kraus, A. L., S. H. Weisbroth, R. E. Flatt, et al. 1984. Biol- infested even though the same caretaker provided care for both ogy and diseases of rabbits, p. 207–240. In Fox, J. G., B. J. groups of rabbits. Cohen, and F. M. Loew (eds.), Laboratory animal medi- Although other authors have referred to the parasite as a rab- cine. Academic Press, Inc., Orlando, FL. bit fur mite, there is one report that identified the parasite on 11. O’Connor, B. M. 1998. Personal communication.

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