Incidence of Mange Infestation in Rabbits

Introduction
Rabbits are essential animals for farmers who raise them in many countries. Inadequate care and diseases are among the most critical challenges facing rabbit breeding (Asmare et al., 2016; Rodrigues et al., 2022). Skin diseases are among the most common diseases in rabbits (Kumsa et al., 2012), which cause severe economic losses due to complications such as alopecia, pruritus, inappetence, self-inflicted trauma, ear canker, and death (Abdelaziz et al., 2020). In Egypt, sarcoptic mange in rabbits was considered second after coccidiosis, recording the highest percentage of losses (Seddiek et al., 2013). Veterinary ectoparasites in rabbits are economically important parasites as they cause significant loss of weight, productivity, and wool quality, with exudative pruritic skin inflammation, severe erythema, and crust formation (Altamemy. 2014). Sarcoptes scabiei and Psoroptes cuniculi, Psoroptes cuniculi were the most common ectoparasites of rabbits (Nuru et al., 2017). The genus Demodex occurs in rabbits’ hair follicles, sebaceous glands, or epidermal pits (Abu Hafsa et al., 2021). Notoedres cati var. cuniculi infestation in rabbits is clinically manifested by the formation of scales and scabs of lips, nose, face, external ear canal, and other body parts (Rao et al., 2020). Cheyletiella spp. are large mites burrowing the keratin layer of the skin in humans and domestic animals, resulting in scales with pseudo-tunnels and debris on the skin surface (Cardells et al., 2021). Mange causes many losses, leading to morbidity and mortality rates. In Spain, the epidemic rate has reached 81% of the wild population (León-Vizcaíno, 1999). Due to the lack of studies on scabies in rabbits in Iraq, and given its importance in veterinary and health problems, we decided to investigate the mange infestation of rabbits.

Materials and Methods

Study animals
A total of 130 rabbits (56 males and 74 females) were examined for lesions on different parts of the body such as the head, nose, ear canal and pinnae, lips, neck, breast, brisket, legs, feet, back, and genitalia (Taylor et al., 2016).

Skin scraping
Skin scrapings were taken from rabbits with some clinical signs of mange following the method described by some researchers (Solikhah et al., 2021; Ola-Fadunsin et al., 2023). The skin-scraping samples were transferred to the laboratory of parasitic diseases at the College of Veterinary Medicine at University of Mosul. We followed all instructions and methods of animal welfare laws in accordance with the guidelines of the International Animal Ethics Committee or the Institutional Ethics Committee, as well as the local laws and regulations.

Laboratory tests
The scraped parts were placed in tubes containing 5 mL of KOH 10%; the tubes were placed in a water bath at 60-80°C for 15 minutes and centrifuged at a speed of 1500-2000 rpm for 5 min, then the supernatant was discarded, and some drops of sediment were placed on a glass slide with cover slide (Yasine et al., 2015). The scabies species were diagnosed based on morphological characteristics using the identification keys (Taylor et al., 2016). Data were analyzed by SPSS software, version 17 (SPSS Inc., Chicago, USA) using the chi-square test.    

                      
Results
In this study, of 130 examined rabbits, 56(43.1%) were naturally infected with several types of mange. The results revealed that S. scabiei var. cuniculi infected 50 (38.5%), Psoroptes cuniculi 32(25%), N. cati var. cuniculi 26(20%), D. cuniculi 12(9%), and Cheyletiella spp. 4(3%) (Table 1 and Figures 1, 2 and 3).

Regarding the organ susceptibility to mange infestation, the results showed that the highest infestation was seen in the abdomen and back, while the lowest infestation rate was found on the tail and perineal area. The infestation rate, the typical lesions of symptomatic rabbits, and the sites of those lesions are listed in Table 2.

The highest rate of infested sites (alopecia, pruritus, and hyperkeratosis) was found on the abdomen and back, while the lowest lesion rate (alopecia) was found on the tail and perineal area (Figure 4).

Based on animal age, the percentage of infestation in the group of animals under one year was 63.3%, while 25% in animals more than one year old. The chi-square test showed a significant difference (P≤0.05) in the percentage of infestation in relation to the animal age. In contrast, no significant differences were observed between the males and females of the same age (Tables 3 and 4). Results of the current study revealed significant differences (P<0.05) among three types of infestation (single, double, and mixed).

 
Discussion 
Mites cause highly contagious skin diseases in rabbits, which influence these animals’ health and productive capacity in many countries (Sant & Rowland, 2009). The present study distinguished the morphological characteristics of S. scabiei var. cuniculi, such as size, which ranged between 320-500 µm in length and 250-410 µm in width. These results agreed with that of Elshahawy et al. (2016), who found that the size of S. scabiei var. cuniculi was 300-504 µm in length and 230-420 µm in width. Psoroptes cuniculi have an oval body shape with pointed mouth parts, as described by Nonga and Mkula (2015). Results of the current study revealed other morphological characteristics of N. cati var. Notoedres cati, D. cuniculi, and Cheyletiella spp, which were similar to those found by Elshahawy et al. (2016).
The results of this study clarified that the percentage of infestation with S. scabiei var. cuniculi was 38.5%, which was too close to the infestation rate with the same mite on sheep (34.6%) and on rabbits (41.6%) as reported by Shahatha et al. (2022) whereas the infestation rate with Psoroptes cuniculi, N. cati var. cuniculi, D. cuniculi and finally Cheyletiella spp. were 25%, 20%, 9%, and 3%, respectively. However, these rates disagreed with the results of Hoshem (2014), who stated that the percentages of P. cuniculi, N. cati, and Cheyletiella spp. were 7.55%, 3.43%, and 1.51%, respectively. These differences could be attributed to the number of animals examined and the management’s performance. On the other hand, our results agreed with Shahatha et al. (2022), who reported that the infestation rate with S. scabiei in cows was 37.5%. The most frequent lesions in rabbits were hyperkeratosis on the head and ears (26.8%), then the abdomen and back (57.1%), and finally on the legs (44.6%), while the alopecia came in the second place after hyperkeratosis and its rates are 26.8% on the head and ears, 57.1% on the abdomen and back, and 19.6% on the tail and perineal areas.
Pruritus was the third noticed lesion on the infested animals, especially in the head and ears (26.8%) and then the abdomen and back (57.1%). These results agreed with those reported by Shahatha et al. (2022), who concluded that hyperkeratosis had the highest lesion rate at 40% while pruritus had the lowest at 20%. This study showed that the youngest animals had a greater infestation rate than those above one-year-old. The infestation rates were 68% for males and 63.3% for females under one-year-old (youngest animals), while 29% for males and 25% for females more than one year old. Our results were similar to the findings of Elshahawy et al. (2016), who reported a higher infection rate in younger rabbits (29%) compared to oldest animals (19.3%). This result could be attributed to keeping more than several age groups of animals together, which might have infestation via direct contact. 
The results of the current study revealed no significant differences between males (46.4%) and females (40.5%) regarding the infestation rates with mange, which agreed with the results of Shahatha et al. (2020) and Arul Prakash et al. (2017). Finally, this research found significant differences among three types of infestations (single, double, and mixed). The double one had the highest rate at 50%, followed by mixed infestation at 33.9%, and finally, the single one had 16.1%. These results closely resembled those obtained by Choe et al. (2020) and Ammam et al. (2022), who showed that rabbits could infest with more than one species of mange mites simultaneously.

Conclusion 
The rabbits of Mosul City were infested with several species of the mange with different percentages. It is necessary to establish control via treatment with potent drugs and maintain the hygiene of the rabbit’s environment. Also, the most vulnerable age group to the many species of mange mites was less or equal to one year.

Ethical Considerations

Compliance with ethical guidelines
Ethical approval was issued by the Institutional Animal  Care and Use Committee, the College of Veterinary Medicine, University of Mosul, on October 2, 2022 (Code: UM.VET.2022.20),

Funding
This research did not receive any grant from funding agencies in the public, commercial, or non-profit sectors. 

Authors' contributions
All authors equally contributed to preparing this article.

Conflict of interest
The authors declared no conflict of interest.

Acknowledgments
The authors would like to thank the College of Veterinary Medicine, University of Mosul.

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