# Invited review: Camel skin diseases survey in Morocco

Asma Kamili, Bernard Faye, Mohammed Bengoumi, Nour Said Tligui

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Asma Kamili, Bernard Faye, Mohammed Bengoumi, Nour Said Tligui. Invited review: Camel skin diseases survey in Morocco. Journal Of Camelid Science, 2019, 12, pp.1-16. hal-05174777

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# Invited review: Camel skin diseases survey in Morocco

Asma Kamili<fnref n="1" />, Bernard Faye<fnref n="2" />*, Mohammed Bengoumi³ and Nour Said Tligui⁴

## Abstract

The present study aimed to collect data related to skin diseases in dromedary camels in the south of Morocco. As a whole, 168 herds from 9 provinces located in the south of Morocco have been prospected. Finally, 275 camels were involved in this monitoring, presenting 336 skin disease cases with different etiologies (bacterial, viral and parasitic). Mite and dermatophyte infections were predominant with 52% and 30% as respective proportions. On average, 11% and 7% of all cases detected suffered respectively from lymphadenitis and camelpox/ecthyma. Skin diseases in dromedary camels are highly affected by the animal's sex, as females were more affected than males; age seemed to have no effect. The absence of systematic treatment and prevention, even though these infections are all treatable, may somehow explain the recidivism of skin diseases in the herd every year.

**Keywords:** Arabian camel, *Camelus dromedarius*, mange, Morocco, ringworm, skin diseases

*Corresponding author: Dr Bernard Faye, bjfaye50@gmail.com

## Introduction

The Arabian camel (*Camelus dromedarius*) is a rustic animal presenting fewer infectious diseases than cattle, but still vulnerable to skin diseases. Faye et al. (2000) reported that mineral metabolism particularities in camels are distinguished by a remarkable adaptability to mineral under-nutrition and some specificities as increasing of absorption and storage capacity in scarcity periods, tolerance of minerals' excess and maintenance of enzymatic activity in a deficient period. However, a reflection on camel sensitivity to skin diseases suggests that exposure of camels in southern zones in Morocco to prolonged periods of drought may have caused deficiencies in certain minerals which are essential for skin integrity.

Skin diseases are of major concern to farmers in southern Morocco, especially sarcoptic mange, a contagious disease that impact on production, which makes it a redoubted disease among farmers (Khallaayoune et al., 2000; Kumar et al., 1992).

The present study, conducted in the framework of a survey in nine provinces in southern Morocco, aims to collect data on herd management and to make appropriate diagnosis of skin diseases in camels in areas characterized by high camel populations.

The main objectives of the present study were:

- to determine the relative proportions of skin diseases in the camel population in the southern provinces of Morocco,

<footnote n="1">¹Office National de Sécurité Sanitaire des Produits Alimentaires, Rabat (Maroc);</footnote>

<footnote n="2">²U.M.R SELMET, C.I.R.A.D-ES, Montpellier (France); ³Regional Office F.A.O, Tunis</footnote>

<footnote>(Tunisie); ⁴Institut Agronomique et Vétérinaire (I.A.V) Hassan II, Rabat (Maroc)</footnote>
- to identify risk factors related to the appearance and persistence of skin diseases in camels, and

- to assess the application of medical and preventive measures.

## Material and methods

### Survey

The survey was conducted in 9 provinces (Figure 1) located in southern Morocco. Overall, 168 herds of camels were selected randomly and monitored. The number of selected camel herds in each province varied according to the local concentration of camels. The distribution of the herds was 20 in Boujdour, 52 in Dakhla, 10 in Essaouira, 12 in Guelmim, 19 in Laayoune, 14 in Ouarzazate, 12 in Smara, 19 in TanTan and 10 in Tata province.

<figure><img src="image_2.png" /><figcaption>**Figure 1:** Geographical distribution of the Moroccan provinces involved in this skin diseases survey</figcaption></figure>

The survey was based on a questionnaire developed to meet the above objectives. This questionnaire consisted of two sheets:

* Herd form: A sheet was filled in for each herd visited and containing at least one camel

with skin lesions. It was used to collect data about owner, herd size and composition, herd management system, herd health history and prophylactic and curative measures implemented by the owner.

* Clinical form: An individual sheet was completed for each animal presenting skin lesions. It was conceived in order to record data related to the animal (age, sex and breed) and to describe detected lesions (camel body location, evolution status, presence of surinfection, lesion progressive stage, extent, contagious nature and period of its appearance) as well as implemented therapeutic and preventive measures. The presence of external parasites such as ticks was also targeted. The presence of external parasites was considered an indicator of the application of prophylactic measures, but those parasites were not collected or diagnosed. The diseases' diagnostic was based on pathognomonic clinical signs and lesions and no further investigations have been conducted to confirm the clinical diagnosis. The negative effect of skin diseases on feeding intake and on milk production was also recorded during the survey, based on interviews with the camel owners and shepherds.

Completed forms were used to conceive a database on Excel. Data entry was followed by database clearing, in order to check the collected information by cross-referencing collected data and photos taken of affected animals. The goal was to get a reliable database and to minimize biases that may be related to errors of registration on the forms or to incorrect answers of the surveyed farmers.

### Statistical analysis

The data set was subjected to descriptive and analytical statistical analyses using Excel Software.

To study age and sex effect on the proportion of skin diseases detected in this survey, a Chi-
square test was used when conditions for
performing the test were satisfied.

Results

In the 168 monitored herds, 268 camels were affected with apparent skin lesions corresponding to 336 skin disease cases with variable etiologies: viral, parasitic or bacterial (Table 1). In fact, one animal could present one or more than one skin disease with the following distribution: 103 cases of ringworm, 175 cases of mange, 22 cases of camelpox or camel contagious ecthyma (C.C.E), and 35 cases of lymphadenitis.

Based on pathognomonic clinical signs and
lesions, sarcoptic mange was diagnosed in
almost half (54%) of the recorded cases and
concerned 66% of affected camels; Ringworm
was registered in 1/3 of cases with a rate of
30%. Lymphadenitis was detected in 11% of
cases and camelpox/C.C.E cases did not
exceed 7% (Table 2).

The mean age of studied cases was 6 ± 7 years (74 ± 84 months) with a range of 1–360 months (30 years). Regarding the age distribution, 50% of animals were over 3 years old, 13% between 1 and 3 years old, and 37% under 12 months with a notable difference related to the disease.

Seventy-two percent of mangy animals were over 3 years old, 11% were between one and 3 years old, and 17% were between 1 and 12 months old. For ringworm, the profile was completely different with a higher proportion in young animals: 73% of the cases were recorded in 1 to 12 months old animals, 22% in 1 to 3 years old, and only 5% in animals older than 3 years. Camelpox/C.C.E was diagnosed in 57% of cases in animals less than one year old. Animals between 1 and 3 years old were affected at a rate of 30%, while those over 3 years old were affected in only 13% of cases.

In the current study, confirmatory diagnosis
and differential laboratory diagnosis between

camelpox and C.C.E was not established. For
lymphadenitis, animals under 3 years old were
the most affected, with rates of 40% in young
ones (under 1 year old) and 43% in 1 to 3 years
old camels. Animals older than 3 years
affected by this disease presented only 17% of
the cases.

Skin diseases in this study were found to be
predominant in females (181 camels and 217
cases) with a rate of 69% versus 31% in males
(85 camels and 105 cases). Nevertheless, this
rate varied for each sex according to age. In
females, 47% of cases were detected in young
camels and 53% in adult animals. For males, it
was recorded that 71% of the cases were in
young animals and 29% among adults.

Camel skin diseases recorded during this study had a negative effect on feeding intake in about 73% of camels. Nevertheless, this negative effect on feeding intake varied according to the disease. It was about 80% for mange, 61% for ringworm, 91% for camelpox/ecthyma and 63% for lymphadenitis. This effect can be explained either by location of lesions which constitute a physical discomfort for apprehension, chewing or swallowing, or by the presence of pruritus which is a source of discomfort for animals. A negative effect on milk production was also recorded in females with a rate of 35%.

In the present survey, 62% of camels with skin
disease were infested by ticks, of which 92%
did not receive any antiparasitic treatment as a
preventive measure against external parasitic
attacks. In addition, dromedary camel herd
management in the south of Morocco was
characterized by an absence of preventive
measures implementation while introducing
new animals into the herd. Indeed, no animal
quarantine or antiparasitic applications were
observed for newly introduced animals. In the
case of affection by skin disease, it is not
common (never in excess of 15%) to resort to
veterinary doctor or livestock technician
<table><caption>**Table 1:** Distribution of camel skin diseases in Moroccan provinces</caption><thead><tr><th rowspan="2">Provinces</th><th colspan="5">Camels herds</th><th colspan="4">Repartition of skin diseases cases</th></tr><tr><th>Number of camels</th><th>Mean</th><th>S.D</th><th>Herds (n)</th><th>Affected camels (n)</th><th>Cases (n)</th><th>Ringworm</th><th>Mange</th><th>Camel pox</th><th>Lymphadenitis</th></tr></thead><tbody><tr><td>Guelmim</td><td>997</td><td>83</td><td>52</td><td>12</td><td>18</td><td>19</td><td>9</td><td>6</td><td>2</td><td>2</td></tr><tr><td>Tan Tan</td><td>794</td><td>42</td><td>35</td><td>19</td><td>38</td><td>49</td><td>10</td><td>28</td><td>4</td><td>7</td></tr><tr><td>Laayoune</td><td>1576</td><td>83</td><td>60</td><td>19</td><td>36</td><td>47</td><td>14</td><td>26</td><td>5</td><td>2</td></tr><tr><td>Boujdour</td><td>1658</td><td>83</td><td>41</td><td>20</td><td>32</td><td>40</td><td>13</td><td>21</td><td>1</td><td>5</td></tr><tr><td>Dakhla</td><td>4777</td><td>92</td><td>54</td><td>52</td><td>88</td><td>110</td><td>41</td><td>52</td><td>2</td><td>15</td></tr><tr><td>Smara</td><td>918</td><td>77</td><td>63</td><td>12</td><td>16</td><td>20</td><td>7</td><td>10</td><td>1</td><td>2</td></tr><tr><td>Tata</td><td>432</td><td>43</td><td>29</td><td>10</td><td>16</td><td>26</td><td>9</td><td>9</td><td>6</td><td>2</td></tr><tr><td>Ouarzazate</td><td>239</td><td>17</td><td>13</td><td>14</td><td>14</td><td>15</td><td>0</td><td>14</td><td>1</td><td>0</td></tr><tr><td>Essaouira</td><td>35</td><td>4</td><td>2</td><td>10</td><td>10</td><td>10</td><td>0</td><td>9</td><td>1</td><td>0</td></tr><tr><td>Total</td><td>11426</td><td>68</td><td>54</td><td>168</td><td>268</td><td>336</td><td>103</td><td>175</td><td>23</td><td>35</td></tr></tbody></table>
<table><caption>**Table 2:** Camel skin diseases distribution, effect of age and sex</caption><thead><tr><th rowspan="2">Disease</th><th colspan="2">Female</th><th colspan="2">Male</th><th rowspan="2">Total</th><th rowspan="2">Diseases distribution* (%)</th></tr><tr><th>Young</th><th>Adult</th><th>Young</th><th>Adult</th></tr></thead><tbody><tr><td>Mange</td><td>36</td><td>89</td><td>30</td><td>20</td><td>175</td><td>54<br>66</td></tr><tr><td>Ringworm</td><td>57</td><td>5</td><td>28</td><td>2</td><td>92</td><td>29<br>35</td></tr><tr><td>Lymphadenitis</td><td>11</td><td>9</td><td>8</td><td>4</td><td>32</td><td>10<br>12</td></tr><tr><td>Camelpox</td><td>10</td><td>0</td><td>12</td><td>1</td><td>23</td><td>7<br>9</td></tr><tr><td>Total</td><td>114</td><td>103</td><td>78</td><td>27</td><td>322</td><td></td></tr><tr><td>Cases (n)</td><td colspan="2">217</td><td colspan="2">105</td><td>322</td><td></td></tr><tr><td>Affected animals (n)</td><td colspan="2">181</td><td colspan="2">85</td><td>266**</td><td></td></tr></tbody></table>

competencies; isolation of affected animals from others apparently healthy, as a preventive measure, was observed in only 3% of cases.

Skin disease treatment application in dromedary camels was dependent on the detected diseases. Indeed, for mange and ringworm a medical injection (based on ivermectin (ND), a medicine distributed freely by Moroccan veterinary services to camel owners in this region), or traditional treatment (most of the time cade oil or drain oil) was established in 40% and 63% of cases respectively. Treatment was applied in 35% of camelpox/C.C.E cases and 17% of lymphadenitis cases.

### Macroscopic description of skin diseases

Mange was characterized by localized generalized form which presented 36% of detected cases. Lesions mainly affected the neck (51%), legs (35%), abdomen (34%) and/or head (15%). They were characterized by the presence of areas of diffuse alopecia with scabs associated or not with hyperkeratosis. Lesions were pruriginous with a low rate of surinfection (4% of mange cases)

(Photos 1).

Ringworm animals showed characteristic lesions with circumscribed areas of alopecia covered by crust. They were mostly located on the abdomen (61%), legs (24%), neck (18%) and/or head (4%). The generalized form was diagnosed in 33% of cases. Lesions of surinfection were rare and hardly exceeded 3% of cases (Photos 2).

For camelpox/C.C.E, lesions were localized in all studied cases and the generalized form was not diagnosed. The most affected areas were mainly the lips (100%), nostrils (57%) and chin (26%). Detected lesions were either vesicles, papules or ulcers with a surinfection rate of 13%. In animals with camelpox/C.C.E, a negative effect on feeding intake was detected in 91% of the cases (Photos 3).

Lymphadenitis was present with two forms, namely skin abscesses in about 54% of cases and ganglionic abscesses in about 43%. The number of animals presenting both forms was limited to a rate which did not exceed 3%. In addition, 63% of dromedary camels with lymphadenitis showed a decrease in feeding

<footnote>*: the 1st line represents the proportion related to the total of cases and the 2nd line represents the proportion of the same disease related to total of affected camels; **: Data related to the sex of two animals was not recorded.</footnote>
intake and lesions were surinfected in 66% of
cases (Photos 4).

Skin abscesses were detected mainly on the
head (53%), chest and abdomen (37%) and
legs (32%). Ganglionic abscesses mainly
affected anterior body parts with a predilection
for prescapular (47%) and cervical lymph
nodes (40%). Detected cases in the posterior
body part mainly concern popliteal (13%) and
mammary (13%) lymph nodes (Photos 4).

Effect of intrinsic factors on skin diseases
proportion (age and sex)

Sex had no significant effect on the
proportions of the four studied skin diseases
(mange, ringworm, camelpox/C.C.E and
lymphadenitis) at P=0.05 (χ² = 7.63 <7.81).

The study of sex effect on the parasitic
diseases proportion, mange and ringworm, also
showed that there was no effect of sex at
P=0.05 (χ² = 0.47 <3.84). Nevertheless, sex had
a highly significant effect on the mange
proportion (P<0.001; χ² = 14.80> 10.83).
Indeed, females were more affected than
males.

The effect of sex on the lymphadenitis
propotion was not significant at P=0.05 (χ² =
0.42 <3.84). The study of sex effect on the

relative proportion of the two detected forms
of lymphadenitis was also in favor of the
absence of a significant effect at P=0.05 (χ² =
0.14 <3.84).

The effect of sex on ringworm and
camelpox/C.C.E proportions was not studied
since the theoretical values of proportions,
specific to each of these two diseases, in the
contingency table were less than 3.

Age had a highly significant effect (P<0.001)
on the proportions of the four studied diseases
(χ²= 88.33 > 16.27).

The effect assessed on the proportion of each
separate disease showed that age had a highly
significant effect (p<0.001; χ² = 14.80> 10.83)
on mange and no significant effect at p = 0.05
(χ²=0.42 <3.84) on the lymphadenitis
proportion. A study of age effect on ringworm
and camelpox/C.C.E proportions was not
performed since the theoretical values of
proportions, specific to each of these two
diseases, in the contingency table were less
than 3.

The relative proportion of skin abscesses and
ganglionic abscesses was not affected by age
and the effect remained not significant at P=
0.05 (χ² = 0.42 <3.84).

<figure><img src="image_3.png" /><figcaption>**Photos 1:** Mange cases (from left to right: animal scratching, generalized form, neck, rump and head)</figcaption></figure>
<figure><img src="image_4.png" /><figcaption>**Photos 2:** Ringworm cases (from left to right: abdomen, neck, tail and head)</figcaption></figure>

<figure><img src="image_5.png" /><figcaption>**Photos 3:** Camelpox and camel contagious ecthyma (CCE) cases</figcaption></figure>

<figure><img src="image_6.png" /><figcaption>**Photos 4:** Lymphadenitis cases (from left to right: cheek, mandibular interspace and shoulder)</figcaption></figure>
Discussion

The present study was part of a project aiming
to study skin diseases' importance in
dromedary camels in Morocco. It was a
continuation of a study carried out in
slaughterhouses in three provinces in southern
Morocco (Guelmim, Tan Tan and Laayoune)
in order to draw up epidemiological and
histopathological patterns of skin diseases
diagnosed in dromedary camels intended for
slaughter.

Nevertheless, interpretation of the
epidemiological data and their extrapolation on
the dromedary camel population in Morocco
was limited by study conditions. Camels
presented for slaughter are about 67% males
and youngs (less than 3 years old) which is not
representative of the camel population in
Morocco. This is obviously explained by herd
management where females are kept for herd
renewal and by consumers' preference for
meat provided by young dromedary camels
(Driot et al., 2011).

The present survey was conducted to provide a
closer picture of skin diseases in the
dromedary camel herd in the Moroccan regions
which are characterized by high concentrations
d of dromedary camel populations.

Mange

Mange mean prevalence did not exceed 12% among all examined dromedary camels presented to the slaughterhouse (Driot et al., 2011). Nevertheless, the present work showed a proportion slightly higher than peak prevalence, up to 42%, which was found at Laâyoune slaughterhouse, during a study conducted in 1994 (Khallaayoune et al., 2000). Indeed, mange was diagnosed in almost half the cases and about 2/3 of the studied camel populations.

These data are concordant with Bornstein and
Younan (2013) who reported that skin diseases
due to different aetiologies (arthropods,

bacteria, fungi and virus) are often observed in
camels. Other than ringworm, camelpox and
contagious echthyma (O.R.F), the most common
prevalent condition was sarcoptic mange
caused by *Sarcoptes scabiei*, which is regarded
as one of the most common diseases of camels
worldwide (Chaudhary and Akbar, 2000).

In southern Tunisia, Jemli et al. (1995)
reported that mange was one of the most
common dromedary camel diseases. A similar
observation was reported in Morocco
(Bengoumi et al., 2005). All dromedary camel
farms were infected and about 10% of the
animals expressed the disease every year.
Camels can be affected by a variety of acarians
including *Sarcoptic scabiei*, *Psoroptes* spp.,
*Chorioptes* spp. and *Demodex* spp. (Sazmand
and Joachim, 2017).

Sarcoptic mange was regarded in a study
conducted in Iran as one of the most prevalent
diseases of camels and it can also be
transmitted to human (Sazmand and Joachim,
2017). In Ethiopia, camels were remarkably
exposed to mange caused by sarcoptic acarian
with an overall prevalence of 31.5% .
*Sarcoptes scabiei* was identified as the only
acarian species in all scrappings collected from
suspected lesions. This observation is in
general agreement with reports by various
authors. Even though both sarcoptic and
chorioptic mange acarians have been reported,
sarcoptic mange caused by *Sarcoptic scabiei* is
by far the most common contagious and
serious condition in camels (Feyera et al.,
2015).

In small camelids of South America, mange
was responsible for 95% of losses due to
ectoparasites, with a 40% prevalence rate in
alpaca and 25% in llama (Twomey et al.,
2009). Sarcoptic mange has been described in
4 species of camelids in South America and
has been reported in llama and alpaca in the
United Kingdom (D'alertio et al., 2005).

According to Legni (1991, cited by D'alertio et
al., 2005), as with other livestock species in terms of prevalence and economic loss, parasitic skin diseases caused by mange were the most important skin diseases affecting camelids in South America.

Mange is easily transmitted in dromedary camel herds due to their skin condition, which is dirty and covered by epidermal debris and secretions, conditions well suited to *Sarcoptes* (Curasson, 1947; Bornstein and Younan, 2013). The infection spreads rapidly within a herd and is responsible for loss in body condition and production. Transmission of mange parasites can be either direct or indirect. The direct is due to camel herds' promiscuity and several other occasions when camels are in contact with each other or when infected camels rub themselves against inanimate objects which surround them. Since these objects are most often rare outside pastures conditions, mangy camels often rub against their congeners. Direct transmission is also frequent from mother to young during suckling periods (Curasson, 1947; Al-Ani and Roberson, 2005; Bornstein and Younan, 2013). It was reported by Feyera et al. (2015) that large herd size and bad body conditions were significantly and positively associated with mange prevalence. Variation in genetics, environment, accessibility to veterinary services, herd size and other husbandry practices can justify reported prevalences of mange in camels. Probably camels living in large herds are more prone to come into contact with infected animals during suckling, herding and housing.

On the other hand, when the infection is initiated, the dromedary camel does not react with pruritus or reacts little and, when it does, the disease is already spread. It has been reported that camel skin is not sensitive enough to withstand attack by insects and reacts less than other animals to contusions and trauma (Curasson, 1947; Bornstein and Younan, 2013). This finding can explain the

diffusion and persistence of skin diseases in camel herds, since when first symptoms and lesions appeared, or when animals began to rub against each other or against objects, the infestation was already diffused.

Detected mange clinical signs in this survey are pathognomonic and identical to what has been reported and there was no need to make further investigations to confirm the diagnosis. Indeed, clinical signs are pruritus, hair loss and general condition alteration of the animal. Acute disease can lead to a subacute or chronic form. Mange lesions begin at the neck, inguinal region and thighs. During the acute phase, pruritus is intense which pushes animals to scratch and rub against solid objects, causing depilation and excoriation (Jemli et al., 1995; Schillinger, 1987; Bornstein and Younan, 2013).

Mange lesions were detected in both localized and generalized forms with signs of alopecia and crust with or without hyperkeratosis, depending on the evolution of the disease. Indeed, Bornstein and Younan (2013) reported that commonly recognized mange chronic signs are crusting, thickening (hyperkeratosis), discolouring and fissuring of the skin.

The different mange clinical pictures overall may be related to different stages of disease progression. Beginning mange lesions were only located in thin skin zones, where symptoms usually appear first (head, internal side of legs and axilla), without spread to the rest of the body. The fine crusts and the skin gritty texture may be due to the burst of vesicles where mite begin to burrow into the epidermis. The light-coloured skinned animals exhibited lesions over the same zones as previous animals. However, in this case, the skin was erythematous and there was oedema in body decline parts. These two lesions were typical of mange initial acute phase. In chronic form, lesions were mostly located on the neck, legs and buttock. These are zones frequently in
contact with other camels and easy to scratch. This explains widespread alopecia and skin thickening in reaction to constant itching (Driot et al., 2011; Bornstein and Younan, 2013).

Regarding the ages of affected dromedary camels, in this work 50% of animals with skin diseases were older than 3 years with a variability related to the disease. Indeed, animals older than 3 years were most predisposed to mange. Such results were in concordance with previous studies conducted in camels in other regions over the world. Indeed, mange prevalence is higher in older animals (Faye, 1997; Kumar et al., 1992; Driot et al., 2011).

Females in this study accounted for 69% of the studied camel population. The effect of sex is insignificant in ringworm and lymphadenitis. These data are concordant with Fadlelmula et al. (1994), who reported that mange is a disease observed in growing young animals only, with no difference between the two sexes. Nevertheless, the effect of sex was detected in many cases. Indeed, females seemed to be more affected than males. Probably, as the adult males used for reproduction are kept in separate pens, the propagation of the disease should be less efficient.

When mange is suspected, diagnosis can be confirmed by demonstration of *S. scabiei* mites in skin scrapings. However, sensitivity of this method is low. The development of an indirect ELISA, demonstrating specific antibodies to *S. scabiei*, for camels is a promising candidate and should be considered as a useful diagnostic and seroepidemiological tool in the future (Bornstein and Younan, 2013).

It is evident in this study that dromedary camel herd managers did not resort frequently to veterinarian or livestock technician competencies for disease diagnosis or treatment. Nevertheless, mange camels are

submitted to either traditional or medical treatment.

For many years, ivermectin was provided by the Ministry of Agriculture in Morocco free of charge to breeders in Moroccan southern provinces and disadvantaged regions, to control gastro-intestinal helminthosis, which was responsible for huge economic losses in camels as well as in other species. This medicine also had an effect on ectoparasites like *Sarcoptes*, which may explain the lower prevalence of mange nowadays than in the past (Driot et al., 2011). Frequent and systematic use of ivermectin limited mange spread and reoccurrence in camel herds; the control is based on systematic use of acaricide solutions or ivermectin injections (Jemli et al., 1995). During the study of Twomey et al. (2009), repeated subcutaneous administration of 0.2 mg/kg bodyweight controlled the outbreak successfully. However, the slow response, especially in females, was disappointing, and can be explained by physiological status and hormone changes.

Feyera et al. (2015) reported that drug treatment (ivermectin and diazinon) resulted in a considerable improvement in the clinical score. All treated camels showed a higher degree of recovery with reference to skin texture, healing of skin lesions and disappearance of crusts. The authors concluded that ivermectin had relatively more efficacy than diazinon, as measured by analyses of skin scrapings, body condition and clinical score changes.

## Ringworm

The ringworm proportion rose to 16% among all animals, which was slightly lower than what was found in a study carried out from June 2002 to April 2003 in South Morocco, where 26% of the camels were affected (El Jouhari et al., 2004).

Ringworm has an inverse predisposition
compared to mange, i.e., it was detected much
more in camels fewer than 3 years old with no
registered effect of sex. Indeed, it was
published that ringworm prevalence was
higher in young calves under one year old
(Faye, 1997; Kumar et al, 1992; Driot et al.,
2011) and under 3 years of age, and the disease
was not observed in animals over 4 years old
(McGrane and Higgins, 1985). Other authors
concluded that ringworm is a common disease
affecting young dromedary camels below three
years of age and *T. verrucosum* was the most
common dermatophyte affecting camels
(Almuzaini et al., 2016; Ganguly et al., 2017).

Classical lesions as described earlier (McGrane
and Higgins, 1985; Fadlelmula et al., 1994; Al-
Ani and Roberson, 2005), circular and known
as “ringworm”, were detected in this study
mainly in the abdomen, legs and neck with a
low rate of surinfection. Clinical examination
of affected animals showed squamous and
crustal circular lesions with areas of alopecia,
but sometimes extensive affected areas were
noted (Al-Ani and Roberson, 2005).

The diversity of ringworm clinical
presentations is associated with the various
stages of the disease evolution. This change
depends on the balance between the host and
the parasite, which depends on climate, more
or less favourable to fungal development, and
on applied treatments (El Jouhari et al, 2004).

Several studies showed that climatic factors
also intervene directly or indirectly. For
example, a mild and humid weather is
favourable to fungal growth, and hence to
ringworm development. The peak incidence of
ringworm was recorded in autumn and winter,
while the incidence was lower in summer.
Indeed, camel skin and damp hairs during
rainy seasons can promote the adhesion of
dermatophyte *arthroconidia* and therefore the
infection is established more frequently during
dry seasons. Rain can help the spread of
infected material from skin flaps found on the

ground (Curasson, 1947; McGrane and
Higgins, 1985; Scott, 1988; Fadlelmula et al.,
1994).

This study showed that ringworm lesions were commonly treated, using medical or traditional treatment without veterinary assistance. It was reported that ringworm lesions can expand in size, and signs of emaciation and fatigue appeared in most affected animals. The disease can even cause death of affected animals (Fadlelmula et al., 1994; Al-Ani and Roberson, 2005). In most cases, spontaneous recovery occurred, although some camels remained infected. Infected camels sould be separated and all instruments and harnesses must be disinfected. Antifungal drug therapy has been used to treat camels suffering from fungal infection. Immunization of susceptible camels, by killed or live attenuated fungal vaccines, was recommended (Al-Ani and Roberson, 2005).

Ringworm, although considered rare in camels,
is a major public and veterinary health
problem. However, the incidence of ringworm
is starting to increase in racing camels due to
intensive housing. Direct contact with other
infected animals and the use of contaminated
utensils are common ways in which ringworm
can spread. The introduction of new camels
with subclinical infection is usually the source
of infection to susceptible herds (Al-Ani and
Roberson, 2005; Al Tayib, 2019). It was
reported in a case study in Saudia Arabia
(Sabra and Al Harbi, 2014) that there is a high
level of zoophilic dermatophytosis, a sporadic
infection of farmers caused by *Dermatophytes
spp.* The frequency of zoophilic fungal
infections among farmers is higher compared
to non-farmers, and there is an occupational
relationship since the same fungus was isolated
from both the animal and worker (Sabra and Al
Harbi, 2014). A recent case of zoonotic
dermatophytosis in camels was also recorded
in India (Tuteja et al., 2019).
## *Camelpox and camel contagious ecthyma (C.C.E)*

Based on clinical signs, camelpox and C.C.E detected cases were very few. It seems that camels under 3 years old were more predisposed to be affected by these diseases. This remark is confirmed by the fact that Poxvirus spreads quickly among herd young that are 2 to 3 years old (McGrane and Higgins 1985) or 1 to 2 years old (Jemli et al., 1995).

Camelpox and C.C.E lesions are localized, mainly in the lips, nostrils and chin, which confirms previous study results conducted in the dromedary camel population in other countries. Indeed, camelpox is a disease well known by breeders and the need for confirmation by laboratory techniques is rarely manifested (McGrane and Higgins, 1985).

The disease is characterized by papulo-vesicular lesions sitting in the lips and chin skin, which often lead to difficulty in chewing and food apprehension and, as a consequence, diseased camels can lose body condition (McGrane and Higgins, 1985; Jemli et al., 1995; Wernery et al., 2014). A brownish crust develops on lesions that usually heal in 3 weeks. Likewise, an increase in the size of lymphatic nodules has been observed. Mammary glands, genitals, inguinal and perianal regions, thighs and sometimes feet are also affected (McGrane and Higgins, 1985). Clinical manifestations range from inapparent to moderate, less frequent infection to a severe systemic infection and death (Yousif et al., 2010). The disease caused death in a dozen cases in southern Tunisia (Jemli et al., 1995).

Camelpox is a contagious disease, widely distributed among camels in India, Pakistan, Afghanistan, Iran, the former USSR, the Middle East, North and East Africa and worldwide, except in the Australian continent (McGrane and Higgins, 1985; Yousif et al., 2010; Bornstein and Younan, 2013). The disease is enzootic in these countries, and

sporadic outbreaks occur with seasonal incidence increasing during the rainy season (Yousif et al., 2010).

Epidemics occur relatively regularly and mainly during rainy seasons; outbreaks during dry seasons appear to be mild and usually of the localized form. Severe secondary infections are common in camelpox, and may be localized to the skin or generalized as septicaemia, eventually leading to death. Morbidity is high and mortality is usually low, but it can reach 28% in generalized forms of the disease and 40–50% in calves (Bornstein and Younan, 2013). Herd outbreaks are often associated with withdrawal stress or poor nutritional status. The majority of cases is of average morbidity, and cured animals appear to have long immunity to reinfection. Occasionally, a severe form of the disease which can be fatal is also encountered (McGrane and Higgins, 1985; Bornstein and Younan, 2013).

In Morocco, the disease is known, but its etiology was confirmed only during an epizootic in southern Morocco in 1984. The epidemiological survey showed that the disease is serious in the area where the infection is recently detected, but cured animals are immunized for a long time (El Harrak, 1991). Similar findings were also reported by other researchers (McGrane and Higgins in 1985; Bornstein and Younan, 2013).

In an attempt to prevent the disease, vaccines have been developed and trialed. There is a vaccine commercialized in Morocco (Jemli et al., 1995) and one called Ducapox® has been used in the UAE since 1994 (Bornstein and Younan, 2013).

Camel contagious ecthyma (C.C.E) has been reported in former-USSR, Mongolia, Kenya, Somalia and Sudan (Azwai et al., 1995; Bornstein and Younan, 2013). Azwai et al. (1995) have reported that C.C.E outbreak
occurred in a shared watering area between
sheep, camels and goats, which provided an
important opportunity for virus transmission
from one species to another. Young animals
are particularly susceptible, suffering from
lesions that often appear around the mouth and
nostrils (Azwai et al., 1995; Ganido-Fariña et
al., 2008; Bornstein and Younan, 2013). The
incidence of endemic C.C.E is higher than that
of camelpox. Morbidity can reach 100%
(Bornstein and Younan, 2013).

It has been reported by Ganido-Fariña et al. (2008) that among animals with skin infections, there is no evidence of systemic infection. The virus of C.C.E has been found in crusts and it has been suggested that outbreaks are due to contact with the virus in the environment or to the persistence of the virus in subclinical herds, causing periodic and undetectable skin lesions. This theory, however, has not been rigorously explored (Ganido-Fariña et al., 2008).

Skin diseases are one factor that affect camel
performances by decreasing food intake in
about 73% of studied cases, with a negative
effect on milk production in about 35% of
cases. In animals with camelpox/C.C.E, a
negative effect on feeding was detected in 91%
of cases. It was reported that C.C.E lesions
can reduce camels' ability to feed, suckle or
graze; primary lesions can also be complicated
by bacterial effects, fungi and insect larvae
(Ganido-Fariña et al., 2008; Bornstein and
Younan, 2013).

Lymphadenitis

Lymphadenitis was present in the two common
forms of skin and ganglionic abscesses,
affecting mainly young camels under 3 years
old, that are more predisposed. Secondary
infections were frequent, but they were rarely
treated.

Lymphadenitis was reported in many
countries. Brown (2004) reported that skin

abscesses are common in feral camels in
central Australia and pus-filled abscesses are
commonly detected during ante-mortem and
post-mortem inspection at Australian abattoirs.
In Jordan, the disease usually affects camels 1-
3 years of age, and the incubation period may
extend up to 3 months (Tarazi and Al-Ani,
2016). In the former-USSR, the disease was
clinically characterized by purulent
inflammation of superficial lymph nodes,
particularly those of the neck, prescapular and
head regions (Buchnev et al., 1987). In Kenya,
abscesses involving the skin and subcutis were
frequently seen in camels and extended to the
lymph nodes. Head, prescapular and presternal
lymph nodes were frequently involved.
Puncture wounds, bites and secondary
infections following diseases such as camelpox
may lead to abscess formation (Juma Ngeiywa,
1992).

In Sudan, abscesses involving the skin and
adnexia are frequently seen in camels. The
lesions may incorporate the skin and
subcutaneous tissue, and commonly the lymph
nodes and other organs. The invasion of this
structure by pyogenic bacteria may be due to
wounds. On the other hand, camel grazing
pastures are thorny shrubs and thorny trees and
bites of animals or secondary infections
following diseases may be responsible for a
great deal of skin infection. The presence of
abscesses usually leads to emaciation and
increases the susceptibility of such animals to
secondary infections (Mohammed, 2010).

Wounds and abscesses were the third most
common disease problem affecting the
surveyed camels, with a peak incidence during
the rainy seasons. The abscesses are most
frequently located in the lymph nodes of the
mandibular region (mandibular, parotid, and
lateral retropharyngeal) followed by the
superficial cervical, subiliac, popliteal,
supermammary and scrotal lymph nodes
respectively (Mohammed, 2010).
Lymphadenitis lesions can had a negative effect on camels' feed intake depending on abscess localization. Mohammed (2010) reported that carcass lymph nodes were affected in the following order of decreasing frequency: prescapular, prefemoral, superficial inguinal and popliteal lymph nodes.

### Common factors

It appears from this study that skin diseases etiology can include several pathogens. The factors that can be implicated strongly in the persistence of these diseases in camel herds in the south of Morocco are mainly:

- presence of ectoparasites (mainly ticks) and absence of a systematic application of antiparasitic treatment as a preventive measure against external parasites;

- lack of biosecurity measures while introducing new camels to a herd (antiparasitic treatment as a preventive measure and animal quarantine).

- absence of treatment or isolation of affected camels.

- lack of water and inadequate preparation for bathing or spraying, leading to inefficient treatment.

Skin diseases have a negative effect on food intake which can affect negatively the dromedary camel production system (milk and meat production, decrease in performance). The gravity of these effects can be directly linked to localization of the lesion which can constitute a physical discomfort for apprehension, chewing or swallowing, or it could be a source of pruritus which affects animal comfort.

Host-parasite interactions depend on the animal body condition and its capacity to build an efficient immune response. Other factors such as age, feeding and infections are likely to influence host defence mechanisms (vermifugation and vaccination against

camelpox). Deficiencies, especially in zinc and copper, may also be considered.

### Conclusions

This study showed that parasitic diseases affecting the skin were highly frequent in camel herds in the south of Morocco. In contrast, bacterial and viral skin diseases were less prevalent. It appeared that age had a significant effect on skin diseases prevalence in camels.

The high proportion of mange and ringworm can be explained, among other factors, by herd management practices characterized by the absence of biosecurity measures and the lack of preventive precautions. Furthermore, the lack of acquired post-infestation immunity can explain the recurrence of these diseases every year in the animals and in the herds. Further studies should be conducted to better understand the functioning of the skin immune system in camels and its responses, especially to mite and dermatophyte infestation (mange and ringworm).

### Acknowledgements

The present study was conducted in the context of the P.R.A.D project no:16867 entitled "Skin diseases and mineral metabolism in camel". We thank the Moroccan central and local veterinary services for their support and assistance with the field activities, without which this work would not have been possible.

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