- Open Access
Histopathology, microbiology and the inflammatory process associated with Sarcoptes scabiei infection in the Iberian ibex, Capra pyrenaica
- José Espinosa†1Email author,
- Arián Ráez-Bravo†2,
- Jorge R. López-Olvera2,
- Jesús M. Pérez1,
- Santiago Lavín2,
- Asta Tvarijonaviciute3,
- Francisco J. Cano-Manuel4,
- Paulino Fandos5,
- Ramón C. Soriguer6,
- José Enrique Granados4,
- Diego Romero7 and
- Roser Velarde2
© The Author(s). 2017
Received: 11 August 2017
Accepted: 20 November 2017
Published: 4 December 2017
Sarcoptic mange has been identified as the most significant infectious disease affecting the Iberian ibex (Capra pyrenaica). Despite several studies on the effects of mange on ibex, the pathological and clinical picture derived from sarcoptic mange infestation is still poorly understood. To further knowledge of sarcoptic mange pathology, samples from ibex were evaluated from histological, microbiological and serological perspectives.
Samples of skin, non-dermal tissues and blood were collected from 54 ibex (25 experimentally infected, 15 naturally infected and 14 healthy). Skin biopsies were examined at different stages of the disease for quantitative cellular, structural and vascular changes. Sixteen different non-dermal tissues of each ibex were taken for histological study. Acetylcholinesterase and serum amyloid A protein levels were evaluated from blood samples from ibex with different lesional grade. Samples of mangy skin, suppurative lesions and internal organs were characterized microbiologically by culture. Bacterial colonies were identified by a desorption/ionization time-of-flight mass spectrometry system (MALDI TOF/TOF).
The histological study of the skin lesions revealed serious acanthosis, hyperkeratosis, rete ridges, spongiotic oedema, serocellular and eosinophilic crusts, exocytosis foci, apoptotic cells and sebaceous gland hyperplasia. The cellular response in the dermis was consistent with type I and type IV hypersensitivity responses. The most prominent histological findings in non-dermal tissues were lymphoid hyperplasia, leukocytosis, congestion and the presence of amyloid deposits. The increase in serum concentrations of acetylcholinesterase and amyloid A protein correlated positively with the establishment of the inflammatory response in mangy skin and the presence of systemic amyloidosis. A wide variety of bacterial agents were isolated and the simultaneous presence of these in mangy skin, lymph nodes and internal organs such as lungs, liver, spleen and kidney was compatible with a septicaemic pattern of infection.
The alteration of biomarkers of inflammation and its implication in the pathogenesis of the disease and development of lesions in non-dermal tissues and septicaemic processes are serious conditioners for the survival of the mangy ibex. This severe clinical picture could be an important factor when considering the decision to eliminate animals that exceed a certain disease threshold from a population.
Sarcoptic mange is a highly contagious infection of the skin caused by the burrowing mite Sarcoptes scabiei that affects both humans and animals worldwide . It is responsible for epizootic disease in several wild ungulate and carnivore species [2–4]. Severe outbreaks of sarcoptic mange have been reported in the Iberian ibex (Capra pyrenaica), some of which have led to high mortality rates [5, 6]. Although many studies have addressed sarcoptidosis in Iberian ibex in recent last years, the pathogenicity of the infection in this host is still not yet fully understood.
Clinical signs of sarcoptic mange generally include a combination of alopecia, scaling and crusting . However, the severity and distribution of these lesions, as well as the outcome of the disease, vary between host species and individuals of the same species [1, 8]. Mild infestations often have little effect on hosts, although chronic infestations can affect fat reserves and food-conversion efficiency [9, 10]. Anemia, damage to inner organs and secondary bacterial complications may also compromise the survival of the host [11–13].
Despite the availability of wide-ranging information on the pathology of sarcoptic mange in the Iberian ibex [14–17], there are still few studies that address the pathological changes that occur in the skin and organs in mangy ibex. The objectives of this study were thus (i) to provide detailed histological descriptions of mangy skin at different stages of the disease; (ii) to assess histological changes in non-dermal organs in ibex with severe sarcoptic mange; (iii) to analyze the activity of markers of the inflammatory process and their implication in the pathogenesis of the disease; and (iv) to characterize microbiologically mangy skin and lesions as a means of identifying possible signs of secondary sepsis. To achieve these goals, we surveyed ibex that were both naturally and experimentally infected with S. scabiei.
Experimental facilities and animals
Thirty nine Iberian ibex (C. p. hispanica) (22 males and 17 females; 1–11 years of age) were captured, 33 in the Sierra Nevada Natural Space (SNNS) (36°55′ to 37°10′N, 2°56′ to 3°38′W), and 6 in the Sierras de Cazorla, Segura y Las Villas Natural Park (SCSVNP) (37°53′ to 37°88′N, 2°53′ to 2°88′W). Initial IgG levels against S. scabiei were measured by an enzyme-linked immunosorbent assay (ELISA) developed for alpine chamois (Rupicapra rupicapra) in order to exclude ibex that had previously been in contact with the disease . Captured ibex were transferred to experimental facilities located in southern Spain (Las Mimbres, Sierra de Huétor Natural Park, 37°18′ to 37°30′N, 3°28′ to 3°47′W). They were kept in small groups (4–6 animals) in separate enclosures under observation during an eight-week acclimatization period. All ibex had ad libitum access to food and water [19, 20].
In addition, 15 naturally infested free-ranging ibex (nine males and six females; 4–9 years of age) were selectively harvested as part of a management program devoted to controlling both ibex density and the spread of sarcoptic mange in the SNNS.
All ibex were captured using a rifle and anaesthetic darts with a combination of ketamine (3 mg/kg) and xylazine (3 mg/kg) .
After an adaptation period, 25 of the 39 ibex (22 from SNNS and three from SCSVNP) were experimentally infested with S. scabiei, and the remaining 14 ibex being left to act as controls. A 2cm2 skin fragment from a naturally S. scabiei-parasitized wild ibex from the SNNS was attached with elastic bandages to the previously shaved inter-scapular region to induce contact between the mites and the host skin. In order to determine the density and therefore the number of mites infesting each ibex, the density of mites was calculated in skin pieces adjacent to those used for the infestation. In these adjacent skin samples, mites were counted with a stereomicroscope after overnight digestion in 5% KOH solutions at 40 °C  and a thermal gradient induced by a light shone from below Petri dishes with black bottoms and transparent central areas .The resulting estimated dose received by each ibex was 750 ± 440 mites.
The experimental period lasted for 150 days after infestation. Experimentally and naturally infected ibex were visually assigned to one of the following three categories defined according to the percentage of skin surface affected: healthy (mange-free ibex), mild (initial and development stages, with lesions on < 50% of the host skin surface), and severe (consolidation and chronic stages with lesions on more than 50% of the host skin surface) .
Blood and skin sample collection
Blood samples and skin biopsies were collected at 26, 46, 103 and 150 days post-infestation (dpi). Blood samples (20 ml) were taken from each ibex (both infested and control animals) by jugular venipuncture, and kept at 4 °C in a cooling box until reaching the laboratory. Adjacent skin biopsies were taken after shaving the inter-scapular region using an 8 mm diameter punch biopsy tool (KRUUSE® Biopsy Punch, Langeskov, Denmark). In the control group, skin samples were only collected at 103 dpi. To do so, each ibex was separated into a handling crush for subsequent physical restraint (blindfolding and limb immobilization) and a local anaesthetic was administered (ANESVET®, Ovejero Lab, León, Spain). After collecting the skin samples, each animal was treated with an antiseptic spray. Each biopsy was placed into 10% neutral buffered formalin for 48–72 h, and then transferred to 60% ethanol and stored at 4 °C until histological analysis.
Necropsy and sample collection
Nineteen of the 25 ibex experimentally infected were euthanized at 150 dpi due to their severe mange infections. Naturally infected animals (all with more than 50% of their skin surface affected) were euthanized at the time of capture. Before euthanasia, blood samples were collected from each ibex. Animals were anaesthetized by intramuscular injection with a mixture of xylazine (3 mg/kg) and ketamine (3 mg/kg), and euthanized with T-61® (embutramide 12 mg/kg, membezonium iodide 3 mg/kg, tetracaine 0.3 mg/kg).
Scabietic ibex were necropsied under strict hygienic conditions immediately after death. Gross pathologic examination was performed on all animals and organs following a standard protocol. The following samples were collected from each ibex for histological study: superficial lymph nodes (SLN) draining the mangy skin lesions (submandibular, parotid, pre-scapular, sub-scapular, inguinal, mammary and popliteal), intracavitary lymph nodes (ILN) (mediastinal, mesenteric, hepatic, renal), central nervous system, tongue, thyroid gland, skeletal muscle, heart (papillary muscle), lungs (apical, middle and caudal lobes), liver, kidney, adrenal gland, spleen, pancreas, small intestine (ileum), large intestine (colon), ovary and testicle. All samples were fixed in a similar way to the skin biopsies. For the microbiological studies, the following samples were taken and stored separately in sterile tubes: skin (especially lesions of exudative dermatitis and/or abscesses), suppurative lesions, lungs, liver, spleen and kidney.
Skin biopsies and the rest of the fixed non-dermal tissues were briefly washed with 10% phosphate buffered saline (PBS) solution and embedded in paraffin wax (EI LEICA TP1020 Automatic Tissue Processor®, Barcelona, Spain). Serial 5 μm sections from all specimens were mounted on glass slides (Super-Frost, Menzel-Gläser, Braunschweig, Germany), stained with haematoxylin and eosin (HE) and analyzed by light microscopy.
Median ± SD of histopathological changes assessed in sarcoptic mange skin lesions on the different days post--infection
103 s dpi
1.45 ± 0.82a
3.18 ± 1.25b
0.60 ± 1.57a
3.51 ± 6.18b
1.63 ± 1.68a
Basal cell hyperplasia/acanthosis2
15.54 ± 2.54a
12.77 ± 1.8b
9.95 ± 2.88c
13.80 ± 3.93b
12.22 ± 2.60b
17.08 ± 4.81a
13.10 ± 4.62b
7.40 ± 3.80c
14.40 ± 3.23b
15.01 ± 3.92b
14.45 ± 3.85a
15.36 ± 3.29a
4.50 ± 3.77c
10.50 ± 3.83b
7.18 ± 5.54b
2.90 ± 0.54a
3.18 ± 0.60a
0.41 ± 0.69b
3.20 ± 1.13a
0.72 ± 0.64b
2.81 ± 0.60a
3.27 ± 0.78a
0.61 ± 0.70b
3.30 ± 0.67a
0.90 ± 0.83b
12.82 ± 4.19a
13.81 ± 3.91a
3.50 ± 3.06c
9.10 ± 3.51b
6.10 ± 3.76b
12.27 ± 3.06a
14.54 ± 2.65a
2.90 ± 2.88c
9 ± 3.80b
6.08 ± 5.85b
27.27 ± 3.70a
24.54 ± 3.32a
19.4 ± 6.10b
25.11 ± 6.65a
21.10 ± 3.17b
45.97 ± 11.85a
44.67 ± 12.14a
29.31 ± 6.48b
34.46 ± 13.40b
31.81 ± 90b
8.49 ± 0.94a
11.40 ± 1.16a
2.02 ± 5.81b
4.23 ± 2.64b
5.14 ± 1.74b
6.72 ± 0.69a
8.32 ± 0.92a
1.14 ± 2.24b
3.42 ± 1.14b
2.53 ± 1.29b
3.52 ± 4.48a
4.17 ± 1.76a
0.71 ± 1.27c
2.41 ± 3.39b
2.77 ± 3.62b
0.53 ± 0.24a
0.64 ± 0.11a
0.37 ± 0.24a
0.42 ± 0.23a
0.43 ± 0.55a
Acetylcholinesterase (AChE) and serum amyloid a (SAA) assay
Within 24 h of collection, serum was obtained by centrifugation at 4750× g for 10 min and stored separately at -82 °C. Serum SAA concentrations (μg/ml) were quantified as the mean value of two measurements using a commercially available ELISA kit (Tridelta Phase™ range serum amyloid, A Tridelta Development Ltd., Bray, Ireland). AChE activity (μmol/ml*min) was measured using acetylthiocholine as a substrate . The method was adapted to an automatic analyzer .
In the laboratory, samples were processed in biological safety cabinets within 12 h after collection. Twenty grams of each tissue and/or pathological material was placed in a sterile airtight bag with 3 ml of sterile 10% PBS and homogenized for 5 min (Stomacher 80 Biomaster®, Lardero, Spain). An aliquot of 800 μl of the resulting homogenate was added to a sterile cryotube together with 200 μl of glycerol. The cryo tubes were stored at -20 °C until microbiological analysis.
Samples were cultured on TSA and Columbia agar plates supplemented with 5% sheep blood (bioMérieux, Madrid, Spain) and incubated aerobically at 37 °C for 24–48 h. Cells from representative bacterial pure and freshly-cultivated colonies were re-suspended in 300 μl of HPLC-grade water and mixed vigorously prior to the addition of 900 μl of HPLC-grade ethanol. Subsequently, an acetonitrile/formic acid extraction protocol was performed following the manufacturer’s instructions (Bruker Daltonik, Bremen, Germany). After protein extraction, 1 μl of each isolate extract was spotted onto a 384-spot polished steel target plate, left to dry at room temperature and then overlaid with 1 μl of α-cyano-4-hydroxy-cinnamic acid (HCCA) matrix. All isolates were analyzed in a Bruker Daltonik UltrafleXtreme MALDI TOF/TOF (desorption/ionization time-of-flight mass spectrometry) system, which obtained one spectrum per sample used to assess the suitability of this spectrometric approach for identification at species level. Each spectrum was acquired using FlexControl software (Version 3.4) in automatic mode in a random sampling pattern. The identification of all the clinical isolates in this study was performed by MALDI Biotyper Real Time Classification software. The reliability of the identification was evaluated from the log (score) values, calculated with the MALDI Biotyper software mentioned above.
The results of the histopathological changes and serum SAA and AChE concentrations were reported as median and standard deviations, calculated using routine descriptive statistical procedures. The Kolmogorov-Smirnov test was used to assess data normality. Non-parametric statistical methods were used to compare groups. A Mann-Whitney U-test was employed to compare the control group with the clinical stage of the exposed groups. To evaluate the response of the different parameters in term of the time of exposure and mange status of the different infested groups, Friedman tests with repeated measures were performed. In a second step, a Wilcoxon signed rank post-hoc comparison test with Bonferroni correction was used to determine the differences between the groups analyzed. A Spearman’s rank correlation coefficient test was applied to establish the coefficients between the different variables analyzed. To compare the frequency of lesions observed in non-dermal tissues between experimentally exposed and naturally infected animals, the Fisher’s exact test was used. P-values < 0.05 were considered to be statistically significant.
All statistical analyses were performed with the R software version 3. 3. 1 (R Development Core Team, December 2016) .
Histopathological and microbiological findings
In the dermis, the number of sebaceous glands also varied according to dpi (Friedman F r test: χ 2 = 90.14, df = 2, P = 0.036), remaining unchanged until 150 dpi, at which point their number fell significantly (post-hoc test: P = 0.044). The number of lymphocytes (r (343) = 0.586, r (346) = 0.584, r (286) = 0.640), eosinophils (r (431) = 0.284, r (398) = 0.324, r (452) = 0.205), mast cells (r (277) = 0.763, r (281) = 0.699, r (149) = 0.811) and neutrophils (r (293) = 0.699, r (354) = 0.566, r (366) = 0.515) was significantly correlated (P < 0.0001) with the presence of spongiotic oedema, exocytosis foci and apoptotic cells respectively. With the exception of plasma cells (Friedman F r test: χ 2 = 10.96, df = 2, P = 0.067), the number of lymphocytes, mast cells, eosinophils and neutrophils was significantly (P = 0.0023, P = 0.012, P = 0.0087, P = 0.0023, respectively) higher during the first 46 dpi, but then decreased significantly (P < 0.001). The number of plasma cells was low in all the stages analyzed. In animals with self-limiting lesions, the number of inflammatory cells decreased significantly (post-hoc test: P < 0.0001) in relation to the first 46 dpi. However, except for neutrophils (post-hoc test: P = 0.019), these values showed no significant differences (post-hoc test: P = 0.394) with the ibex that reached the most severe stages of the disease.
Other changes observed (not shown in Table 1) include: mixed hyperkeratosis (ortho-and parakeratotic) with a predominance of the orthokeratotic form 46 dpi, bacterial colonies on the surface, mite feces, dermal fibrosis from the basal lamina to secretory duct of the sebaceous glands, multifocal deposits of melanin at the level of the basal lamina, pilose follicles in the catagen phase, and the dilation of the apocrine glands. Folliculitis was only detected in one ibex.
Description of necropsy findings in the non-dermal tissue of the Iberian ibex affected by severe sarcoptic mange
Gross pathologic examination
Lymphadenomegaly (two and three times the normal size).
Lymphoid hyperplasia with activation of LF, formation of germinal centers and increase in lympho-plasma cells and macrophages in cords and medullary sinuses (Serous lymphadenitis) (+++)
Purulent lesion (7.76%) (Fig. 3)
Purulent lymphadenitis (7.76%) (+++)
Congestion and edema (+++)
Subcapsular, follicular and medullary amyloidosis (71.35%) (++)
Lymphadenomegaly (less than twice the normal size)
Histological pattern similar to superficial LN (++)
Subcapsular, follicular and medullary amyloidosis (75.23%) (++)
Sarcocystis spp. (mesenteric LN) (12.38%) (+)
Gliosis and perivascular cuffs of mononuclear cell (25.00%) (+)
Sarcocystis spp. with cellular infiltration (lymphocytes, mast cells and eosinophils) (58.82%) (+)
Sarcocystis spp. with monocuclear infiltration (32.35%) (+)
Mononuclear myositis in the absence of parasites (14.74%) (+)
Sarcocystis spp. (44.11%) (+)
Absence of pericardial fat
Mononuclear myocarditis (monocytes, lymphocytes and plasma cells) with infiltration of adipose cells (23.52%) (+)
Chicken fat clot (35.29%)
Muscle mineralization (5.88%) (+)
Interstitial emphysema in apical lobes (41.17%)
Granulomatous inflammation with presence of intra- alveolar parasites and infiltration of eosinophils, neutrophils and lymphocytes (verminous pneumonia) (88.23%) (+++)
Fibrotic nodular lesions in caudal lobes (88.23%)
Infiltration of neutrophils, eosinophils, macrophages and lymphocytes, congestion, edema and areas of necrosis (bacterial pneumonia) (8.82%) (+++)
Infiltration of neutrophils, eosinophils, macrophages and lymphocytes, congestion, edema and areas of necrosis (bacterial pneumonia) (8.82%) (+++)
Ascitic fluid (transudate)
Perivascular amyloid deposits in portal triad and hepatic sinusoids (11.76%) (++)
Congestion (+++) and leukocytosis (67.64%) (++)
Parasitic fibrosis (8.82%) (+)
Absence of perirenal fat
Amyloid deposits in glomerular mesangium (amyloid nephrosis) and cortical and medullary tubular interstitium with decreased capillary lumen (chronic interstitial nephritis and ischemic tubular atrophy) (20.58%) (++)
Mesangial thickening, tubular mineralization and leukocytosis (50.00%) (+)
Amyloid deposits in cortex and adrenal medulla (26.47%) (++)
Leukocytosis (5.88%) (+) and adrenal cortical hypoplasia (17.64%) (+++)
Hyperplasia of LF with formation of germinal centers (+++)
Amyloid deposits in LF and PLS of the white pulp and the splenic cords and venous sinuses of the red pulp “sago spleen” (70.58%) (+++)
Congestion (+++) and leukocytosis (+)
Amyloid deposits in exocrine pancreas (15.38%) (+) and leukocytosis (+)
Chronic parasitic enteritis (21.21%) (++)
Amyloid deposits in MALT (25.75%) (+)
Biomarkers of inflammation
Median ± SD (range) of serum SAA and AChE concentrations in Iberian ibex according their sarcoptic mange status
4.45 ± 6.47a (1.50–26.80)
4.72 ± 11.52a (1.50–51.40)
11.61 ± 13.47b (1.51–80.40)
0.29 ± 0.12a (0.21–0.80)
0.42 ± 0.19b (0.20–0.12)
0.33 ± 0.17c (0.10–0.90)
Median ± SD (range) of serum SAA concentrations in relation to the percentage of amyloidosis detected in the total number of organs analyzed per ibex (n = 25)
5.05 ± 4.67a (1.50–9.50)
9.50 ± 4.61b (1.51–10.80)
14.35 ± 7.44c (9.30–31.30)
21.65 ± 9.97d (11.40–51.40)
Microbiological agents isolated by the MALDI-TOF MS method in Iberian ibex (n = 34) affected by severe sarcoptic mange
Mangy skin (n = 34)
Superficial suppurative lesions (n = 16)a
Other tissues (n = 43)
Lungs (n = 12)
Corynebacterium glutamicum c
Corynebacterium glutamicum c
Staphylococcus nepalensis b
Liver (n = 11)
Spleen (n = 10)
Staphylococcus nepalensis b
Kidney (n = 10)
The present study reveals structural changes in the skin and several internal organs in Iberian ibex affected by sarcoptic mange, and shows a relationship between pathological findings and the systemic inflammatory response. Additionally, mangy skin and lesions associated with S. scabiei infection were characterized microbiologically.
The macroscopic and histological skin lesions observed in mangy ibex closely match the classical descriptions of sarcoptic mange in wild and domestic animals [1, 3]. The cellular response was dominated largely by mononuclear cells, eosinophils and mast cells (intact and degranulated) up to 46 dpi. Subsequently, the number of cells fell significantly from 103 dpi onward. Our observations agree with those in red foxes (Vulpes vulpes) , raccoon dogs (Nyctereutes procyonoides) , wombats (Vombatus ursinus)  and Eurasian lynx (Lynx lynx) . However, the infiltration of eosinophils and mast cells was not as intense as in the above mentioned species and was similar to the findings previously described in wild boars , which may explain the presence of less obvious marked hyperkeratosis. According to our results, ibex showed signs that are compatible with a combined type I (immediate) and type IV (delayed) hypersensitivity reaction to infection . We thus propose that up to 46 dpi, the histological pattern corresponded to type I hypersensitivity since cytotoxicity signs were observed (Fig. 2b) and correlated positively with the number of cells. Subsequently, these signs decreased along withthe cellular infiltrate which suggests type IV hypersensitivity (Fig. 2c).This conclusion needs to be demonstrated by future studies by the immune-histochemical isotype of the lymphocytes or by the expressed cytokine pattern. The neutrophilic response could be due not only to the presence of the mites, but also to secondary bacterial infections or excoriations. As in all other species, the number of plasma cells was low, which may be linked to a reduced role of the humoral response in the infection. We can therefore say that the overexpression of eosinophils, mast cells and neutrophils was associated with a detrimental and non-protective response that was unable to control the infection. This was shown by the observations of ibex with self-limiting clinic process. The presence of abundant serocellular crusts is apparently a mechanism that destroys mites or inhibits their burrowing into the skin as these crusts contain specific antibodies and other toxic components that can intoxicate mites . The hypertrophy and dilation of sebaceous and apocrine glands could be due to the obstruction of the excretory duct of glands by the hyperkeratotic crusts. Finally, the orto- and parakeratotic scales in the stratum corneum correspond to the previous passage of mites through the incompletely differentiated layers of the epidermis.
Cholinesterases have been reported as having the capacity to increase local and systemic inflammatory events in various pathological states . In our study we observed an increase in AChE levels in the localized form of the disease in experimentally-infested ibex (Table 3), which coincides and correlates significantly with the increase in inflammatory activity observed in the mangy skin during the first 46 dpi. Our results are similar to those described in canine demodicosis  and reinforce the idea that S. scabiei infection alters the cholinergic system and thereby contributing to the establishment of the local inflammatory response and the pathogenesis of the disease.
A wide variety of bacterial agents were isolated in mangy ibex (Table 5). The simultaneous presence of these pathogens in mangy skin, and also suppurative lesions in lymph nodes and in various organs is compatible with a septicaemic pattern of infection [12, 39]. The bacteria identified were similar to those previously described in psoroptic mange and other skin diseases in livestock [40, 41]. Staphylococcus was the dominant genus and infrequent species such as S. nepalensis were isolated. Infections by these bacteria are often secondary to a primary skin disease that provides the conditions for these commensal bacteria to proliferate [40, 42, 43]. Under these conditions, some bacterial strains can produce diverse dermotoxins that can aggravate the skin injuries produced by mites [44, 45]. Further toxicity studies are necessary if we are to specify the type of toxins expressed in mangy ibex. It has also been demonstrated that the colonization of skin lesions due to Psoroptes ovis with S. aureus causes a specific response of IgG antibodies against S. aureus antigens, suggesting that these bacteria may play some role in the immune-pathogenesis of mange . The mites themselves could contribute to the spread of these pathogenic bacteria since various strains of Staphylococcus have been isolated in mite burrows and in their faecal pellets . However, it has been reported that both mites and the skin bacteria produce molecules that inhibit the pathways of the complement system and stimulate the production of various cytokines and, thereby, promoting bacterial survival and growth as well as the chemotaxis of inflammatory cells [13, 48].
In humans, especially in children, scabies-associated skin bacterial infection is a common risk factor for systemic complications such as acute post-streptococcal glomerulonephritis and sometimes rheumatic heart disease [49, 50]. However, in mangy ibex, no necrotic foci, abscesses or signs of inflammation associated with bacteremia were found in the kidneys, livers, spleens or lungs. This thereby indicates that the lympho-hematogenus dissemination of these pathogens a priori has fewer serious consequences than in other species [11, 12, 29, 39]. The areas of myocarditis and gliosis detected have also been described in other species with sarcoptic mange [29, 39], although in our case we cannot assume that this was due to the septicaemic state. From a veterinary perspective, the administration of antibiotic substances should be considered, in addition to antiparasitic treatment, in the individual treatment of sarcoptic mange in the Iberian ibex.
In this study we provide a complete description of sarcoptic mange in the Iberian ibex through a description of its effects in naturally and experimentally infested animals, combining a serological, microbiological and histological approach. The alteration of biomarkers of inflammation and its implication in the pathogenesis of the disease and development of lesions in non-dermal tissues and septicaemic processes are serious conditioners for the survival of mangy ibex. These findings could be relevant in the management of affected ibex populations, since this could contribute to decisions on the elimination of animals that exceed a certain disease threshold from a population. In turn, our work provides a solid basis for further investigation of other factors that influence the pathogenesis of this disease.
We would like to thank the Consejería de Medio Ambiente de la Junta de Andalucía and in particular the Sierra Nevada Natural Space (SNNS) for their logistical support and to the Sierra de Huétor Natural Park for the transfer of their experimental facilities. Special thanks are also due to the park wardens and fieldworkers in the SNNS, and above all to Apolo Sánchez, José López, Isidro Puga, Elías Martínez, Francisco Felipe and Antonio Rodríguez for their professional and personal involvement in the study. We are also grateful Manolo Herrera for the maintenance of the ibex and the facilities during the experimental phase and the contributions of the SCSVNP to the study. Thank you to Michael Lockwood for the English revision, to the Health Surveillance VISAVET Centre of the Complutense University of Madrid and Department of Microbiology at the University of Jaén for the microbiological diagnosis, the Interdisciplinary Laboratory of Clinical Analysis (Interlab-UMU) of the University of Murcia for the serum assays, and the Service of Veterinary Pathology of the UAB for the histological preparation of samples.
This study was funded by MINECO from the Spanish Government (grant numbers CGL2012–40043-C0–01, CGL2012–40043-CO2–02 and CGL2016–80543-P). The authors’ research activities are partially funded by the PAIDI Research Group RNM-118 from Junta de Andalucia. José Espinosa was supported by a PhD Grant (grant number ECC/1402/2013: BES-2013-063931). This study is part of the project "Bases biológicas para la gestión de la sarna sarcóptica en la cabra montés (Capra pyrenaica) de Sierra Nevada".
Availability of data and materials
Data supporting the conclusions of this article are included within the article.
Designed the study: JE, RV, JMP and JLO. Performed the ibex sampling: JEG, JLO, FJCM, PF, JE, AR and RCS. Laboratory analyses: AT, DR, RV, SL and JE. Analyzed the data: JE, JMP, RV and RCS. Wrote the paper: JE. All authors read and approved the final manuscript.
This study complied with all Andalusian, Spanish and European legal requirements and guidelines regarding experimentation and animal welfare. Handling procedures and sampling frequency were designed to reduce stress and minimize the impact on the health of the subjects, as per European (2010/63/UE) and Spanish (R.D 53/2013) standards. The study was approved by the Ethics on Animal Welfare Committee of the University of Jaén and authorized by the Dirección General de Producción Agrícola y Ganadera of the Consejería de Agricultura, Pesca y Medio Ambiente of the Junta de Andalucía (Ref: SA/SIS/MD/ps/ October 25, 2012). The Sierra Nevada Natural Park staff also approved this study.
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