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Camel filariasis (Dipetalonema evansi) and its association with clinical balanoposthitis with reference to prominent changes in clinical findings, serum testosterone, semen analysis, and testicular histopathology

BMC Veterinary Research volume 20, Article number: 1 (2024) Cite this article

Abstract

Background

Camel filariasis induced variable clinical syndromes characterized by fever, lethargy, localized dermal lesions, loss of condition, and testicular and scrotal swelling. The objective of the present work focused on clarifying the diagnostic importance of clinical findings, serum testosterone, and semen analysis as well as blood smear and testicular histopathology as a differential tool between only balanoposthitis without filariasis male camels group (OnlyBpgr) and balanoposthitis-filariasis infected male camels group (BpFlgr). The study also monitored the associations between the severity of ticks’ infestations in investigated male camels and the occurrence of balanoposthitis only or balanoposthitis with filariasis.

Results and conclusions

The study reported significant correlation between serum testosterone, serum cortisol, and sperm vitality and abnormalities percentages. The study included male camels (n = 250) classified into three groups: healthy control group (Contgr; n = 30), OnlyBpgr (n = 210), and BpFlgr (n = 10). These male camels were clinically and laboratory examined, and skin scraping tests and testicular histopathology were conducted. The study confirmed the association of the changes in clinical findings, whole blood picture, serum testosterone, serum cortisol, and semen analysis, with OnlyBpgr and BpFlgr. These changes were more prominent in BpFlgr than in OnlyBpgr. Skin scraping test results revealed a higher severity of live ticks’ infestation in BpFlgr than in OnlyBpgr because, unlike OnlyBpgr, all camels in BpFlgr (n = 10) were suffering from live ticks’ infestation. It also concluded the higher efficacy of histopathology of testicular tissues in male camels as a diagnostic tool for adult filaria in balanoposthitis-affected male camels than blood smear because all cases of camel filariasis in the current work were negative for microfilaria on microscopic examination of diurnal blood smear as well as testicular histopathology revealed detection of adult filaria in all camel filariasis associated with balanoposthitis. Strong correlation relationships were demonstrated between serum testosterone, serum cortisol, and semen analysis results. Positive correlations were reported between serum testosterone levels and sperm vitality percentages. However, negative correlations were stated between serum testosterone and each of serum cortisol and sperm abnormalities either in Contgr, OnlyBpgr, or BpFlgr.

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Background

In a variety of dry, semi-arid, and tropical regions in Asia, Africa, and Australia, dromedary one-humped camels (Camelus dromedarius) were well suited for severe environments [1,2,3]. These dromedary camels were valuable because they served a variety of functions, including providing food, milk, a means of transportation, and work [4].

Egypt did not give camels sufficient attention when it came to parasite infections, especially those caused by helminthes. However, according to Baraka et al. [5], helminthes were the main reason for reduced milk and meat production, declining male fertility, and declining female calving rates. Because camels were living in a difficult habitat, there had not been many studies on them. The herds’ non-sedentary lifestyle and continual movement in search of grass and water sources were to blame for this.

Products that are produced by camels, such milk, meat, and wool, might be impacted by a number of circumstances. Parasitic illnesses that had a negative impact on camels’ health were one of the main causes of the decrease in milk and meat production [6]. In camels, the heart, hepatic, pulmonary, and spermatic arteries, as well as the mesenteric lymph nodes and lymph vessels, were all affected by the filarial worm Dipetalonema evansi (D. evansi) [7, 8]. Different Aedes mosquito species could act as this parasite’s vectors. Mosquitoes consumed microfilariae while feeding on infected dromedary blood. The parasites then migrated to the mosquitoes’ chest muscles, where they continued to grow. After 10 days, presented larvae in mosquito’s proboscis had the ability to cause infection in a new host [9].

According to Hashem and Badawy [10], one of the most significant nematode-borne parasitic diseases that affected humans, animals, and birds was filariasis. The health, productivity, and working activity of camels were negatively impacted by hemoparasitic disorders such dipetalonemiasis [11].

One of the most significant diseases influencing camels in Upper Egypt was camel filariasis, which was caused by D. evansi and exhibited clinical symptoms that had an impact on camel reproductive function, working ability, and productivity [12]. Moreover, filaria infection in camels might be acute or chronic producing different clinical changes like loss of body weight, skin lesions, severe weakness, high body temperature and swelling of both scrotum and testis [12, 13].

Seasonal variations had a significant effect on the prevalence rate of D. evansi infection, with the summer months recording the greatest incidence and the winter months the lowest [14]. According to Borji et al. [15], the group of camels aged (4–5 years old) had the highest infection rate with D. evansi.

Reproductive efficacy was one of the key features associated with the raising of food animals. Traditional camel reproductive management involved having the owner’s camels handle mating throughout the rutting season. Due to their short mating season, difficult sperm collection, and later sexual maturation than other farm animals, dromedary camels really had poor reproductive performance [16].

Accordingly, the present work focused on clarifying the diagnostic importance of clinical findings, serum testosterone and semen analysis as well as blood smear and testicular histopathology as a differential tool between only balanoposthitis without filariasis male camels group (OnlyBpgr) and balanoposthitis-filariasis infected male camels group (BpFlgr). The study also monitored the associations between the severity of ticks’ infestations in investigated male camels and the occurrence of balanoposthitis only or balanoposthitis with filariasis. The study reported significant correlation between serum testosterone, serum cortisol, and sperm vitality and abnormalities percentages.

Materials

Animals

Two hundred and 50 mature male camels (n = 250) were involved through the current study They belonged to private farms in the Assiut and Aswan governorates, Egypt. The investigated male camels were taken kindly from the farm by permission that was taken from the farm owner. Their ages ranged between 6 and 10 years. Their body weight ranged from 650 to 740 kg. The study was carried out during the breeding season (December to March) during daytime. Camels were housed in an open yard. Animals were group-fed on a diet composed mainly of commercial concentrates mixture (12% crude protein and 70% Total Digestible Nutrients; TDN) (4 kg\head\day) in addition to roughage material of about 10 kg\head\day, which was Egyptian clover during the winter season (10 kg\head\day). Drinking water was offered all day. Based mainly on their histopathological findings as well as clinical findings and laboratory assays, the examined camels were classified into three main groups. Some of these camels were kept as a healthy control group (Contgr; n = 30). The other camels were suffering from clinical signs of balanoposthitis (n = 220). Out of these balanoposthitis-infected camels (n = 220), 10 mature camels (4.55%) were diagnosed as positive for filariasis based mainly on their histopathological findings, and they were referred to as balanoposthitis-filariasis infected camels group (BpFlgr; n = 10). The other balanoposthitis-infected camels (n = 210) was referred to as only balanoposthitis without filariasis group (OnlyBpgr; n = 210). All camels were examined clinically, haematologically, and biochemically, and semen analysis was conducted. Regarding euthanasia methods, the male camels were slaughtered in a local abattoir at Aswan, Egypt. Histopathology of testicular tissues was carried out for 10 of the control group and for all balanoposthitis-affected camels (n = 220).

Samples

Samples were obtained during the breeding season (December to March). The jugular vein was used to collect whole blood and serum samples, and all necessary steps were done during sample preparation and collection to ensure a precise evaluation of hematological and biochemical parameters. Serum samples were obtained and stored at − 20 °C for further hormonal analysis using test kits obtained from commercial sources [17].

Epididymal sperms were collected according to Shahin et al. [18] to assess sperm vitality and abnormalities.

Each selected animal was also examined for ectoparasites, mainly live ticks, by taking a skin scraping before and after treatment application [19].

Clinical examination

The clinical examinations included mainly parameters of heart and respiratory rates, and rectal temperatures as well as rumen movements was done as described by Fowler [20]. According to Hutjens [21]; Hulsen [22]; Burfeind et al. [23]; Götze et al. [24], Khalphallah et al. [25, 26], and Elmeligy et al. [27], clinical scoring system and manure scoring of examined male camels were conducted. This monitoring included estimation of appetite score, rumen filling score (RFS), manure digestion score (MDS) and manure condition score (MCS). Feces were assessed for color, consistency, amount, fiber particle length, and shape.

Complete blood picture indices

Complete blood pictures, including red blood corpuscles (RBCs), total leucocytic count (TLC), differential leukocytic count (DLC), hemoglobin (Hb), and packed cell volume (PCV) were manually estimated according to Coles [17]; Harvey [28]; and Latimer et al. [29].

Microscopical examination of blood smears

According to Abdel-Rady [12]; Coles [17]; Weiss and Wardrop [30]; Zajac and Conboy [31], blood films of the wet, thin, and thick types, as well as concentration technique (Knott’s technique), were created for the diagnosis of microfilaria larvae (D. evansi).

Wet blood film

Two tiny droplets of blood were placed 1 centimeter apart on a clean, dry slide, covered with a cover slide, and examined at low power (× 10) to check for the mobility of microfilariae according to Abdel-Rady [12] and Coles [17].

Thin blood film

Two thin blood films were made, dried, fixed with absolute methanol for 5 minutes, dried again, and then stained for 30 minutes with Geimsa stain 10%. Excess stain was cleaned off, and a low-power lens examination was followed by a 100x oil immersion lens examination, according to Coles [17].

Thick blood film

Two drops of blood were placed on a clean, dry slide, speeded into a circle with a one-cm diameter, and then allowed to dry at room temperature. Dehemoglubinization was done by repeatedly submerging the slide in a container of distilled water, followed by 3–5 minutes of 100% methyl alcohol fixation and drying. 30 minutes of Geimsa dye 10% staining, and low power (10 x) and oil immersion lens (100 x) examination [12].

Concentration technique (Knott’s technique)

10 ml of 2% formalin and 1 ml of blood with EDTA were completely combined in a centrifuge tube. One drop of 0.1% methylene blue was added to the mixture and mixed before being transferred to a slide for microscopic examination. Thin and thick films were then prepared from the first sediment, fixed with absolute methyl alcohol, stained with Geimsa stain, and examined under a microscope. The mixture was centrifuged at 1000 rpm for 2 minutes [32].

Serum testosterone and cortisol hormone analysis

Through the use of commercial kits from Biodiagnostic, Cairo, Egypt, serum samples were examined using an enzyme-linked immunosorbent assay (ELISA-Sandwich Protocol) to determine the concentration of the hormone testosterone. Commercial radioimmunoassay kits from RandD Systems (MN 55413, Inc. at 614 McKinley Place NE in Minneapolis, Toll Free in the USA and Canada) were used to assess the levels of serum cortisol.

Sperm vitality and abnormalities

To assess sperm vitality, Moskovtsev and Librach [33] transferred a smear from the diluted semen samples to a glass slide and stained it with 5% eosin and 10% nigrosin stains. Two hundred spermatozoa from each sample were inspected under a light microscope, and the spermatozoa that were stained red were identified as being dead and counted. According to Menon et al. [34], the sperm morphological abnormalities included spermatozoa with aberrant or abnormal heads and tails.

Skin scraping test

Each male camel in Contgr, OnlyBpgr, or BpFlgr had a skin scraping taken in order to check for ectoparasites, primarily ticks. Each animal had a skin scraping taken in order to check for tick infestation. Then, samples prepared in 10% KOH solution were microscopically examined for adult ticks and identified according to Soulsby [35], Urquhart et al. [36], and Urquhart et al. [37]. In each case, the average number of ticks per microscopic field was estimated. The ticks’ infection was later determined by counting the live ticks on each cow and categorizing them as follows: + reflecting 1 to 10 live ticks, ++ reflecting 10 to 100 live ticks, and +++ reflecting more than 100 live ticks [13, 38,39,40].

Gross and histopathological examination

Male camels were slaughtered in a nearby abattoir in Aswan, Egypt. Testicular tissues were histopathologically examined for the 220 camels infected with balanoposthitis and the 10 members of the control group. In neighboring abattoir in Aswan, Egypt, the animals were slaughtered. There was a thorough inspection of the testicles. The testes were removed, cut into 1- to 2-cm-square pieces, and preserved in 10% neutral buffered formalin for later analysis. The samples were cleaned, dried in ethyl alcohol in increasing concentrations, cleaned in methyl benzoate, and then embedded in paraffin wax. Hematoxylin and eosin was used to stain a number of 3–5 μm thick paraffin sections, which were subsequently inspected [41].

Statistical analysis

SPSS statistical software program for Windows, version 10.0.1 (SPSS Inc., Chicago, IL., USA) was used for data analysis. The obtained data were described as mean ± SD. The data obtained from the clinical findings and laboratory analyses were analyzed using by general linear model repeated measures ANOVA and the significance level of results was set at p < 0.05. The significance of differences was evaluated between the means at Contgr, OnlyBpgr and BpFlgr. The correlation coefficient was calculated using Pearson Correlation at p < 0.05 or p < 0.01 between serum testosterone, serum cortisol, and percentages of sperm abnormalities and vitalities in examined male camels.

Results

Clinical findings

The control male camels showed normal clinical findings, as temperature, pulse and respiratory rates, rumen movements, appetite score, RFS, MDS and MCS were within the reference ranges. Significant elevations (p < 0.05) were observed in rectal temperature, pulse and respiratory rates, as well as a significant drop (p < 0.05) in rumen movements, appetite score, RFS, MDS and MCS was reported in each of OnlyBpgr and BpFlgr comparing with Contgr. These significant changes were demonstrated between OnlyBpgr and BpFlgr for rectal temperatures, pulse and respiration rates, while they were absent for rumen movements, appetite score, RFS, MDS, and MCS. Values of rectal temperatures, pulse and respiration rates were remarkably (p < 0.05) elevated in BpFlgr when they were compared with those in OnlyBpgr (Table 1).

Table 1 Mean values (M ± SD) of temperature, pulse rates, respiration rates, rumen movements, appetite score, RFS, MCS, and MDS in Contgr (n = 30), OnlyBpgr (n = 210), and BpFlgr (n = 10) male camels
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Out of 210 male camels in OnlyBpgr, most of the camels were suffering from loss of appetite (n = 180), fever (n = 185), polypnea (n = 185), tachycardia (n = 185), pale mucous membranes (n = 165), alopecia (n = 100), pruritis (n = 100) and emaciation (n = 100) (Table 2).

Table 2 The most common clinical findings in Contgr (n = 30), OnlyBpgr (n = 210), and BpFlgr (n = 10) male camels
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Out of 10 male camels in BpFlgr, anorexia, pale mucous membranes, alopecia, and pruritis were observed in all filariasis-positive camels. Fever, polypnea and tachycardia were described in most of the male camels with the acute form of filariasis (n = 8). Emaciations were observed in chronic cases of camel filariasis (n = 2) (Table 2; Fig. 1).

Fig. 1
figure 1

Balanoposthitis-filariasis-infected male camels showed balanoposthitis (White arrow)

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All male camels either in OnlyBpgr or BpFlgr had normal lymph nodes and normal lung sounds as well as cough, abnormal nasal discharges, corneal opacity, melena and diarrhea were not described. In contrast, All OnlyBpgr and BpFlgr had signs of orchitis and balanoposthitis (Table 2).

Complete blood picture indices

Whole blood picture indices i.e. RBCs, Hb, PCV, TLC, and DLC, were within the reference ranges in control healthy male camels. OnlyBpgr had normal values of RBCs, Hb, and PCV, while DLC showed neutrophilic leukocytosis. BpFlgr had lower values of RBCs, Hb and PCV as well as eosinophilic leukocytosis was also reported. RBCs, Hb, and PCV values were remarkably (p < 0.05) dropped in BpFlgr compared to Contgr and OnlyBpgr. TLC was significantly (p < 0.05) increased in OnlyBpgr and BpFlgr when compared with control healthy camels. However, these significant changes were not reported between OnlyBpgr and BpFlgr. Furthermore, no significant alterations were demonstrated between Contgr and OnlyBpgr for values of RBCs, Hb, and PCV (Table 3).

Table 3 Mean values (M ± SD) of whole blood picture indices in Contgr (n = 30), OnlyBpgr (n = 210) and BpFlgr (n = 10) male camels
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Microscopic examination of blood samples in diurnal using different methods of blood film preparation i.e., thin film, thick film, and concentration technique, revealed the percentage of infection (Overall prevalence) with microfilaria was 0% in all examined male camels, including Contgr, BpFlgr comparing with and OnlyBpgr (Table 4).

Table 4 Overall prevalence (%) of Camels filariasis (Dipetalonema evansi) in Contgr (n = 30), OnlyBpgr (n = 210) and BpFlgr (n = 10) male camels based on blood films data
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Serum testosterone and cortisol hormones

OnlyBpgr and BpFlgr had significantly (p < 0.05) lower serum testosterone values than those in Contgr. These significant changes were absent between OnlyBpgr and BpFlgr. These values were lower than their reference ranges. Serum levels of cortisol were significantly (p < 0.05) elevated in OnlyBpgr and BpFlgr when compared with their values in Contgr. These significant differences were not observed between OnlyBpgr and BpFlgr whereas their serum cortisol values were higher than their reference ranges (Table 5).

Table 5 Mean values (M ± SD) of serum testosterone and cortisol hormones in Contgr (n = 30), OnlyBpgr (n = 210) and BpFlgr (n = 10) male camels
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Sperm vitality and abnormalities

The percentages of vital sperms were significantly (p < 0.05) higher, however, the percentages of sperms abnormalities were significantly (p < 0.05) lower in Contgr their values in OnlyBpgr and BpFlgr. No remarkable changes were reported between OnlyBpgr and BpFlgr either for sperms vitality percentages or for sperm abnormalities percentages (Table 6).

Table 6 Mean values (M ± SD) of either normal or abnormal sperm percentages in Contgr (n = 30), OnlyBpgr (n = 210) and BpFlgr (n = 10) male camels
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Skin scraping test

Skin scraping test results revealed that Contgr was free from ticks under the microscope (−). The severity of ticks’ infestation was more clear in OnlyBpgr and BpFlgr. Out of 210 camels in OnlyBpgr, 100 male camels had ticks, whereas 10–100 (++) adult ticks were detected microscopically. All camels in BpFlgr (n = 10) were suffering from live ticks’ infestation whereas more than 100 (+++) adult ticks were detected microscopically. The number of live ticks detected microscopically was significantly (p < 0.05) higher in OnlyBpgr and BpFlgr when they compared with their values in Contgr. The number of live ticks was remarkably elevated in BpFlgr compared to OnlyBpgr (Table 7).

Table 7 Skin scraping test results and severity of ticks’ infestation in Contgr (n = 30), OnlyBpgr (n = 210) and BpFlgr (n = 10) male camels
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Gross and histopathological examination

In the present study, out of the infected camels with balanoposthitis (n = 220), 10 camels (4.55%) had lesions and white, slender shape of D. evansi as well as most infections with these mature nematodes were seen in the testes of male camels with balanoposthitis.

Histopathology of the testicular tissues of the healthy male camels showed normal morphological structures, seminiferous tubules lined by germinal epithelium, and Sertoli cells resting on the basement membrane. Sperms were seen in the lumen and interstitial spaces in between the tubules, which contained interstitial cells of Leydig, blood vessels, and lymph vessels (Fig. 2). On the other hand, histopathology of the testicular tissues of the balanoposthitis-affected male camels without filarial infection in OnlyBpgr showed necrosis and atrophy of seminiferous tubule. Furthermore, incomplete spermatogenesis and interstitial mononuclear inflammatory cells infiltration were observed (Fig. 3). In contrast, histopathology of the testicular tissues of the infected male camels with balanoposthitis and filariasis in BpFlgr showed the presence of mature nematodes of filaria in the testes of male camels with balanoposthitis. It described a section of Dipetalonema evansi (is seen free in the luminal area of an artery in the testicular parenchyma. Marked reduction of the number of seminiferous tubules and shedding and dark stained nuclei of degenerating cells were seen. A wide interstitial tissue gap, congested blood vessels, and interstitial edema were associated with inflammatory cell infiltration (Fig. 4).

Fig. 2
figure 2

A photomicrograph of a section in the camel testis showed normal morphological structures of seminiferous tubules (ST) lined by germinal epithelium (G) and Sertoli cells (SE) resting on the basement membrane (BM). Sperms (arrowhead) were seen in the lumen and interstitial spaces (IS) in between the tubules, which contained interstitial cells of Leydig (L), blood vessels, and lymph vessels

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Fig. 3
figure 3

A photomicrograph of a section in camel testis, which had balanoposthitis without filarial infection, showing necrosis and atrophy of seminiferous tubule (arrow). There were incomplete spermatogenesis (arrowhead) and interstitial mononuclear inflammatory cells infiltration (star)

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Fig. 4
figure 4

A photomicrograph of a section in camel testis, which had balanoposthitis, showing a section of Dipetalonema evansi (arrow) is seen free in the luminal area of an artery in the testicular parenchyma. Marked reduction of the number of seminiferous tubules (ST); shedding and degenerating cells had dark stained nuclei. There was a wide interstitial tissue gap, congested blood vessels (BV), and interstitial edema associated with inflammatory cells infiltration

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Correlations between serum testosterone, serum cortisol, percentages of sperm abnormalities, and vitalities in examined male camels

Significant correlations were demonstrated between serum testosterone, serum cortisol, sperm vitality, and sperm abnormalities (Table 8).

Table 8 Pearson correlation coefficient between serum testosterone, serum cortisol, percentages of sperm abnormalities and vitalities in examined male camels
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Positive correlations were reported between serum testosterone levels and sperm vitality percentages, however, negative correlations were stated between serum testosterone and each of serum cortisol and sperm abnormalities either in Contgr, OnlyBpgr or BpFlgr. A significant elevation in serum testosterone in Contgr was associated with a significant raise in sperm vitality percentages. Furthermore, in OnlyBpgr and BpFlgr, significant drop in serum testosterone values was associated with a significant drop in sperm vitality percentages. A significant elevation in serum testosterone in Contgr was associated with a significant drop in each of serum cortisol and sperm abnormalities percentages. A significant drop in serum testosterone values was associated with a significant elevation in sperm vitality percentages in OnlyBpgr and BpFlgr (Table 8).

Serum cortisol concentrations were positively correlated with sperm abnormalities percentages. However, they were negatively correlated with sperm vitality percentages in Contgr, OnlyBpgr, or BpFlgr. A remarkable elevation in serum cortisol was associated with a remarkable increase in sperm abnormalities in OnlyBpgr and BpFlgr, while a significant drop in serum cortisol was associated with a significant drop in sperm abnormalities percentages in Contgr. A remarkable increase in serum cortisol was associated with a remarkable drop in sperm vitality percentages in OnlyBpgr and BpFlgr, while a significant drop in serum cortisol was associated with a significant increase in sperm vitality percentages in Contgr (Table 8).

Negative correlations were observed between sperm vitality percentages and sperm abnormalities percentages either in Contgr, OnlyBpgr or BpFlgr. The significant reduction in sperm abnormalities percentages was associated with a significant elevation in sperm vitality percentages in Contgr. A remarkable elevation in sperm abnormalities percentages was associated with a remarkable reduction in sperm vitality percentages in OnlyBpgr and BpFlgr (Table 8).

Discussion

Clinical findings

Several clinical manifestations correlated with camel filariasis include scrotal and testicular enlargement, localized skin lesions, severe exhaustion, emaciation, and high body temperatures [13, 42]. Referring to the current study, the control male camels showed normal clinical findings whereas temperature, pulse and respiratory rates, rumen movements, appetite score, RFS, MDS, and MCS were within the reference ranges mentioned by Fowler et al. [20]; Hutjens [21]; Bhatt et al. [43]; Nielsen [44]; Bramley et al. [45]; Hamad et al. [46]; Hassan et al. [47]; Kamr et al. [48]; Mohamed et al. [49]. On the other side, OnlyBpgr and BpFlgr had significant elevations in rectal temperature, pulse and respiratory rates as well as a significant drop in rumen movements, appetite score, RFS, MDS and MCS comparing with Contgr. These significant changes were demonstrated between OnlyBpgr and BpFlgr for rectal temperatures, pulse, and respiration rates, while they were absent for rumen movements, appetite score, RFS, MDS and MCS. Rectal temperatures, pulse, and respiration rates were remarkably elevated in BpFlgr when they compared with those in OnlyBpgr. These results were confirmed by Abdel-Rady [12]; Muhammad et al. [50]; Kachhawaha et al. [51]. Muhammad et al. [50]; Kachhawaha et al. [50] hypothesized that the increase in body temperature might be caused by the stress because of microfilaria migration in the host’s body. An increase in heart rate and respiratory rate was used to compensate up for anemia and meet the body’s oxygen needs.

The previous reports mentioned that camels naturally infected with microfilaria displayed fever, rigidity in their movements, emaciation, pale mucous membranes, and decreased appetite [51, 52]. These findings and results were mentioned also by Abdel-Rady [12]; Karram et al. [13]; Agag et al. [52] and supporting the current results, which referred to variations in percentages of involved male camels that had clinical abnormalities either in OnlyBpgr and BpFlgr. Most of the camels in OnlyBpgr suffered from loss of appetite, fever, polypnea, tachycardia, pale mucous membranes, alopecia, pruritis and emaciation. On the other hand, all infected male camels in BpFlgr had anorexia, pale mucous membranes, alopecia, and pruritis. BpFlgr had signs of Fever, polypnea, and tachycardia that were described in most male camels with acute filariasis. Emaciations were observed in chronic cases of camel filariasis. Moreover, all male camels either in OnlyBpgr or BpFlgr had normal lymph nodes and normal lung sounds as well as cough, abnormal nasal discharges, corneal opacity, melena and diarrhea were not described. All OnlyBpgr and BpFlgr had signs of orchitis and balanoposthitis. In contrast, Muhammad et al. [50]; Kachhawaha et al. [51] reported that clinical examination in camel filariasis recorded swollen pharyngeal lymph nodes. Abdel-Rady [12] differentiated between the acute and chronic forms of camel filariasis, with the chronic form characterized by generalized debility and emaciation in camels. The acute form is distinguished by unwillingness to move, severe orchitis, and balanoposthitis. Some similarities in clinical finding between the current study and what were reported by Abdel-Rady [12] might be attributed to the fact that the organs i.e. mainly testis and prepuce, affected by the parasites in the current study were the same organs affected in camels studied by these investigators. Furthermore, Chhabra and Gupta [53] added that mild infections of D. evansi were not diagnosed. Cachexia, possibly orchitis, neurological manifestations, and probably death were the signs of severe illnesses. Dipetalonemiasis symptoms included reduced appetite, fatigue, pale mucous membranes, orchitis, arteriosclerosis, spermatic cord aneurysms, and heart failure.

Blood picture indices

The number of positive filariasis blood films at midnight was much higher than what was collected at midday [54, 55]. The prevalence of D. evansi microfilariae in blood samples ranged from 0.88 to 46.7%, according to other earlier investigations [56]. The control camels in the current study had normal values of blood pictures indices that were supported by Fowler [20]; Adah et al. [55]; Poonia et al. [57]; Khalphallah et al. [58]. OnlyBpgr in the current work had normal values of RBCs, Hb and PCV while DLC showed neutrophilic leukocytosis. BpFlgr was suffering from anemia as they had lower values of RBCs, Hb and PCV as well as eosinophilic leukocytosis was also reported. Comparing different investigated male camel groups, BpFlgr had lower values of RBCs, Hb and PCV comparing with Contgr and OnlyBpgr. TLC was significantly increased in OnlyBpgr and BpFlgr compared to control healthy camels. Hence, these significant changes were absent between OnlyBpgr and BpFlgr.

Furthermore, Contgr and OnlyBpgr had no significant difference between each other either for values of RBCs, Hb or PCV. These results were supported by Muhammad et al. [50]; Kachhawaha et al. [51]. On the other hand, the severity of the hemoglobin decrease caused by microfilariae feeding on the blood in peripheral blood was dependent on the number of worms present. The most significant hematological change was eosinophilia [50].

Microscopic examination of blood samples in diurnal i.e., at mid-day, using different methods of blood film preparation, revealed that the percentage of microfilaria infection was 0% in all examined male camels i.e., Contgr, OnlyBpgr, and BpFlgr. These results were supported by Adah et al. [55], who revealed a correlation between the number of microscopically positive cases for camel filariasis and the number of blood samples collected during the day and night. Additionally, the blood samples collected at night gave more positive cases although the number of blood samples collected during the day was higher than that of night. This may be due to the nocturnal periodicity of D. evansi microfilariae, as 8 of 143 examined blood samples (5.59%) taken at night were positive. This means that, compared to the diurnal sample, nocturnal sampling increased the likelihood of finding microfilaria. Saleh [54] also added that microfilariae were 10 times more likely to be found in blood samples taken at night than in those taken during the day. El-Amin et al. [59] indicated that microfilariae had a biphasic periodicity pattern with peak concentrations around 8 p.m. and between 4 and 6 a.m. These findings were different from those noted by Karram et al. [13], who showed that the microfilairae count in camel blood was unaffected by time of day or night but was influenced by a febrile state. This nocturnal behavior of microfilariae might be owed to chemotactic substances found in D. evansi larvae that are altered by day and night.

Serum testosterone and cortisol hormones

All diseased camels through the present work suffered from orchitis and balanoposthitis that reflected serum levels of testosterone and cortisol. OnlyBpgr and BpFlgr had significantly lower values of serum testosterone than those in Contgr. These significant changes were absent between OnlyBpgr and BpFlgr. These values were lower than their reference ranges mentioned by Tibary and Anouassi [60]; Deen [61]. Compared to the non-breeding season, testosterone levels in blood plasma and testicular tissue increased dramatically during the breeding season. Testicular tissue also had a greater testosterone concentration than blood [62]. Males’ testosterone levels are frequently necessary for proper spermatogenesis [63, 64] and reproductive tract function [65].

Additionally, testosterone was crucial for avoiding apoptotic cell death in tissues that depended on androgens [66, 67]. Both the proliferation and the level of testosterone in the testis were negatively correlated with the degree of apoptosis. As a result, testosterone played a crucial role as both a testicular product and a regulator of the testis’s functions [64]. Regarding to the current study, serum levels of cortisol were significantly elevated in OnlyBpgr and BpFlgr when compared with their values in Contgr. These significant differences were not observed between OnlyBpgr and BpFlgr, whereas their serum cortisol values were higher than their reference ranges mentioned by Saeb et al. [68]. Since excess cortisol was synthesized and released into the systemic circulation under stressful conditions, measuring blood cortisol concentration was utilized as a standard approach for detecting stress in farm animals [69]. In general, cortisol supports energy consumption, reproduction, immunological response, inflammatory processes, growth, and brain function to assist the body `in maintaining homeostasis. Nevertheless, sustained elevations in glucocorticoid levels had a detrimental effect on immunological response or reproductive activity [70, 71].

Sperm vitality and abnormalities

Orchitis and balanoposthitis were described in all diseased camels in both OnlyBpgr and BpFlgr, as the previous reports mentioned that the testes were in charge of spermatozoa production and androgen secretion. Cellular differentiation took place over a long time to produce the spermatozoon. Based on biochemical and cytochemical changes, morphofunctional modifications arose during this process [72, 73]. Testosterone in males is necessary for optimal spermatogenesis [63, 64] and proper reproductive tract function [65]. The present study reported a significant reduction in sperm vitality percentages as well as a significant increase in sperm abnormalities percentages in OnlyBpgr and BpFlgr compared to Contgr. No remarkable changes were reported between OnlyBpgr and BpFlgr either for sperm vitality percentages or for sperm abnormalities. These results were supported by previous research by Suresh et al. [74], in which androgen deprivation caused an immediate arrest in the meiotic transition of primary spermatocytes to spermatids, thereby halting sperm production. According to a number of studies, testosterone also affects the epididymis’ size and function, impacting the maturation and survival of spermatozoa during epididymal transit [75, 76].

Additionally, the production of certain caput and cauda epididymal proteins was impacted by the testosterone hormone. Some of these proteins may be crucial for spermatozoa’s development, storage, and acquisition of fertilization potential [77]. On the other hand, in such a natural mating reproductive management, poor male fertility could result in significant pregnancy failures. One of the main causes of slowing down and disrupting the spermatogenesis processes, which led to low sperm concentration and quality, was testicular degeneration, which might be brought on by infections, chemicals, and environmental factors. It was demonstrated that D. evansi-caused filariasis could result in orchitis and spermatic cord hematomas [78, 79].

Skin scraping test

Camels with both the acute and chronic forms of camel filariasis have hard ticks on them. Hard tick infestations were found in 11 out of 13 positive cases; no lakes or mosquito populations were found in surrounding areas of the positive cases [12]. This observation agreed with the results obtained by Ramadan [80], who stated that Hard ticks collected from microfilaria-infected camels had the microfilariae separated from their mouth and body cavities. These results confirmed the findings of the current study in which skin scraping test results revealed a higher severity of live ticks’ infestation in BpFlgr than that in OnlyBpgr because, unlike OnlyBpgr, all camels in BpFlgr were suffering from live ticks’ infestation. According to Liebish [38]; Greiner [39]; Bowman [40], Contgr were free from ticks under the microscope (−). The severity of ticks’ infestation was clearer in OnlyBpgr (++) and BpFlgr (+++). The numbers of live ticks detected microscopically were significantly higher in BpFlgr when comparedto their values in OnlyBpgr. On the other hand, Abdel-Rady [12] confirmed the high incidence rates of filariasis in the El-Wady El-Gaded governorate, which might be attributed to the presence of hard ticks, the disease’s primary vector, which was present on all suspected and infected camels in a heavy manner (microscopically confirmed and clinically ill), as well as other predisposing factors like breeding, fluctuation of temperature in day and night, and management systems, were mentioned.

Gross and histopathological examination

It was stated that D. evansi filariasis could produce orchitis and spermatic cord hematomas by compromising spermatogenesis processes, resulting in low sperm concentration and quality [78, 79]. Moreover, in the arteries of the spermatic cords, white adult nematodes were discovered during macroscopic examinations of infected testis [81]. In the present study, out of the infected camels with balanoposthitis (n = 220), 10 camels (BpFlgr; 4.55%) had lesions and white, slender shape of D. evansi as well as most of the infections with these mature nematodes were seen in the testes of male camels with balanoposthitis (BpFlgr). Kheirandish et al. [81] supported the current results, whereas they mentioned that the five infected samples in male camels had gross lesions and white, slender D. evansi. Sazmand et al. [82] reported that 13.89% of camels contained adult nematodes in one organ. They found that mature D. evansi nematode infections tended to occur more frequently in the testes and that males were considerably more susceptible than females to have macroscopic adult worm infections.

On the other hand, D. evansi filariasis could additionally affect other tissues such as the mesentery, lymph nodes, right auricle, and pulmonary arteries [83]. The current study reported the presence of mature adult filaria in the camels’ testes in BpFlgr. In contrast, the presence of mature nematode in the testicular tissue was a rare condition. Another helminth that could infect the testis was Dirofilaria. In other research, D. immitis and D. repens were found in the spermatic cord, epididymis, and scrotum [84,85,86]. However, D. repens frequently caused subcutaneous nodules, while D. immitis mostly affected the cardiovascular system. Only human, cat, and dog infections with Dirofilaria were reported [87]. On the other hand, testicular dirofilariasis was a rare illness, and most reported cases involved the subcutaneous form in the scrotum. However, according to one study [88], D. evansi was present in the testicular tissue of 50% of the rats. Accordingly, the filariasis produced by D. evansi represented a unique parasitic manifestation of adult nematodes in the tissues of the male camels’ testicular organs.

Regarding the current study, histopathology of the testicular tissues of the healthy male camels showed normal morphological structures of the seminiferous tubules. Sperms were seen in the lumen and interstitial spaces between the tubules, which contained interstitial cells of Leydig, blood vessels, and lymph vessels. On the other hand, in OnlyBpgr, histopathology of the testicular tissues of the balanoposthitis-affected male camels without filarial infection showed necrosis and atrophy of seminiferous tubule. Furthermore, incomplete spermatogenesis and interstitial mononuclear inflammatory cell infiltration were observed. In contrast, the infected male camels in BpFlgr showed histopathologically the presence of mature nematodes of filaria in the testes of male camels with balanoposthitis. Marked reduction of the number of seminiferous tubules as well as shedding and degenerating cells with dark stained nuclei were seen.

Moreover, a wide interstitial tissue gap, congested blood vessels, and interstitial edema associated with inflammatory cells infiltration were reported. These results were confirmed by Chhabra and Gupta [53]; Kheirandish et al. [81]; Sazmand et al. [82]. According to Kheirandish et al. [81], spermatogenetic activity, increased interstitial space tubules, obstruction of testicular blood vessels by parasites, hypertrophy of blood vessels, degenerative and necrosis changes in the tubules, and destruction of the spermatogenic cells were all noted through their histopathological examination of D. evansi-infected testis. They also added that all stages of spermatogenic cells occurred in most seminiferous tubules, such as spermatogonia, primary and secondary spermatocytes, and round spermatids. In most of the seminiferous tubules, spermatozoa were observed in their lumens. Degenerative alterations in the seminiferous tubules had been observed along with the presence of adult nematodes in the spermatic cord. Moreover, Sazmand et al. [82] showed fibrosis, atrophy, and inflammation in testes from infected camels with D. evansi. Additionally, they noted the necrosis and sloughing of germ cells, arterial wall inflammation with hemorrhage in a few interstitial tissue locations, and eosinophil and lymphocyte infiltration.

Correlations between serum testosterone, serum cortisol, percentages of sperm abnormalities, and vitalities in examined male camels

Significant correlations were demonstrated between serum testosterone, serum cortisol, sperm vitality, and sperm abnormalities. Positive correlations were reported between serum testosterone levels and sperm vitality percentages. However, negative correlations were stated between serum testosterone and each of serum cortisol and sperm abnormalities either in Contgr, OnlyBpgr, or BpFlgr. Serum cortisol concentrations were positively correlated with sperm abnormalities percentages. However, they were negatively correlated with sperm vitality percentages in Contgr, OnlyBpgr, or BpFlgr. Negative correlations were observed between sperm vitality percentages and sperm abnormalities percentages either in Contgr, OnlyBpgr, or BpFlgr.

Conclusion

The study confirmed the association of the changes in clinical findings, whole blood picture, serum testosterone, serum cortisol, and semen analysis, with OnlyBpgr and BpFlgr. These changes were more prominent in BpFlgr than in OnlyBpgr. These changes were also more evident in BpFlgr and OnlyBpgr than in Contgr. Skin scraping test results revealed a higher severity of live ticks’ infestation in BpFlgr than in OnlyBpgr because, unlike OnlyBpgr, all camels in BpFlgr (n = 10) were suffering from live ticks’ infestation. The present work also concluded the higher efficacy of histopathology of testicular tissues in male camels as a diagnostic tool for adult filaria in balanoposthitis-affected male camels than blood smear because all cases of camel filariasis in the current work were negative for microfilaria on microscopic examination of diurnal blood smear as well as testicular histopathology revealed detection of adult filaria in all camel filariasis associated with balanoposthitis. Strong correlations were demonstrated between serum testosterone, serum cortisol, and semen analysis results. Positive correlations were reported between serum testosterone levels and sperm vitality percentages. However, negative correlations were stated between serum testosterone and each of serum cortisol and sperm abnormalities either in Contgr, OnlyBpgr or BpFlgr. Serum cortisol concentrations were positively correlated with sperm abnormalities percentages. However, they were negatively correlated with sperm vitality percentages in Contgr, OnlyBpgr, or BpFlgr. Negative correlations were observed between sperm vitality percentages and sperm abnormalities percentages either in Contgr, OnlyBpgr, or BpFlgr.

Availability of data and materials

The datasets used and/or analyzed during the current study are available from the corresponding author upon reasonable request. Data was also available after publishing in this journal.

Abbreviations

BpFlgr :

balanoposthitis-filariasis infected male camels group

D. evansi :

(Dipetalonema evansi)

DLC:

differential leukocytic count

Hb:

hemoglobin

OnlyBpgr :

only balanoposthitis without filariasis male camels group

MCS:

manure condition score

MDS:

manure digestion score

PCV:

packed cell volume

RBCs:

red blood corpuscles

RFS:

rumen filling score

TLC:

total leucocytic count

OnlyBpgr :

only balanoposthitis without filariasis male camels group

References

  1. Gaughan JB. Which physiological adaptation allows camels to tolerate high heat load–and what more can we learn? J Camelid Sci. 2011;4:85–8.

    Google Scholar 

  2. Faye B. Role, distribution and perspective of camel breeding in third millennium economies. Emir J Food Agric. 2015;27(4):318–27.

    Article  Google Scholar 

  3. Tibary A, El Allali K. Dromedary camel: A model of heat resistant livestock animal. Theriogenol. 2020;154:203–11.

    Article  Google Scholar 

  4. Marai I, Zeidan A, Abdel-Samee A, Abizaid A, Fadiel A. Camels’ reproductive and physiological performance traits as affected by environmental conditions. Trop Subtro Agroecosyst. 2009;10:129–49.

    Google Scholar 

  5. Baraka TA, El-sherif MT, Kubesy AA, Illek J. Clinical studies of selected ruminal and blood constituents in dromedary camels affected by various diseases. Acta Vet Brno. 2000;69(1):61–8.

    Article  Google Scholar 

  6. Shafqaat A, Butt AA, Muhammad G, Athar M, Khan MZ. Haematobiochemical studies on the haemoparasitized camels. Intl J Agric Biol. 2004;6:331–4.

    Google Scholar 

  7. Elamin EA, Mohamed GE, Fadl M, Elias S, Saleem MS, El-Bashir MO. An outbreak of cameline filariasis in the Sudan. British Vet J. 1993;149(2):195–200.

    Article  CAS  Google Scholar 

  8. Oryan A, Valinezhad A, Bahrami S. Prevalence and pathology of camel filariasis in Iran. Parasitol Res. 2008;103(5):1125–31.

    Article  PubMed  CAS  Google Scholar 

  9. Duvallet G, Boireau P. Other vector-borne parasitic diseases: animal helminthiases, bovine besnoitiosis and malaria. Rev Sci Tech. 2015;34(2):651–49.

    PubMed  CAS  Google Scholar 

  10. Hashem MA, Badawy A. Haematological and biochemical studies on filariasis. Int J Vet Med. 2008;4(2):1–7.

    Google Scholar 

  11. Higgins ASJ, Allen WR, Mayhew IG, Snbow DH. An introduction to the camel in heath and disease. In: Proceedings of 1st international camel conference. Dubai. 1992:9–17.

  12. Abdel-Rady A. Prevalence of Filariasis in camels (Camelus dromedarius) in upper Egypt with special reference to treatment. J Parasit Dis. 2021;45:930–6.

    Article  PubMed  PubMed Central  Google Scholar 

  13. Karram MH, Ibrahim H, Abdel-all TS, Manaa AM. Clinical and haematological changes in camel infected with Trypanosoma evansi and microfilaria. Assiut Vet Med J. 1991;25(49):118–24.

    Google Scholar 

  14. Ali GA. Ecto and endoparasites of camel. PhD thesis. Assiut Egypt: Faculty of Veterinary Medicine Assiut University; 2005.

    Google Scholar 

  15. Borji H, Ramzi G, Parandeh S. Epidemiological study on haemoparasites of dromedary in Iran. J Camel Pract Res. 2009;16(2):217–9.

    Google Scholar 

  16. Skidmore JA. The main challenges facing camel reproduction research in the 21st century. Reprod Suppl. 2003;61:37–47.

    PubMed  CAS  Google Scholar 

  17. Coles EH. In: Saunders WB, editor. Veterinary Clinical Pathology, vol. 46–47. 4th ed. USA: Philadelphia; 1986. p. 132–9.

  18. Shahin MA, Khalil WA, Saadeldin IM, Swelum AA, El-Harairy MA. Comparison between the effects of adding vitamins, trace elements, and nanoparticles to SHOTOR extender on the cryopreservation of dromedary camel Epididymal spermatozoa. Animals (Basel). 2020;10(1):78.

    Article  PubMed  PubMed Central  Google Scholar 

  19. Abdally MH. Acaricidal efficacy of Ivomec (Ivermectin) and Dectomax (Doramectin) on Sarcoptic mange mites (Sarcoptes spp.) of Arabian camels (Camelus dromedarius) in Saudi Arabia. J Entomol. 2010;7:95–100.

    Article  CAS  Google Scholar 

  20. Fowler ME. Medicine and surgery of camelids, vol. 408. 3rd ed. USA: IO:Ames; Blackwell Publishing Ltd; 2010. p. 89–109.

    Google Scholar 

  21. Hutjens M. Manurology 101. Dairy Today. 1996:26. https://www.scribd.com/document/550026414/Manure-evaluation-Milkproduction-com.

  22. Hulsen J, Cow signals. How to understand the speech of cows. Praha. ISBN 978-80-86726;: Profi Press s.r.o; 2007.

    Google Scholar 

  23. Burfeind O, Sepúlveda P, von Keyserlingk MAG, Weary DM, Veira DM, Heuwieser W. Technical note: evaluation of a scoring system for rumen fill in dairy cows. J Dairy Sci. 2010;93(8):3635–40.

    Article  PubMed  CAS  Google Scholar 

  24. Götze K, Crivellaro P, Pieper L, Engelhard T, Staufenbiel R. Assessment of rumen fill in dairy cows for evaluation of the individual feed intake in herd management. Tierarztl Prax Ausg G Grosstiere Nutztiere. 2019;47(1):5–13.

    PubMed  Google Scholar 

  25. Khalphallah A, Elmeligy E, Aamer AA, AbdelAll T, Oikawa S. Nakada K diagnostic and prognostic significance of serum gastrin and pepsinogen in displaced abomasum dairy cows. BJVM. 2018;21(1):67–75.

    Article  Google Scholar 

  26. Khalphallah A, Aamer AA, AbdelAll T, Elmeligy E, Oikawa S, Nakada K. Changes in clinical and blood lipid metabolism parameters in Holstein dairy cattle during the transition period. BJVM. 2018;21(4):420–8.

    Article  Google Scholar 

  27. Elmeligy E, Oikawa S, Mousa SA, Bayoumi SA, Hafez A, Mohamed RH, et al. Role of insulin, insulin sensitivity and abomasal functions monitors in evaluation of the therapeutic regimen in ketotic dairy cattle using combination therapy with referring to milk yield rates. Open Vet J. 2021;11(2):228–37.

    Article  PubMed  PubMed Central  Google Scholar 

  28. Harvey JH. Atlas of veterinary hematology. USA: Pennsylvania; Philadelphia; WB Saunders Company; Elsevier; 2001. p. 3–74.

    Book  Google Scholar 

  29. Latimer KS, Mahaffey EA, Prasse KW. Duncan and Prasse's veterinary laboratory medicine: clinical pathology. 5th ed. USA: Iowa; Wiley-Blackwell; Blackwell Publishing Ltd; 2011. p. 3–82.

    Google Scholar 

  30. Weiss DJ, Wardrop KJ. Schalm’s veterinary hematology. 6th ed. USA: Ames; Iowa; Wiley-Blackwell Publishing Ltd; Wiley-Blackwell; 2010. p. 123–421.

    Google Scholar 

  31. Zajac AM, Conboy GA. Veterinary Clinical Parasitology. 8th ed. USA: Iowa 50014–8300; Ames 2121 State Avenue Wiley-Blackwell Publishing Ltd John Wiley & Sons Inc 2012, 185–208.

    Google Scholar 

  32. Lawrence R, Thomas C. A guide to laboratory procedures and identification. USA: Chicago; American Society of Clinical Pathologists; 1987. p. 328.

    Google Scholar 

  33. Moskovtsev and Librach. Methods of sperm vitality assessment. In: In: spermatogenesis. Springer; 2013. p. 13–9.

    Chapter  Google Scholar 

  34. Menon AG, Thundathil JC, Wilde R, Kastelic JP, Barkema HW. Validating the assessment of bull sperm morphology by veterinary practitioners. Can Vet J. 2011;52(4):407–8.

    PubMed  PubMed Central  Google Scholar 

  35. Soulsby EJI. Helminths, arthropods and protozoa of domesticated animals. 7th ed. UK: London; Tindall; Bailliere; 1986. p. 809.

    Google Scholar 

  36. Urquhart GM, Armour J, Duncan AM, Jennings FW. Veterinary parasitology. 3rd ed. USA: Ames; IA; Blackwell Science Ltd; 2003. p. 4–78.

    Google Scholar 

  37. Urquhart GM, Armour J, Duncan JL, Dunn AM, Jennings FW. Veterinary parasitology. 1st ed. England: Longman Scientific and Technica; 1987.

    Google Scholar 

  38. Liebish A. Bayticol pour-on: A new product and a new method for the control of stationary ectoparasites in cattle. Vet Med Rev. 1986;1:17–27.

    Google Scholar 

  39. Greiner E. Diagnosis of arthropod parasites. In: Zajac AM, Conboy GA, editors. Veterinary clinical parasitology. 8th ed. USA: Wiley-Blackwell; 2012. p. 217–302.

    Google Scholar 

  40. Bowman DD. Parasites of Ruminants, Diagnostic Parasitology. In: Georgis’ Parasitology for Veterinarians. 10th ed. USA: Missouri 63043; St. Louis; Elsevier Saunders; 2014. p. 358–369.

  41. Bancroft JD, Gamble M. Theory and practice of histological techniques book. USA: New York; Churchil Livingstone; Elsevier; 2008.

    Google Scholar 

  42. Abu El-Magd MM, Agag BI, El-Seify MA, Ragab AM. Electrophoretic pattern of camel sera infected with Dipetalonema evansi microfilariae before and after treatment by Ivermectin (Ivomic M., S. & D. In: Proceeding of 3rd scientific congress. Assiut Egypt: Faculty of Veterinary Medicine, Assiut University; 1988. p. 147–59.

    Google Scholar 

  43. Bhatt FL, Kholi RN, Rathore US. The normal body temperature, respiratory frequency and heart rate of the camel. Indian Vet J. 1960;37:456–62.

    Google Scholar 

  44. Nielsen KS. Desert Animals. Adaptation and environment. Oxford University Press; 1964. p. 277.

    Google Scholar 

  45. Bramley E, Costa ND, Fulkerson WJ, Lean IJ. Associations between body condition, rumen fill, diarrhoea and lameness and ruminal acidosis in Australian dairy herds. N Z Vet J. 2013;61(6):323–9.

    Article  PubMed  CAS  Google Scholar 

  46. Hamad B, Aggad H, Hadef L, Adaika A. Effect of cold and hot seasons on thermoregulation and hemogram blood parameters of dromedary camel (Camelus dromedarius) in Algeria. Livestock Res Rural Dev. 2017;29(7):1–8.

    Google Scholar 

  47. Hassan HY, Gadallah S, Kamr A, Abdelazeim A. Serum iron, calcium, phosphorus and magnesium concentrations and their effects on hemato-immune dynamics in diseased camels (Camelus dromedarius). EC Veterin Sci. 2019;4(10):1–11.

    Google Scholar 

  48. Kamr A, Gadallah S, Arbaga A, Hassan HY. Oxidant and antioxidant biomarkers and the risk factor of age on their concentrations in pneumonic Arabian camels (Camelus dromedarius). J Camelid Sci. 2020;13:40–8.

    Google Scholar 

  49. Mohamed RH, Khalphallah A, Nakada K, Elmeligy E, Hassan D, Ebissy EA, et al. Clinical and correlated responses among steroid hormones and oxidant/antioxidant biomarkers in pregnant, non-pregnant and lactating CIDR-pre-synchronized dromedaries (Camelus dromedarius). Vet Sci. 2021;8(11):247.

    Article  PubMed  PubMed Central  Google Scholar 

  50. Muhammad SA, Farooq AA, Akhtar MS, Hayat CS. Dipetalonemiasis in a dromedary camel and its treatment. Pak Vet J. 2004;24(4):205–6.

    Google Scholar 

  51. Kachhawaha S, Srivastava MK, Kachhawa JP, Mugdal NK, Daga M, Kachhwaha S, et al. Microfilariasis in a camel (Camelus dromedarius)–A case report. J Camel Prac Res. 2013;20(2):207–8.

    Google Scholar 

  52. Agag BI, Nasser MH, Abu-El-Magd MM, Hafez IA. Clinical and biochemical studies on microfilaria and trypanosoma infected camels. Assiut Vet Med J. 1993;29(57):125–34.

    Google Scholar 

  53. Chhabra MB, Gupta SK. Parasitic diseases of camels- an update, 2 helminthoses. J Camel Pract Res. 2006;13(2):81–7.

    Google Scholar 

  54. Saleh M. Incidence of camel microfilaria among coast guard borders. MVSc thesis. Cairo University Egypt: Faculty of Veterinary Medicine; 1976.

    Google Scholar 

  55. Adah AS, Ayo JO, Rekwot PI, Aluwong T, Arimie DI. Haematological profile of the one-humped camel subjected to packing (load-carrying) in the harmattan season in the semi-arid region of Nigeria. Bangladesh J Vet Med. 2017;15(1):39–44.

    Article  Google Scholar 

  56. Sazmand A, Joachim A. Parasitic diseases of camels in Iran (1931-2017) - a literature review. Parasite. 2017;24:21.

    Article  PubMed  PubMed Central  Google Scholar 

  57. Poonia R, Srivastava A, Sena S, Srivastava M. Study on certain blood and serum parameters of camel Camelus dromedarius maintained on different diets. UK J Pharm Biosci. 2016;4(6):12–8.

    Article  CAS  Google Scholar 

  58. Khalphallah A, Elmeligy E, Zakaria AM, Ghallab RS, Abdulkarim A, Mohamed RH. Comparative study of efficacy of prepartum injection of multivitamins and selenium- vitamin E (ά-tocopherol)-combination on post-partum clinical findings, serum steroids, calf and placental weights, and milk antioxidant biomarkers changes in female dromedary camel. Open Vet J. 2022;12(5):657–67.

    Article  PubMed  PubMed Central  Google Scholar 

  59. El-Amin EA, Mohamed GE, Fadl M, Elias S, Saleem MS, Elbashir MOA. An outbreak of Cameline filariasis in the Sudan. Br Vet J. 1993;149(2):195–201.

    Article  CAS  Google Scholar 

  60. Tibary A, Anouassi A. Theriogenology in camelidae. Anatomy, physiology, pathology and artificial breeding. Morocco: Rabat; IAV HassanII; Actes Ed.; 1997. p. 489.

  61. Deen A. Testosterone profiles and their correlation with sexual libido in male camels. Res Vet Sci. 2008;85(2):220–6.

    Article  PubMed  CAS  Google Scholar 

  62. El-Harairy MA, Attia KA. Effect of age, pubertal stage and season on testosterone concentration in male dromedary camel. Saudi J Biol Sci. 2010;17(3):227–30.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  63. McLachlau RL, Wreford NG, O’Donnell L, de Kretser DM, Robertson DM. The endocrine regulation of spermatogenesis: independent roles for testosterone and FSH. J Endocrinol. 1996;148(1):1–9.

    Article  Google Scholar 

  64. Goeritz F, Quest M, Wagener A, Fassbender M, Broich A, Hildebrandt TB, et al. Seasonal timing of sperm production in roe deer: interrelationship among changes in ejaculate parameters, morphology and function of testis and accessory glands. Theriogenol. 2003;59(7):1487–502.

    Article  CAS  Google Scholar 

  65. Luke MC, Coffey DS. The male sex accessory tissues. Structure, androgen action and physiology. In: Knobil E, Neill DS, editors. The physiology of reproduction. USA: New York; Raven Press; 1994. p. 1435–87.

    Google Scholar 

  66. Thompson EB. Apoptosis and steroid hormone. Mol Endocrinol. 1994;8:665–73.

    PubMed  CAS  Google Scholar 

  67. Hikim AP, Amador AG, Klemcke HG, Bartke A, Russell LD. Correlative morphology and endocrinology of Sertoli cells in hamster testes in active and inactive states of spermatogenesis. Endocrinol. 1989;125(4):1829–43.

    Article  CAS  Google Scholar 

  68. Saeb M, Baghshani H, Nazifi S, Saeb S. Physiological response of dromedary camels to road transportation in relation to circulating levels of cortisol, thyroid hormones and some serum biochemical parameters. Trop Anim Health Prod. 2010;42(1):55–63.

    Article  PubMed  CAS  Google Scholar 

  69. Mormède P, Andanson S, Aupérin B, Beerda B, Guémené D, Malmkvist J, et al. Exploration of the hypothalamic–pituitary–adrenal function as a tool to evaluate animal welfare. Physiol Behav. 2007;92(3):317–39.

    Article  PubMed  Google Scholar 

  70. Minton. Function of the hypothalamic-pituitary-adrenal axis and the sympathetic nervous system in models of acute stress in domestic farm animals. J Anim Sci. 1994;72(7):1891–8.

    Article  PubMed  CAS  Google Scholar 

  71. Möstl E, Palme R. Hormones as indicators of stress. Domest Anim Endocrinol. 2002;23(1–2):67–74.

    Article  PubMed  Google Scholar 

  72. Baccetti. Insect sperm cells. Adv Insect Physiol. 1972;9:315–97.

    Article  CAS  Google Scholar 

  73. Fawcett DW. The mammalian spermatozoon. Dev Biol. 1975;44(2):394–436.

    Article  PubMed  CAS  Google Scholar 

  74. Suresh R, Medhamurthy R, Moudgal NR. Comparative studies on the effects of specific immunoneutralisation of endogenous FSH or LH on testicular germ cell transformation in the adult bonnet monkey (Macaca radiata). Am J Reprod Immunol. 1995;34(1):35–43.

    Article  PubMed  CAS  Google Scholar 

  75. Robaire B, Viger RS. Regulation of epididymal epithelial cell functions. Biol Reprod. 1995;52(2):226–36.

    Article  PubMed  CAS  Google Scholar 

  76. Hinton BT, Palladino MA, Rudolph D, Lan ZJ, Labus JC. The role of the epididymis in the protection of spermatozoa. Curr Top Dev Biol. 1996;33:61–102.

    Article  PubMed  CAS  Google Scholar 

  77. De Pauw IM, IGoff AK, van Soom A, Verberckmoes S, De Kruif A. Hormonal regulation of bovine secretory proteins derived from caput and cauda epididymal epithelial cell cultures. J Androl. 2003;24(3):401–7.

    Article  PubMed  Google Scholar 

  78. Amin YA, Noseer EA, Fouad SS, Ali RA, Mahmoud HYAH. Changes of reproductive indices of the testis due to Trypanosoma evansi infection in dromedary bulls (Camelus dromedarius): semen picture, hormonal profile, histopathology, oxidative parameters, and hematobiochemical profile. J Adv Vet Anim Res. 2020;7(3):537–45.

    Article  PubMed  PubMed Central  Google Scholar 

  79. Moghaddar N, Oryan A, Hanifepour M. Helminths recovered from the liver and lungs of camel with special reference to their incidence and pathogenesis in shiraz, Islamic Republic of Iran. Indian J Anim Sci. 1992;62:1018–23.

    Google Scholar 

  80. Ramadan EI. Studies of Acanthochilonema evanosi with special reference to the distribution of microfilariae in the different organs of the camel and their elimination from circulatory blood. PhD thesis. Cairo University Egypt: Faculty of Veterinary Medicine; 1982.

    Google Scholar 

  81. Kheirandish R, Azizi S, Nourollahifard S, Imani M, Kermani RS, Hassanzadeh S. Histopathologic and histomorphometric evaluation of Dipetalonema evansi infection in camel testicular tissue. J Parasit Dis. 2021;45(4):959–63.

    Article  PubMed  PubMed Central  Google Scholar 

  82. Sazmand A, Tafti MH, Hekmatimoghaddam S, Moobedi I. Dipetalonema evansi infection in camels of Iran's central area. Pak J Biol Sci. 2013;16(13):647–50.

    Article  PubMed  Google Scholar 

  83. Dakkak A, Ouhelli H. Helminthes and helminthoses of dromedary: a review of the literature. Rev Sci Tech-Off Int Epizoot. 1987;6:447–61.

    Google Scholar 

  84. Pampiglione S, Elek G, Pálfi P, Vetési F, Varga I. Human Dirofilaria repens infection in Hungary: a case in the spermatic cord and a review of the literature. Acta Vet Hung. 1999;47(1):77–83.

    Article  PubMed  CAS  Google Scholar 

  85. Theis JH, Gilson A, Simon GE, Bradshaw B, Clark D. Case report: unusual location of Dirofilaria immitis in a 28-year-old man necessitates orchiectomy. Am J Trop Med Hyg. 2001;64(5–6):317–22.

    Article  PubMed  CAS  Google Scholar 

  86. Singh R, Shwetha JV, Samantaray JC, JBando G. Dirofilariasis: a rare case report. Indian J Med Microbiol. 2010;28(1):75–7.

    Article  PubMed  CAS  Google Scholar 

  87. Simón F, Siles-Lucas M, Morchón R, González-Miguel J, Mellado I, Carretón E, et al. Human and animal dirofilariasis: the emergence of a zoonotic mosaic. Clin Microbiol Rev. 2012;25(3):507–44.

    Article  PubMed  PubMed Central  Google Scholar 

  88. Mowlavi GH, Masoud J, Mobedi I. Hydatidosis and testicular filariasis (D. Evansi) in camel (Camelous dromedaries) in central parts of Iran. Iran J Public Health. 1997;26(1–2):21–8.

    Google Scholar 

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Acknowledgments

Not Applicable.

Funding

Open access funding provided by The Science, Technology & Innovation Funding Authority (STDF) in cooperation with The Egyptian Knowledge Bank (EKB). The study did not receive any external funds.

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Authors and Affiliations

  1. Division of Internal Medicine, Department of Animal Medicine, Faculty of Veterinary Medicine, Assiut University, Assiut, 71526, Egypt

    Arafat Khalphallah

  2. Faculty of Veterinary Medicine, Omar Al-Mukhtar University, Al-bayda, 919, Libya

    Taher Al-Daek

  3. Department of Parasitology, Faculty of Veterinary Medicine, Aswan University, Aswan, 81528, Egypt

    Mahmoud Abdelhamid

  4. Veterinary Teaching Hospital, Faculty of Veterinary Medicine, Assiut University, Assiut, 71526, Egypt

    Enas Elmeligy

  5. Department of clinical studies, Collage of Veterinary Medicine, King Faisal University, Al-Ahsa, Saudi Arabia

    Sayed Fathi El-Hawari

  6. Department of Animal Diseases, Faculty of Veterinary Medicine, Aleppo University, Aleppo, Syria

    Khaled A. Khesruf

  7. Division of Clinical Laboratory Diagnosis, Department of Animal Medicine, Faculty of Veterinary Medicine, Assiut University, Assiut, 71526, Egypt

    Heba A. Nasr

  8. Department of Theriogenology, Obstetrics, and Artificial Insemination, Faculty of Veterinary Medicine, Aswan University, Aswan, 81528, Egypt

    Ragab H. Mohamed

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  1. Arafat Khalphallah
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  2. Taher Al-Daek
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  4. Enas Elmeligy
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  5. Sayed Fathi El-Hawari
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  6. Khaled A. Khesruf
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  8. Ragab H. Mohamed
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Contributions

All authors prepared the conception and design of the study. A.K., S.F.E., K.A.K., T.A., and R.H.M. conducted the field study and camel examination. A.K., H.A.N., E.E. and M.A. collected laboratory samples and conducted laboratory analyses. R.H.M., H.A.N., E.E., and A.K. manipulated and statistically analyzed the data. K.A.K., T.A., M.A., and S.F.E. performed analysis, data curation, and interpretation of data. A.K., H.A.N., E.E., K.A.K., and M.A. drafted the manuscript. E.E., T.A., S.F.E., R.H.M., and A.K. carried out final writing, critical review, and revision. All authors have read and approved the final manuscript.

Corresponding author

Correspondence to Arafat Khalphallah.

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Ethics approval and consent to participate

The current study was conducted in accordance with ARRIVE guidelines (https://arriveguidelines.org) and approved by the ethical committee of the Faculty of Veterinary Medicine, Assiut University, Egypt, licensed number 06/2023/0143 whereas the study is in accordance with the Egyptian bylaws and OIE animal welfare standards for animal care and use in research and education. The investigated male camels were taken kindly from the farm by obtaining informed consent from the owner.

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The authors declare that they have no competing interests.

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Khalphallah, A., Al-Daek, T., Abdelhamid, M. et al. Camel filariasis (Dipetalonema evansi) and its association with clinical balanoposthitis with reference to prominent changes in clinical findings, serum testosterone, semen analysis, and testicular histopathology. BMC Vet Res 20, 1 (2024). https://doi.org/10.1186/s12917-023-03844-5

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Keywords

BMC Veterinary Research

ISSN: 1746-6148

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