Introduction
Camelids, particularly the one-humped dromedary camels (Camelus dromedarius), play a vital role in the socio-economic status of numerous arid and semi-arid regions across the globe [1]. These resilient animals serve as indispensable assets for communities, providing transportation, meat, milk, and other essential products [2]. Despite the economic and cultural significance of one-humped dromedary camels [3], there is a scarcity of research that examined erythrocyte osmotic fragility (EOF) and oxidative stress biomarkers in relation to symptomatic and asymptomatic conditions. The existing literature predominantly focuses on traditional hematological parameters in camel health assessments [4,5], thus leaving a void in our knowledge regarding erythrocyte health and oxidative stress responses.
EOF and oxidative stress biomarkers are crucial indicators of cellular health, and they play a pivotal role in assessing the physiological well-being of animals [6–8]. EOF assesses the ability of erythrocytes to withstand changes in osmotic pressure, thus, reflecting their structural integrity and resilience. The osmotic fragility test involves exposing red blood cells to varying concentrations of saline solutions and determining the extent to which they swell or shrink. This process helps to evaluate the ability of the cell to regulate water intake and maintain its structural integrity under different conditions [9,10].
Oxidative stress biomarkers are indicators that provide insights into the balance between the production of reactive oxygen species (ROS) and the antioxidant defense mechanisms within an organism. The oxidative stress biomarkers encompass a range of molecules and enzymes, which include malondialdehyde (MDA), glutathione (GSH), superoxide dismutase (SOD), and catalase [8].
One-humped dromedary camels, being resilient inhabitants of arid regions, face inherent risks associated with environmental stressors and infectious diseases [11] that can potentially lead to alterations in EOF and oxidative stress biomarkers. Therefore, the objectives of this research were to examine the alterations in EOF, and assess oxidative stress biomarkers in symptomatic and asymptomatic dromedary camels. By addressing these, the research seeks to deepen our understanding of one-humped dromedary camel physiology, with the goal of refining and tailoring approaches to address their unique health challenges.
Materials and Methods
Location of sampling
The sampling of camels in this study was carried out at the Mai’adua international border market, Mai’adua Local Government Area, Katsina State. Mai’adua Local Government Area, Katsina state, Nigeria. Mai’adua town comprises one of the 10 districts under the Daura Emirate of Katsina state. Katsina State lies on the following coordinates, latitude 13°10’N to 22°134ʹN and longitude 8°13ʹE to 43°716’E. The State is bordered by Zamfara State to the West, and Kaduna State to the South, and Jigawa and Kano States to the East. Livestock such as cattle, sheep, goats, donkeys, horses, and camels are abundant. There is extensive cross-border movement of camels from neighboring African countries into the State.
Animals sampled
A total of 30 dromedary camels, aged between 1 and 10 years, were sampled in this study. These camels originated from different locations including parts of Northern Nigeria, and other neighboring African countries.
Study design and sampling technique
A cross-sectional study design was used. Also, a simple random sampling technique based on convenience was adopted.
Grouping of camels
The 30 camels were randomly assigned into two groups, i.e., symptomatic (10) and asymptomatic (20). This grouping was based on observed clinical signs such as diarrhea, poor body condition, tick infestation, cutaneous lesions (symptomatic), and the absence of these signs (asymptomatic). The consent of the camel owners was obtained.
Collection of blood
After the restraint of each camel in a crouching position, 5 ml of blood was collected via jugular venipuncture and divided into two parts. One part was poured into a labeled vacutainer containing ethylenediaminetetraacetic acid, and processed for EOF determination. The other part was poured into a labeled plain tube and allowed to clot. The serum was harvested and analyzed for oxidative stress biomarkers.
Determination of EOF
EOF was determined using the modified method described by Adenkola et al. [12] and involved the use of varying concentrations (0.0%, 0.1%, 0.3%, 0.5%, 0.7%, and 0.9%) of sodium chloride (NaCl) solution.
Determination of catalase activity
Catalase (CAT) activity was measured based on the decomposition rate of hydrogen peroxide by catalase [13].
Determination of superoxide dismutase activity
SOD was measured based on superoxide generation by xanthine oxidase, superoxide-dependent reduction of cytochrome c or nitro blue tetrazolium, and dose-dependent inhibition by SOD [14].
Determination of glutathione peroxidase activity
The serum activity of glutathione peroxidase activity (GPx) was carried out using the modified Ellman’s method of Rajagopalan et al. [15].
Determination of malondialdehyde concentration
The serum MDA concentration was determined using thiobarbituric acid reactive substance and the double heating method as modified by Yavuz et al. [16].
Results
Erythrocyte osmotic fragility
The EOF result showed slightly less resistance of erythrocytes to hemolysis in the symptomatic than in the asymptomatic camels. At 0.3% NaCl concentration, there was a significantly higher (p < 0.05) rate of hemolysis in the symptomatic camels compared to the asymptomatic camels (Fig. 1).
Figure 1.
Mean ± SD erythrocyte osmotic fragility of asymptomatic and symptomatic camels. Values with different alphabets at the same concentration differs significantly at p < 0.05.
Biomarkers of oxidative stress
The mean serum GPx activity was non-significantly (p > 0.05) lower in symptomatic camels than in asymptomatic camels (Fig. 2).
Figure 2.
Mean ± SD activities of glutathione peroxidase, catalase, and superoxide dismutase of asymptomatic and symptomatic camels. Values with different alphabets for the same enzyme differs significantly at p < 0.05.
The mean serum CAT activity in the symptomatic camels was significantly (p < 0.05) lower compared to the values obtained in the asymptomatic group (Fig. 2).
The mean SOD activity in the symptomatic camels (10.13 ± 1.61 U/ml) was non-significantly (p > 0.05) higher than that of the asymptomatic camels (Fig. 2).
The mean serum MDA concentration in the symptomatic group was non-significantly (p > 0.05) higher compared to the level in the asymptomatic group (Fig. 3).
Figure 3.
Mean ± SD malondialdehyde concentration of asymptomatic and symptomatic camels.
Discussion
The EOF result from this study suggests that the erythrocytes of symptomatic camels are less resistant to hemolysis compared to asymptomatic camels, particularly at 0.3% NaCl concentration. This raises intriguing questions regarding the potential implications for the health status of these animals. The findings indicate that the erythrocytes of the symptomatic camels were more prone to hemolysis at lower salt concentrations, and this could be indicative of underlying health conditions affecting the EOF. This difference in osmotic fragility may be associated with the health status of the camel health. One possible explanation for these findings could be an underlying imbalance in the osmotic stability of erythrocytes in symptomatic camels, potentially linked to variations in membrane composition or structural integrity [17,18]. The increased susceptibility to hemolysis may be indicative of compromised erythrocyte function, a response to pathological conditions affecting the cellular membrane, or systemic changes [19].
The non-significant decrease in serum GPx activity in symptomatic camels in this study suggests a potential trend towards reduced antioxidant capacity in these animals. GSH peroxidase plays a crucial role in scavenging ROS [20], and even a non-significant decrease may indicate a compromise in the antioxidant defense system, contributing to oxidative stress. A study in camels infested with gastrointestinal parasites, revealed a reduction in GPx activity, thus, suggesting a link between parasitic infestation and decreased antioxidant activity [21].
The significantly lower CAT activity in the serum of symptomatic camels is a noteworthy finding. Catalase is a key enzyme that catalyzes the decomposition of hydrogen peroxide, and its reduced activity in symptomatic camels implies a diminished ability to neutralize this ROS [22]. This result suggests a compromised capacity to counteract oxidative stress in symptomatic camels, potentially contributing to cellular damage and oxidative injury. Research on camels has shown that a decrease in CAT activity is associated with various health conditions and oxidative stress. For instance, a study on camels with hydatid cysts infection found that the levels of catalase were significantly decreased, indicating an imbalance between oxidants and antioxidants [23].
The non-significant increase in SOD activity in symptomatic camels suggests a potential adaptive response to counteract elevated oxidative stress. SOD is a crucial antioxidant enzyme involved in the scavenging of superoxide radicals [24]. The observed trend towards higher activity may represent an effort to cope with increased oxidative challenges in symptomatic camels.
The significantly higher MDA concentration in the symptomatic group compared to the asymptomatic group suggests a higher level of oxidative damage to lipids in the former. This finding is consistent with the broader understanding that oxidative stress is linked to various diseases and physiological disturbances in animals [25], including camels. MDA is a byproduct of lipid peroxidation, and its elevated levels in symptomatic camels support the presence of oxidative stress-induced cellular injury in these animals [26]. The observed increase in MDA levels in the symptomatic camels is indicative of an imbalance between oxidants and antioxidants, leading to oxidative damage. This imbalance can have detrimental effects on physiological processes and overall health, as evidenced by the association of MDA elevation with conditions such as endometritis and hydatid cysts in camels [23,27]. In addition, the decrease in antioxidant enzyme activities, such as catalase, in symptomatic camels further supports the notion of compromised antioxidant defense and increased oxidative stress [23] in this study.
The outcomes of this study may suggest that erythrocyte fragility, CAT activity, and MDA concentration could serve as potential biomarkers for assessing the health status of dromedary camels. However, it is essential to consider potential confounding factors that might influence EOF, such as nutritional status, environmental conditions, or concurrent diseases.
Conclusion
The findings of this study highlight a marked relationship between the symptomatic state in one-humped dromedary camels and elevated hemolysis rates at 0.3% NaCl concentration, as well as reduced CAT activity. However, there were no significant differences in the activities of Gpx and SOD, and MDA, between the symptomatic and asymptomatic camels. These results contribute valuable insights into the physiological variations associated with the health of camels, and provide a basis for further research involving the mechanisms associated with oxidative stress and antioxidant defense in camels under different health conditions.
