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Effects of Toxocara canis Infection and Albendazole Treatment on Oxidative/Nitrosative Stress and Trace Element Status in Dogs

Priyanka S. Dey
Vol 8(4), 144-153
DOI- http://dx.doi.org/10.5455/ijlr.20170720111145

The present study was conducted with the objectives of studying the oxidative/nitrosative and trace element alterations in naturally Toxocara canis infected dogs before and after treatment with albendazole and to explore the effect of albendazole treatment on oxidative/nitrosative status in healthy dogs. Six naturally infected dogs with T.canis were selected for the present study. These cases were treated with albendazole @ 25 mg/kg orally for 3 consecutive days and monitored weekly up to 28 days of post treatment. Six apparently healthy dogs acted as healthy control and were also treated with albendazole @ 25 mg/kg orally. A highly significant increase in NO (p< 0.01) and LPO (p<0.01); highly significant decrease in GSH (p< 0.01), SOD (p<0.01) and CAT (p< 0.01) and altered liver function were recorded in T. canis infected dogs as compared to healthy control. After treatment with albendazole significant (P<0.01) restoration of haematobiochemical alterations, the oxidant /antioxidant disturbances and plasma nitrate within 7 days of post treatment and non significant improvement in the values of plasma Zn and Co were observed. In healthy dogs no alterations in the oxidative and nitrosative stress parameters were noticed before and after treatment with albendazole. From the present study it was concluded that T.canis induces oxidative/nitrosative stress in dogs. Besides clearing the worm burden, treatment with albendazole can restore the disturbance of oxidative and nitrosative indices in T canis infected dogs. Albendazole treatment will not alter any oxidative/nitrosative status in healthy dogs.


Keywords : Albendazole Dog Oxidative/Nitrosative Stress Toxocara canis Trace Elements

Ascariasis is one of the frequently recorded parasitic diseases of animal and humans in tropical countries like India. It has been reported that 55 to 82 % of pups in India suffers due to ascariasis (Mapplestone and Bhaduri, 1940). Dogs may be infected via the placenta or through the dam’s milk or by ingesting T. canis eggs or paratenic hosts containing larvae. Human beings gets infection by ingestion of embryonated Toxocara eggs through food or soil or by penetration of larva through skin. The disease in dogs is characterized by diarrhea, abdominal discomfort, stunted growth, pot-bellied appearance, pneumonia and presence of worms in feces and vomitus. In severe cases, puppies may die from obstruction of the gall bladder, bile duct or pancreatic duct, or rupture of intestine leading to peritonitis (Soulsby, 2006). Pathogenic impact of T. canis on the host is due to larval migration and/or the adult forms in the intestines. Besides intake of nutrient, mechanical hindrance of intestinal function, the secretary/excretory products of the parasite are harmful to the host’s tissues. Presence of T. canis and its developing larvae cause disturbances in animals’ health, quite frequently inducing anaemia, vomiting, diarrhea, weakness and even death in young pups (Soulsby, 2006). The exact mechanism by which T. canis causes deaths among animals is not fully understood.

Reactive oxygen species (ROS) and reactive nitrogen species (RNS) are produced as normal products of cellular metabolism. In biological systems, they can have both beneficial and detrimental effects (Valko et al., 2007). Some recent studies have suggested the role of oxidative stress as an important factor in the pathogenesis of intestinal parasitic infection in human beings (Chandramathi et al., 2009). Oxidative stress occurs in biological systems due to the excessive production of ROS/RNS and/or because of the impotence of the enzyme and non enzyme systems i.e. antioxidants, to eliminate those (Valko et al., 2007). Parasites can stimulate excessive production of ROS/RNS and provoke the occurrence of oxidative stress. It is also recently reported that certain drugs can be very harmful for the delicate oxidant-antioxidant equilibrium, provoking oxidative stress during their biotransformation (Dimitrijevi´c et al., 2012). Albendazole (ABZ) is a broad spectrum anthelmintic drug, frequently used in India for therapy of gastrointestinal nematode infection in dogs. Trace elements have a number of structural, catalytic and regulatory functions in the organism and they also play a major role in the immune system. Few studies have explored the relationship between the common GI nematode infections and trace elements (van der Hulst et al., 1998). But, few authors (Koski et al., 2003) opine that still much work has to be done to study the role of trace elements in gastrointestinal nematode infection. Some anthelmintic drugs even in therapeutic dosages can induce oxidative stress in animals during their biotransformation (Dimitrijevi´c et al., 2012). Benzimidazole is the most frequently used drug in therapy of T. canis infections especially ABZ, as it also affects the larvae of this parasite. Albendazol interacts with the eukaryotic cytoskeleton protein, tubulin, by inhibiting its polymerization into microtubules. It has been reported that some anthelmintics can also achieve an antiparasitic effect by interfering with parasites’ metabolic processes, resulting in increased ROS and RNS production (Valko et al., 2007). Toxicological research has confirmed that ABZ and other derivates of benzimidazole can bring an organism into a state of oxidative stress (Pedrosa et al., 2001). The increased exposure to ROS/RNS leads to cellular oxidative stress and consequently damages biomacromolecules, leading to controlled (apoptosis) and uncontrolled cell death (necrosis).

As much as there is no report on the oxidative/nitrosative stress status during ascariasis in dogs. Therefore the present study was undertaken to study the oxidative/nitrosative and trace element alterations in naturally Toxocara canis infected dogs before and after treatment with albendazole and to explore the impact of albendazole treatment on oxidative/nitrosative status in healthy dogs.

Materials and Methods                                 

Study Area

This study was conducted at Referral Veterinary Polyclinic section of Indian Veterinary Research Institute, Izatnagar during June 2014 to June 2015.

Animals

Dogs presented to the Referral Veterinary Polyclinic for treatment with  the clinical signs of diarrhea, anaemia, vomiting, emaciation and pot-bellied appearance were screened using coprological technique for detection of Toxocara eggs and confirmed to be infected with Toxocara canis (Soulsby, 2006). Dogs having severe infection (EPG ≥2500) of T. canis were selected for this study. These dogs were treated with albendazole @25mg/kg, PO, consecutively for three days and monitored weekly up to 28 days post treatment. Another six apparently healthy animals were selected to study the effect of albendazole treatment on Oxidative/Nitrosative status of host. These dogs were administered with albendazole @25mg/kg, PO and blood samples were collected prior to treatment, and 24 and 72 hours after the treatment.

Faecal Examination

Faecal samples were collected directly from rectum and examined within one hour of collection using both direct smear and flotation techniques on ‘0” day (before treatment), 7th and 28th day of post treatment according to the standard procedure (Soulsby, 2006).

Blood Collection and Processing

Sampling of Blood

Blood samples (5.0 ml) were collected on days 0, 7, 14, 21 and 28 of post treatment by venipuncture from the cephalic and/or radial vein using a disposable syringe after taking consent of the owners. For haematological examination, 1.0 ml of blood was transferred into tubes containing ethylene diamine tetra acetic acid (EDTA) as anticoagulant. For estimation of oxidative stress indices, nitric oxide and biochemical parameters remaining 4.0 ml of blood was transferred into tubes containing heparin as anticoagulant.

Determination of Oxidative Stress Indices                    

Preparation Erythrocyte Haemolysate, RBC Suspension and Separation of Plasma

The blood samples (4 ml) were centrifuged at 3,000 rpm for 15 min in refrigerated condition to obtain plasma. After collecting plasma in eppendorf tubes, the packed erythrocytes were washed three times with phosphate buffer saline solution (PBS, pH 7.4). Washed erythrocytes were mixed with chilled distilled water and shaken vigorously to prepare 10% haemolysate. Another 500 ml of washed erythrocytes were mixed with 500 ml of phosphate buffer saline solution to prepare RBC suspension for estimation of reduced glutathione. Haemoglobin concentration in the 10% haemolysate and RBC suspension were estimated by cyanomethaemoglobin method as given by Vankampen and Zinglstra, (1961).

Measurement of Oxidative Stress Indices

Erythrocytic LPO was estimated as per the method given by Placer et al. (1996). The concentration of malonaldehyde in nanomoles per millilitre of erythrocyte hemolysate was derived using 1.56×105/mol/cm as extinction coefficient (Utley et al. 1967). The GSH level in erythrocytic hemolysate was determined according to the standard method (Prins and Loos, 1969). The superoxide dismutase (SOD) activity was determined by the method of Menami and Yoshikawa (1979) which is a modification of the method given by Marklund and Marklund (1974). Each unit of SOD activity is defined as the quantity of enzyme that inhibited autooxidation of pyrogallol by 50% under suitable experimental conditions. Activity was expressed as units/mg Hb/ml. The activity of catalase (CAT) was determined from RBC hemolysate as described by Cohen et al. (1970). Decomposition of H2O2 was followed directly by the decrease in absorbance per min/mg Hb and it was taken as a measure of the CAT activity. Nitric oxide level of blood plasma was measured by nitrate reduction on copper– cadmium alloy (Cu–Cd alloy) followed by colour development with Griess reagent (0.1% naphthalene diamine dihydrochloride in 3N hydrochloric acid and 1% sulphanilamide, 1:1) as per the method described earlier (Sastry et al., 2002).

Estimation of hemato-Biochemical Parameters

For haematology, blood was used to determine haemoglobin (Hb %), packed cell volume (PCV %), total erythrocyte count (TEC), total leukocyte count (TLC), differential leucocyte count (DLC), absolute neutrophil count (ANC) and absolute eosinophil count as per standard protocol (Jain, 1986). Standard procedures were employed to determine the levels of total protein and albumin, globulin, albumin: globulin ratio, urea nitrogen and Creatinine. The values of serum globulin were measured as the difference between total protein and albumin and from this albumin: globulin ratio was calculated.

Analysis of Blood Micro Minerals

Whole blood samples were wet digested using double acid mixture i.e. nitric acid: perchloric =5:1 (AOAC1984). Concentration of Cu, Co, Fe and Zn in acid digest were estimated using atomic absorption spectrometer (Electronic corporation of India Model no AAS 4141). Air acetylene 8:2 was used as combustion gas. Quality control criteria of analysis were maintained by analysis of reference standards from Sigma aldrich, USA

Statistical Analysis

Data obtained was subjected to stastical analysis as per the standard method (Snedecor and Cochran, 1994). One-way analysis of variance was done with the help of SPSS software 16th version to analyze the data.

Results     

  1. canis infected dogs showed characteristic clinical signs such as anorexia, diarrhea, poor body condition and pot-bellied appearance, presence of T. canis eggs in stool, vomiting, nasal discharge, pale mucous membrane and rough hair coat. Treatment with albendazole remits signs of diarrhea, vomiting and anorexia within 7 days of treatment. Stool samples of all 6 dogs were negative to T. canis eggs on day 7 post treatment. The mean values of different parameters of hemato-biochemical profile, oxidative stress indices and trace elements are presented in Tables 1 to 4.

Table 1: Haematological and serum biochemical parameters (mean±SE) in Toxocara canis infected and healthy control dogs

Parameters Control (n=6) Infected (n=6)
Hb (g/dL) 12.08±0.17b 8.90±0.18a
PCV (%) 36.25±0.53b 24.94±0.58a
TEC (x106/μL) 5.77±0.07ab 4.18±0.16a
TLC (x103/μL) 8.51±1.67b 12.33±3.36a
ANC (x103/μL) 5.55±0.01a 6.70±0.02ab
AEC (x103/μL ) 0.13±0.09a 0.75±0.01c
Total Protein (g/dl) 6.45±0.12c 4.05±0.20a
Albumin (g/dl) 2.83±0.04b 1.30±0.09a
Globulin (g/dl) 3.61±0.11b 2.74±0.15a
A:G Ratio 0.78±0.02b 0.48±0.04a

Means bearing different superscript differ significantly (p<0.05)

In haematology, there were significant (p<0.05) reductions in Hb, PCV and TEC in T. canis infected dogs as compared to healthy control. After treatment with albendazole continuous increasing (p<0.01) trend in levels of RBC, PCV was noticed from 7th day of post treatment but there were no significant changes in the values of TLC and ANC (Table 3). Highly significant (p<0.01) improvement in the values of TP, albumin and A: G ratio, and markers of liver function were recorded from 7th day of post treatment (Table 3). In oxidative stress indices, significant (p<0.01) increase in values of LPO and NO and decrease (p<0.01) in antioxidant enzyme GSH, SOD and CAT were recorded in T.canis  infected dogs as compared to healthy control (Table 2). No significant changes in the values of Fe, Cu, Co and Zn were noticed between T canis infected and healthy dogs (Table 2).

Table 2: Oxidative, nitrosative and trace element status (mean±SE) in Toxocara canis infected and healthy control dogs

Parameters Control (n=6) Infected (n=6)
LPO(nmol MDA/ml/mg Hb) 2.37 ± 0.48a 4.41 ± 0.62b
GSH(μmol/ml) 0.29 ± 0.11a 0.17 ± 0.04a
SOD (U/mg Hb) 2.48 ± 0.10b 1.10 ± 0.07a
CAT (U/mg Hb) 4.35 ± 0.12b 1.28 ± 0.12a
NO(μmol/l) 4.65 ± 0.33a 29.64 ± 5.32b
Cu (μg/g) 0.64 ± 0.03a 0.89 ± 0.19a
Co (μg/g) 0.29 ± 0.12a 0.13 ± 0.05a
Zn (μg/g) 3.80 ± 0.09a 2.7 ± 0.67a
Fe(μg/g) 116.40 ± 4.70a 105.80 ± 12.9a

Means bearing different superscript differ significantly (p<0.01)

Table 3: Effect of albendazole treatment on haematobiochemical values (mean±SE) in T.canis infected dogs

Parameters Before treatment 1st week post treatment 2nd week post treatment 3rd week post treatment 4th week post treatment
Hb (g/dl) 8.90±0.18a 11.53±0.45b 12.08±0.23b 12.22±0.23b 12.19±0.09b
PCV (%) 24.94±0.58a 34.61±1.35b 35.26±0.69b 37.67±0.81b 35.59a±0.28b
TEC (106/mm3) 4.18±0.16a 5.90±0.22b 6.04±0.11b 6.11±0.13b 6.09±0.04b
TLC (/Cmm) 12325±336a 12336±167a 12553±28a 12533±405a 12506±298a
ANC (/Cmm) 6697±227ab 6846±110ab 7157±220b 7146±272b 7169±149b
AEC (/Cmm) 753±12c 596±15b 533±15b 457±21b 428±8b
BUN (mg/dl) 7.04±0.31a 7.04±0.29a 7.21±0.58ab 8.81±0.44b 8.99±0.43b
Creatinine (mg/dl) 0.46±0.09a 0.62±0.06a 0.62±0.13a 0.75±0.20a 0.74±0.26a
ALT (U/L) 117±2.61 b 102±3.86 b 97±8.50 b 77±4.50 a 84±8.82 ab
ALP (U/L) 182±7.70 b 142±5.20 ab 109±6.96 ab 108±6.76 ab 117±2.90 ab
TP (g/dl) 4.05±0.20a 4.96±0.25ab 5.48±0.18bc 5.68±0.16bc 6.01±0.09c
Albumin (g/dl) 1.30±0.09a 2.23±0.17b 2.66±0.11b 2.80±0.19b 3.04±0.21b
Globulin (g/dl) 2.74±0.15a 2.72±0.13a 2.82±0.17a 2.88±0.18a 2.97±0.03a
A:G Ratio 0.48±0.04a 0.82±0.04b 0.95±0.05b 0.98±0.10b 1.02±0.03b
Total Bilirubin (mg/dL) 0.76±0.02 a 0.64±0.01 a 0.68±0.01 a 0.66±0.01 a 0.67±0.06 a
Direct Bilirubin (mg/dL) 0.53±0.03 b 0.39±0.02 a 0.45±0.02 a 0.36±0.01 a 0.46±0.04 a
Indirect Bilirubin (mg/dL) 0.23±0.02 a 0.25±0.02 a 0.23±0.02 a 0.30±0.02 a 0.21±0.02 a
Glucose (mg/dL) 79.66±0.66 a 76.33±1.11 a 77.93±0.63a 77.43±0.90a 77.66±0.33a
CKMB(IU/L) 44.23±0.66 a 41.66±0.71 a 43.10±0.55a 40.60±0.40a 40.30±1.45a

Mean values bearing the different superscript in the row differ significantly (P < 0.01)

Mean values bearing the same superscript in the row do not differ significantly (P > 0.05)

Treatment with albendazole significantly restored (P<0.01) hematobiochemical alterations, the oxidant /antioxidant disturbances and plasma nitrate within 7 days post treatment (Table 4). No significant effect on trace elements before and after treatment except non significant improvement in the values of plasma Zn and Co was observed (Table 4). In healthy dogs significant difference was not observed in any of oxidative and nitrosative stress parameters before and after treatment with albendazole (Table 5).

Table 4: Effect of albendazole treatment on oxidative, nitrosative and trace element status (mean±SE) in T. canis infected dogs

Parameters Before treatment 1st week post treatment 2nd week post treatment 3rd week post treatment 4th week post treatment
LPO  (nmol MDA/ml/mgHb) 4.41±0.62b 2.86±0.21ab 2.45±0.31ab 2.06±0.27a 1.84±0.02 a
GSH (µmol/ml) 0.17±0.04a 0.20±0.01a 0.23±0.04a 0.63±0.23b 0.91±0.16b
SOD  (U/mg Hb) 1.10±0.07a 1.98±0.04b 1.85±0.07b 1.91±0.14b 1.89±0.12b
CAT (U/mg Hb) 1.28±0.12a 3.92±0.15b 3.99±0.25b 4.01±0.03b 4.06±0.03b
NO (µmol/l) 29.64±5.32b 12.33±0.59a 12.89±1.96a 13.88±0.55ab 13.67±1.28ab
Cu (μg/g) 0.89±0.19a 0.72±0.17a 0.66±0.01a 0.75±0.13a 0.65±0.19a
Co  (μg/g) 0.13±0.05a 0.31±0.04a 0.28±0.10a 0.25±0.12a 0.27±0.13a
Zn  (μg/g) 2.7±0.67a 4.5±0.81a 4.2±0.44a 4.38±0.08a 3.60±0.95a
Fe  (μg/g) 16.5±2.06a 20.4±0.37ab 21.33±1.20ab 21.60±0.94ab 22.33±0.88b

Mean values bearing the different superscript in the row differ significantly (P < 0.01)

Mean values bearing the same superscript in the row do not differ significantly (P > 0.05)

Table 5: Effect of Albendazole treatment on oxidative and nitrosative status in healthy dogs

Parameters Before Albendazole treatment 24 hrs after Albendazole treatment 72 hrs after Albendazole treatment
LPO (nmol MDA/ml/mg Hb) 2.37 ± 0.48a 3.27 ± 0.05a 3.18 ± 0.42a
GSH (µmol/ml) 0.29 ± 0.11a 0.10 ± 0.01a 0.09 ± 0.01a
SOD (U/mg Hb) 2.48±0.10a 2.28±0.08a 2.14±0.09a
CAT (U/mg Hb) 4.35±0.12a 4.23±0.08a 4.19±0.05a
NO (µmol/l) 4.65 ± 0.33a 8.87 ± 3.65a 6.53 ± 0.56a

Mean values bearing the same superscript in the row do not differ significantly (P > 0.05)

Discussion

This is the first report documenting involvement of oxidative and nitrosative stress in T. canis infected dogs as well as its status during treatment with albendazole. In present study, T. canis infected dogs had severe anaemia as evidenced with low values of Hb, PCV and TEC. Hayat et al. (1999) reported anaemia in buffalo calves infected with T. vitolorum and he opined that toxins liberated by ascarids worms may cause bone marrow suppression. Although the ascarid worms do not suck blood from the host, anaemia present might be due to the presence of worms in the intestine, which interferes with the absorption of nutrients and thereby the formation of erythrocyte precursors (Koski and Scott, 2003). Proteinases released by GI nematodes especially ascarids during invasion of host tissues will hydrolyse haemoglobin, which may also contribute for the development of anaemia in ascariasis (Hayat et al., 1999). Post treatment improvement in the haematocrit values in T. canis infected dogs reflects the efficacy of albendazole in reducing the pathological effects besides reduction of worm burden. There were no significant differences in the values of TLC and ANC before and after treatment. This is in accordance with the findings of earlier workers (Yarsan et al., 2003). Highly significant increase in the value of AEC in T. canis infected dogs on day ‘0’ might indicate the allergic reaction induced by host due to the migration of T. canis larva in host tissues (Yarsan et al., 2003). Antigens released by GI nematodes will initiate the cascade of immune reaction with the release of Th2 cytokines, including interleukin IL-4, IL-5, IL-9, IL-10, and IL-13. Among these cytokines IL-5 plays an important role in the development of eosinophilia (Koski and Scott, 2003). Highly significant decrease in the values of AEC after treatment with albendazole is in agreement with the findings of many workers (Koski and Scott, 2003 and Yarsan et al., 2003). Highly significant improvement in the values of BUN on 14th, 21st and 28th day of post treatment might reflect the improvement in body condition of the dogs after treatment. Although creatinine was found to increase after the institution of treatment but the difference was not significant. This may also be due to the increase in muscle mass after treatment.

Hypoproteinemia, hypoalbuminemia and low A: G ratio in T.canis infected dogs might be due to the poor absorption of nutrients from gastrointestinal tract. Ascarid worms present in gastrointestinal tract will cause intestinal pathology and thereby interferes with the absorption of nutrients (Koski and Scott, 2003). Pathological effect induced by the migration of T. canis larva in liver might also contribute to the occurrence of hypoproteinemia and hypoalbuminemia (Yarsan et al., 2003). Highly significant increase in the values of TP, albumin and A: G ratio after treatment agrees with Brown et al. (1980), who opined that deworming enhances nutrient absorption of the macronutrients. The reactive oxygen and nitrogen species play a complex role in many diseases and in metabolic regulations in a diseases process and oxidative stress has been implicated in several parasitic diseases of man and animal (Chandramathi et al., 2009). Parasite -induced oxidative stress could be mediated by liberation of proinflammatory cytokines. In the present study increased LPO levels in T. canis infected dogs indicates increased level of lipid peroxidation in erythrocytes of affected animals, which in turn reflects elevated oxidative stress in these animals. Involvement of oxidative stress in ascariasis has been documented in human beings (Chandramathi et al., 2009). Helminth parasites secrete enzymes that generate free radicals such as superoxide and other intermediate products of free radical activity such as hydrogen peroxide in mammalian tissues (Dimitrijevi´c et al., 2012).

Alteration in antioxidant enzyme levels have been reported in many disease processes as a consequence of enhanced ROS production either by up-regulation of the enzyme activity or utilization of the antioxidant enzyme to counter the ROS. In the present study utilization of SOD, CAT and GSH was observed in T. canis infected dogs leading to the exhaustion of the host SOD, CAT and GSH in neutralizing the free radicals produced by the parasites. After processing of parasitic antigens activated phagocytic cells generate large amounts of highly toxic molecules, NO and many cytokines. NO or its stable metabolites have been identified as major effector molecules during the majority of parasitic infections (Nahrevanian, 2009). In this study elevated NO levels before treatment supported the observations of earlier workers (Nahrevanian, 2009 and Demirci et al., 2006). We also found reduction in oxidative and nitrosative stress in all albendazole treated dogs within 7 days post treatment. This suggests that upon the elimination of worm burden from host, oxidant and antioxidant equilibrium is attained on its own. This supports the findings of Daoud et al. (2000), as they found that exogenous administration of antioxidants in order to minimize free radical damage to the intestine resulted in prolongation of parasite survival and reduction in efficacy of anthelmintics.  Destruction of intestinal absorptive surface by helminths impairs absorption of macro and micronutrients (Koski and Scott, 2003). This may be the reason for low values of Zn and Co in T. canis infected dogs and these findings are in agreement with the findings of earlier report (Rahman et al., 2002). In healthy dogs significant difference was not observed in oxidative and nitrosative stress parameters before and after treatment with albendazole. This may suggest that oxidative damage caused by Benzimidazoles will not affect host. Pedrosa and co-workers, 2001 suggested that Benzimidazole group of anthelmintics exert their anthelmintic efficacy by inducing oxidative stress in parasites. From this study it can be concluded that treatment with albendazole will not elicit any oxidative / nitrosative stress in host.

Conclusion

From our study it can be concluded that besides causing haematobiochemical alterations and interfering with micronutrient absorption, T. canis infestation induces oxidative and nitrosative stress in dogs. This may contribute somewhere in the pathogenesis of T.canis infestation. Treatment with albendazole does not elicit oxidative / nitrosative stress in dogs. Albendazole effectively clears worm burden, restores oxidative/nitrosative imbalance and improves micromineral absorption in T. canis infested dogs.

Acknowledgements

The authors are thankful to the Director, Indian Veterinary Research Institute, Bareilly for providing facilities to conduct the research work.

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