Prevalence of Gastrointestinal Nematodes of Dogs and Associated Hematological Changes in Gombe State, Nigeria

doi:10.21203/rs.3.rs-4852349/v1

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Prevalence of Gastrointestinal Nematodes of Dogs and Associated Hematological Changes in Gombe State, Nigeria

https://doi.org/10.21203/rs.3.rs-4852349/v1

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Gastrointestinal (GI) nematodes are a common parasitic problem in dogs, causing significant health issues. These parasites live in the digestive tract and can lead to a variety of symptoms, depending on the type and severity of infection. A cross sectional study was conducted from August 2023 to December 2023 to determine the prevalence of gastrointestinal nematodes of dogs and their effect on haematological parameters in Gombe State, Nigeria. A total of 200 faecal samples from dogs were collected using systematic random sampling technique from six (two from each Senatorial zone) randomly selected Local Government Areas (LGAs) out of the eleven LGAs in the State. Formalin-ether centrifugation-floatation technique was used to detect nematode parasites using microscopy. Haematological evaluations were performed according to standard procedures. The overall prevalence of gastrointestinal nematodes of dogs in the study area was 36.5%. The parasites identified were Ancylostoma caninum, Toxocara canis and Trichuris vulpis with 58.9%, 28.7% and 12.3% prevalences respectively. The haematological parameters revealed reduction of the Mean Corpuscular Volume (MCV) of both the infected and non-infected dogs below the reference values while only the infected group has Mean Corpuscular Hemoglobin Concentration (MCHC) below the reference values. There were eosinophilia, monocytosis and leukocytosis in the infected group whereas neutrophilia occurred in both the infected and non-infected groups. All other haematological values are within the reference ranges. This study establishes the prevalence of gastrointestinal nematodes of dogs and associated risk factors in Gombe State, Nigeria.

Small Animal Medicine

Dogs

gastrointestinal nematodes

haematology

Gombe State

Gastrointestinal nematodes of dogs are among the most frequent pathogenic agents that veterinarians who treat companion animals encounter. They are also one of the primary causes of dog mortality (Martínez-Moreno et al., 2007). As a result, they pose a risk to the animals, their owners, and veterinarians. Several intestinal parasites in dogs are zoonotic, meaning they have an impact on public health (Moro and Abah, 2019). Although the close bond between humans and dogs and their role as companion animals provide many benefits, they also pose a risk to public health because of the possibility of natural parasitic infection transmission from dogs to humans through unfavourable environmental and behavioral factors (Patz et al., 2002). Certain zoonotic illnesses like ancylostomiasis or cutaneous larva migrans, as well as toxocariasis or visceral larva migrans, are caused by some of these parasitic nematodes (Ugbomoiko et al., 2008). In most tropical and subtropical parts of the world, including Nigeria, canine gastrointestinal nematode infection continues to be a significant cause of hindrance to the health and well-being of dogs (Zelon, 2003; Ramirez-Barrios et al., 2004). These gastrointestinal nematodes have a direct life cycle in which the larvae or eggs are shed in the excrement of infected dogs, hatch in the environment, and then infect other dogs by ingestion or skin penetration. Certain nematodes, such as Toxocara canis, can also spread through lactation or transplacentally (Endrias and others, 2010). Consequently, depending on the amount of infecting larvae as well as host characteristics like breed, age, and acquired resistance, canine helminthosis could range in severity from asymptomatic infection to rapidly lethal disease (Bowman et al., 2003). In dogs, intestinal nematodes can result in acute intestinal blockage, emaciation, anemia, constipation, intermittent diarrhea, and a potbelly appearance (Kumar et al., 2014). Anemia, fatigue, melena, and weight loss are the results of blood loss caused by Ancylostoma caninum. Intestinal blockage, malnourishment, and in extreme situations, the larvae's migration to other organs are caused by Toxocara canis. Bloody diarrhea, colitis, and dehydration are brought on by Trichuris vulpis (Epe, 2009). Dog intestinal nematodes cannot be diagnosed using only symptomatology-based diagnostics, as stated by Carroll and Grove in 1986. By identifying parasitic elements (eggs, larvae, and adults) in their feces, particularly based on the two main diagnostic parameters: size and shape, intestinal nematodes infections in small animals can be detected (Foreyt, 1989). To concentrate parasite materials in fecal samples, a variety of methods and techniques are available, each having pros and cons of their own. The majority of gastrointestinal parasites have been diagnosed by fecal flotation, which is also a highly helpful method for evaluating the majority of parasites that affect dogs (Dryden et al., 2005). This method has the benefit of recovering parasite cysts and eggs based on variations in the flotation solution, faecal debris, and egg specific gravities, which makes identification easier (Sloss et al., 1999). Utilizing several common flotation medium, the centrifugal-flotation process decreases the time for for eggs and cysts to float (Maurelli et al., 2014). Haematological measures are useful for evaluating pathological conditions in animals as well as serving as excellent markers of the physiological state of the animals. Apart from their application in the identification and tracking of illnesses and anomalies, haematological investigations aid medical professionals in the diagnosis of numerous ailments and the evaluation of blood damage (Audu et al., 2022). The current study therefore sought to ascertain the intestinal nematode infection rate in domestic dogs under field conditions as well as the effect of these infections on the health of the animals by evaluating several risk variables and hematological parameters of both infected and non-infected dogs.

STUDY AREA

The study was carried out in Nigeria's northeastern geopolitical zone in Gombe State (Jewel in the Savannah). With Gombe Town serving as its administrative and commercial center, Gombe State was established in 1996 by separating from the former Bauchi State. Situated between latitudes 9°301N and 12°301E and longitudes 8°451 and 11°451E, the State spans 20,265 km². The Northeastern subregion's five other states—Adamawa, Bauchi, Borno, Taraba, and Yobe—share shared borders with the state. The State is divided into 114 Wards and eleven (11) Local Government Areas (LGAs). Akko, Balanga, Billiri, Dukku, Funakaye, Gombe, Kaltungo, Kwami, Nafada, Shongom, and Yamaltu/Deba are the Local Government Areas (Wikipedia, 2006).

SAMPLING PROCEDURE AND STUDY DESIGN

A cross sectional study was conducted from August 2023 to December 2023. Two LGAs from each senatorial zone, or six out of the eleven, were chosen. Targeted locations included homes, dog markets, and both private and public veterinary clinics. To choose the specific dog based on availability and accessibility, systematic random sampling was employed. A clinical examination was conducted. Dogs exhibiting symptoms like fever, diarrhea, vomiting, anorexia, ascites, dehydration, emaciation, and epilation all indicative of helminthosis were classified as sick, whereas those exhibiting no symptoms were considered to be apparently healthy. The canines' demographic characteristics were noted. Based on the average age at initial estrus and the age variation in canine dentition, dogs younger than 7 months were classified as pups, and those older than 7 months were classified as adults (Salvin et al., 2011). The study subjects' external reproductive structures were used to ascertain their sex. Dog breeds were divided into three categories: exotic, cross, and local. The formula of Thrusfield (2005) was used to calculate the sample size, with a 95% confidence interval and 22.4% prevalence rate as reported by Esonu et al. (2019) in Zaria, Nigeria. For accuracy, the originally estimated sample size of 197 was raised to 200. Dogs with and without infections had their hematological profiles taken, and compared with the reference values.

ETHICS APPROVAL AND CONSENT TO PARTICIPATE

All samples were obtained using the usual procedure for sample collection without causing discomfort or injury to the animals. Approval was granted by the University of Maiduguri Research and Ethics committee before the study was carried out. Consent were sought from owners of all the dogs sampled in line with the research ethics before the sample collections.

SAMPLES COLLECTION

Each dog was securely restrained. Using sterile polythene bags, faecal samples were taken once per rectum. Every animal had at least 10g of feces collected, which were then put in a cool flask and brought to the lab for analysis. The cephalic vein was used to collect the blood sample. A volume of approximately 5 milliliters of blood was aseptically drawn and then placed into sample bottles with EDTA added as an anticoagulant. After being labeled and stored in an ice pack box, the blood and faecal samples were brought to the pathology and parasitology labs at the University of Maiduguri for processing.

LABORATORY PROCEDURES

PARASITOLOGICAL EXAMINATION

Macroscopically, every faecal sample was inspected to check for adult nematodes or other endoparasites, as well as for color, blood, mucus, and consistency. Utilizing the Formalin-Ether concentration procedure, microscopic analysis was carried out (Garcia and Bruckner 1988; Sloss et al., 1999; Maurelli et al., 2014). To ensure proper fixation, the fecal sample was carefully mixed with 10 ml (10%) formalin and allowed to stand for 30 minutes. The formalin/stool combination was mixed with physiological saline (0.85%) and passed through two layers of gauze. After adding around 3 milliliters of ethyl ether to the filtrate, it was violently shaken for 30 seconds. The mixture was centrifuged at 2500 rpm for 10 minutes. The sediment was re-suspended in a saturated salt solution with a specific gravity of 1.2 g/mL, and the supernatant that was produced was disposed of. The solution was added more often until a convex meniscus developed. After the universal tube was filled, a coverslip was placed on it and left for roughly five minutes. After that, the coverslip was set on the glass slide and inspected under a microscope for eggs of the nematodes.

HEMATOLOGICAL EXAMINATIONS

Determination of Packed Cell Volume (PCV).

A microhaematocrits capillary tube was filled with approximately 0.05 ml of blood through capillary action, and one end of the tube was sealed with plastacine. The tubes were placed in a micro-haematocrit centrifuge machine (Hawsley, England) and spun for five minutes at 2,500 revolutions per minute (rmp). A hemocrit reader was used to read the PCV (%) in accordance with Strin and Freeman (2022) instructions.

Determination of Haemoglobin (HB) concentration

The cyanmethaemoglobin technique, as detailed by Smock (2018), was used to determine the concentration of hemoglobin. In short, five milliliters of modified Drabeck's solution (200 mg of potassium ferricyanide or 50 mg of potassium cyanide and 140 mg of potassium hydrogen phosphate) were well mixed with 0.02 milliliters of blood. The volume was then increased to one liter using distilled water, and the pH was adjusted to 7.0. After letting this mixture remain for roughly ten minutes, a spectrometer was used to measure the hemoglobin concentration photometrically at 540 nm. Values for hemoglobin were obtained using a standard curve.

Determination of Red Blood Cell (RBC) count

The pipette from the hemocytometer kit and the red blood cell dilution solution were utilized Turgeon (2016). After gently suctioning the blood sample through the glass mouthpiece of the attached rubber tube with a toma red cell dilution pipette, the blood column was pushed until it reached the 0.5 mark on the stem. Simultaneously, a vertically positioned pipette was submerged in the diluting fluid, and it was slowly rotated while suction was applied until the bulb reached the 101-mark. Using an index finger over the tip, the pipette was removed. It was then held at one end with the second finger and the index finger at the other end horizontally while being combined for two minutes.

Filling was accomplished by positioning the tip of a pipette containing freshly diluted blood against the edge of the cover slip at an angle of 450 directly opposite one of the cells, which was allowed to fill simultaneously. This was done using a clean, grease-free hemocytometer and cover slip that was placed on the groove of the Neubauer counting chamber. In the same manner, the second compartment was filled. The counting chamber was put on the microscope stage after being left for a few minutes to allow the cells to settle. A x10 eye piece and x40 objective were used to view the erythrocytes, and five of the twenty secondary squares each containing sixteen smaller squares were tallied. The RBC/mm3 value was computed as follows:

H= N x 10 x 200 x 5 where

N= Number of RBC counted

10= Depth of counting chamber

200= Dilution factor

5= secondary squares

H= final answer/ cubic millimeters

Red Blood Cells (RBC) Indices

Using established formulas, Mean Corpuscular Volume (MCV), Mean Corpuscular Haemoglobin (MCH), and Mean Corpuscular Hemoglobin Concentration (MCHC) were determined from RBC, PCV, and Hb data (Strin and Freeman, 2022).

Determination of White Blood Cell (WBC) count

Strin and Freeman (2022) described the use of an improved Neubauer counting chamber. A minimum of 25% of the bulb content was discharged using the same method as for the erythrocyte count after mounting and letting it settle for three minutes. The process was otherwise identical to that of the erythrocyte count. The dilution factor was filled to the 11marks in the stem distal to the bulb. Next, the nucleated cells in the first little squares on the immediate right were revealed, followed by the second row. The huge square (1mm³) in the upper left corner, made up of 16 smaller squares, was revealed. The process was repeated for the 16 small squares. The total count was calculated by multiplying the proportionately produced diluted sample's number of cells (L) in millimeters squared by the dilution factor. The typical size of a big Corner square is 1 mm², and its depth is 0.1 mm³. After counting four squares and using a dilution factor of 20, the total count per milliliter was ascertained as follows:

20x 10/4 x L cells = 50 x L cells

Differential Leucocytes Count (DLC)

The Differential Leucocytes Count (DLC) was carried out in compliance with Wang and Hasserjian's (2018) instructions. Cover slips and a spotless, grease-free slide were employed. The glass slide was held horizontally on the bench with the thumb and forefinger of the left hand, and a drop of well-mixed blood was deposited close to the right end. The cover slip was then used to create a neat, thin smear with the edge. The date and identification were then inscribed in pencil on the slide after it had been dried by waving it in the air. After fixing the air-dried slide with methyl alcohol for three minutes, the freshly made staining solution, which included some Giemsa, was applied.An equivalent volume of buffered distilled water (PH 7.2) was used to wash the stained smears. For counting, the battlement method was employed. The stained smear was coated with a drop of immersion oil, placed under a microscope, and counted using an x100 objective. Starting at the narrow end of the smear and moving around the edge in three fields two filed up and two filed down the film was thoroughly analyzed. Until at least 100 cells were counted, the sequence was repeated. The quantity of each type of cell was determined using the percentages of white blood cells that were acquired along with the overall count of white blood cells.

Thus: DLC (%)/100 xWBC

STATISTICAL ANALYSIS

Graph pad prism version 5 was used to analyse the data generated. Chi-square/Fisher’s exact test was employed to determine the association between helminthosis and age, sex, breed and health status of dogs (p≤0.05). The hematological data obtained in the study were summarized as means and standard deviations using statistical model in Microsoft excel software and compared with the standard reference values as described by Meinkoth and Clinkebeard, (2010). Independent samples t-test was used to determine the difference between the mean haematological values of the infected and non-infected dogs, values of p<0.05 were considered significant. The prevalence was calculated for all data as the number of infected individuals divided by the number of examined individuals and was expressed in percentage by multiplying by 100.

The overall prevalence of gastrointestinal nematodes of dogs in this study was 36.5% out of the 200 faecal samples examined. The nematodes identified were Ancylostoma caninum, Toxocara canis and Trichuris vulpis with prevalences of 58.9%, 28.7% and 12.3% respectively occurring either in single or mixed infections (Table 1). Out of the 112 Male dogs and 88 Female dogs sampled, 41(36.6%) and 32(36.4%) were positive respectively. There was no statistically significant association between the Sex of the dogs sampled (P>0.05). Out of the 116 Adult dogs and 84 Puppies sampled, 32(27.6%) and 41(48.8%) were positive respectively. There was statistically significant association between the Age of the dogs sampled (P>0.05). Out of the 36 Exotic, 66 Cross and 98 Local breeds of dogs sampled, 11(30.6%), 23(34.8%) and 39(39.8%) were positive respectively. There was no statistically significant association between the breed of dogs sampled. Out of the 68 sick and 132 apparently healthy dogs sampled, 31(45.6%) and 42(31.8%) were positives respectively. There was no statistically significant association between the health status of the dogs sampled (P>0.05) (Table 2). The associated hemogram showed that, the Mean Corpuscular Volume (MCV) of both the infected and non-infected dogs were below the reference values while only the infected group has Mean Corpuscular Hemoglobin Concentration (MCHC) below the reference values indicating Microcytic hypochromic (Iron deficiency) anaemia. There was eosinophilia, monocytosis and leukocytosis in the infected group whereas neutrophilia occurred in both the infected and non-infected groups. All other haematological values are within the reference ranges. There was no statistically significant difference between the Mean haematological values of the infected and non-infected dogs (Table 3) (P>0.05).

Intestinal nematodes are a common parasite problem that can pose a severe health risk to dogs and the general public in developing countries such as Nigeria. The topic of canine intestinal parasites is highly relevant in numerous parts of the world since dogs can act as hosts, reservoirs, carriers, and transmitters of multiple illnesses (Traub et al., 2005). In this study, the overall prevalence of gastrointestinal nematodes is 36.5%. This is higher than 22.4% reported by Esonu et al., (2019) in Zaria and 31.5% reported by Ezema et al., (2019) in Maiduguri. The higher prevalence might be due to the cohabitation and mingling of many non-infected dogs with infected dogs which enhances cross transmission resulting from continuous environmental contamination with eggs from infected feaces. The nematodes identified were; Ancylostoma caninum (58.9%), Toxocara canis (28.7%) and Trichuris vulpis (12.3%) in either single (83.6%) or mixed (16.4%) infections. Prevalence of intestinal parasites among the sexes recorded in this study revealed a slightly higher prevalence among the males, which correlates with the reports of Kutdang et al. (2010) who reported a higher prevalence of intestinal parasites in male dogs compared to female in his studies conducted in Jos, Plateau State. The higher prevalence of gastrointestinal nematodes in male dogs might be due to the fact that they tend to travel great distances in pursuit of female partners during their breeding season which could increase their exposure to the infectious agents, as reported by Mustapha et al., (2016). Puppies showed significantly higher prevalence (48.8%) of intestinal nematodes compared to the Adult dogs (27.6%) (P<0.05). This is similar with the report of Ahmed et al., (2014) who also reported higher prevalence in the puppies than the adults. This observation can be explained by the adult's age-specific immunity to parasites and the puppies' exposure to transplacental or transmammary infection in their early days of life, as noted by Epe (2009).

Although, canine helminthosis does not show disposition for any particular breed (Eguı´a Aguilar et al., 2005), the higher prevalence rate among local (39.8%) and cross (34.8%) breeds dogs might be due to their higher proportion among the dogs sampled, whereas the lower prevalence among the exotic (30.6%) breed might be attributed to the humane handling such as; routine deworming, intensive confinement, good nutrition and proper hygienic measures by the owners, possibly because of the value accorded to them and companionship. Similar findings on breed based prevalences was also reported by Kumar et al., (2014). Compared to dogs that appeared healthy (31.8%), sick dogs exhibited a greater prevalence (45.6%). This could be because the parasites are widespread in the research area, host vulnerability, ease of infection, and immunological impairment leading to a high incidence of clinical cases. Blood parameters are reported to be negatively impacted by intestinal helminths (Shahat et al., 2022). The haematological data showed that the infected group had significantly lower RBC, Hb, and PCV values than the non-infected group, indicating iron deficiency anemia brought on by ongoing blood loss. The RBC, Hb, and PCV results in this investigation were in agreement with the findings of Kumar et al. (2014) and Qadir et al. (2011). Dogs with the infection had higher WBC counts, which suggested leukocytosis. This result was in agreement with Sharma et al. (2010). The release of histamine and compounds similar to histamine from tissues harmed by the parasite impact may be the cause of this increase. Ogunkoya et al. (2006) and Sharma et al. (2010) found comparable results to the significant increase in eosinophils reported in the infected group, suggesting eosinophilia. According to Kirkova et al. (2005), this increase may be related to the larval migration and defensive mechanism against intestinal nematodes. In addition to monocytosis shown in the infected group, neurophilia in both the infected and non-infected groups may also be caused by concurrent chronic infections, inflammatory reactions, or physiological stress (Audu et al., 2022).

This study established the prevalence (36.5%) of gastrointestinal nematodes of dogs in association with haematological alteration in Gombe State, Nigeria. Gastrointestinal nematodes are a significant health concern for dogs in Nigeria, leading to various clinical and hematological abnormalities. Effective management and control of these parasites are crucial not only for the health of dogs but also for public health. Regular deworming, improved veterinary care, and public education are essential components in combating GI nematode infections in this region.

FUNDING INFORMATION

The research work is funded by the authors of the manuscript. There was no external funding.

COMPETING OF INTEREST

The authors declared that, there is none.

AUTHORS' CONTRIBUTIONS

Y. Audu conceived the idea, design the research work and write the draft manuscript. M. H. Timta collected the samples in the field and performed the laboratory procedures. U. M. Bamanga compiled and analyzed the data generated.

AKNOWLEDGEMENT

We sincerely appreciate the technical assistance of Malam Yauba and Malam Samaila of the Veterinary Parasitology and Veterinary Pathology laboratories respectively of the University of Maiduguri and all those who contributed in one way or the other toward the success of this work.

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Table 1

Prevalence of gastrointestinal nematodes of dogs in Gombe State
NEMATODES	NUMBER POSITIVE	PREVALENCE (%)
A. caninum	43	58.9
T. canis	21	28.7
T. vulpis	9	12.3
A. caninum/T. Canis	7	9.6
A. caninum/T. canis/ T. vulpis	5	6.8
Total single infections	61	83.6
Total mixed infections	12	16.4
Total	73	36.5

Table 2

Prevalence of gastrointestinal nematodes of dogs in Gombe State according to sex, age, breed and health status
VARIABLES		NUMBER POSITIVE (%)	NUMBER EXAMINED
SEX	MALE	112	41(36.6)	0.9807
SEX	FEMALE	88	32(36.4)	0.9807
AGE	ADULT	116	32(27.6)	0.0376
AGE	PUPPY	84	41(48.8)	0.0376
BREED	EXOTIC	36	11(30.6)	0.7741
	CROSS	66	23(34.8)
	LOCAL	98	39(39.8)
HEALTH STATUS	SICK	68	31(45.6)	0.1978
HEALTH STATUS	APPARENTLY HEALTHY	132	42(31.8)	0.1978

Table 3

Means and standard deviations (SD) of the haematological parameters of dogs infected and non-infected by the gastrointestinal nematodes of dogs in Gombe State
Blood parameters	Infected (Mean ± SD)	Non-Infected (Mean ± SD)	Reference ranges
PCV (%)	35.20 ± 1.41	36.15 ± 3.24	37.00–55.00
Hb (g/dl)	11.25 ± 0.43	13.17 ± 1.17	12.00–18.00
RBC (*10¹²/L)	6.05 ± 0.28	6.64 ± 1.15	5.50–8.50
MCV (fl)	58.12 ± 3.68	54.36 ± 5.31	60–77
MCH (pg)	19.25 ± 1.05	19.95 ± 2.64	19.5–24.5
MCHC (g/dl)	31.96 ± 2.41	34.80 ± 1.80	32.00–36.00
WBC (*10⁹/L)	17.55 ± 1.72	9.53 ± 1.64	6.00–17.00
Neutophil (*10⁹/L)	16.25 ± 3.82	12.98 ± 2.76	3.00-11.50
Eosinophil (*10⁹/L)	1.81 ± 0.38	0.62 ± 0.27	1.00-1.25
Basophil (*10⁹/L)	0.00 ± 0.00	0.00 ± 0.00	0.00-1.40
Monocyte (*10⁹/L)	1.91 ± 0.25	0.37 ± 0.18	0.15–1.35
Lymphocyte (*10⁹/L)	3.28 ± 1.47	2.35 ± 0.39	1.00-4.80
Thrombocyte (*10⁵/µL)	2.85 ± 0.21	3.98 ± 0.50	2.00–5.00
T = 1.017, df = 12, P value = 0.3294

The authors declare no competing interests.

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Prevalence of Gastrointestinal Nematodes of Dogs and Associated Hematological Changes in Gombe State, Nigeria

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