Front. Vet. Sci. Frontiers in Veterinary Science Front. Vet. Sci. 2297-1769 Frontiers Media S.A. 10.3389/fvets.2021.751130 Veterinary Science Original Research A Cross-Sectional Study on the Association Between Risk Factors of Toxoplasmosis and One Health Knowledge in Pakistan Maqsood Tooba 1 Shahzad Khuram 1 Naz Shumaila 2 Simsek Sami 3 Afzal Muhammad Sohail 4 Ali Shahzad 5 Ahmed Haroon 1 * Cao Jianping 6 7 8 9 * 1Department of Biosciences, COMSATS University Islamabad (CUI), Islamabad, Pakistan 2Department of Biological Sciences, National University of Medical Sciences (NUMS), Rawalpindi, Pakistan 3Department of Parasitology, Firat University, Elazig, Turkey 4Department of Life Sciences, Faculty of Science, University of Management and Technology (UMT), Lahore, Pakistan 5Department of Wildlife and Ecology, University of Veterinary and Animal Sciences, Lahore, Pakistan 6National Institute of Parasitic Diseases, Chinese Center for Disease Control and Prevention (Chinese Center for Tropical Diseases Research), Shanghai, China 7Key Laboratory of Parasite and Vector Biology, National Health Commission of People's Republic of China, Shanghai, China 8World Health Organization (WHO) Collaborating Centre for Tropical Diseases, Shanghai, China 9The School of Global Health, Chinese Center for Tropical Diseases Research, Shanghai Jiao Tong University School of Medicine, Shanghai, China

Edited by: Si-Yang Huang, Yangzhou University, China

Reviewed by: Wei Cong, Shandong University, China; Zedong Wang, First Hospital of Jilin University, China

 *Correspondence: Haroon Ahmed haroonahmad12@yahoo.com Jianping Cao caojp@yahoo.com

This article was submitted to Veterinary Humanities and Social Sciences, a section of the journal Frontiers in Veterinary Science

 18 11 2021 2021 8 751130 31 07 2021 26 10 2021 Copyright © 2021 Maqsood, Shahzad, Naz, Simsek, Afzal, Ali, Ahmed and Cao. 2021 Maqsood, Shahzad, Naz, Simsek, Afzal, Ali, Ahmed and Cao

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Toxoplasmosis is a zoonotic disease caused by Toxoplasma gondii, a protozoan that infects warm-blooded animals and humans. Approximately one third of the global population is infected by T. gondii. We conducted a cross-sectional study to assess the risk factors and One Health knowledge of toxoplasmosis in Rawalpindi and Islamabad, Pakistan. From July through December 2020, we collected data using questionnaires. The results showed that 60% of participants had heard or read about the disease, 23.3% of participants had no knowledge about the disease, and 16.8% participants were not sure about the disease. More than half of the participants (53.3%) reported that toxoplasmosis was caused by toxins, 5.3% reported that toxoplasmosis was an animal disease, 13.8% reported that toxoplasmosis was a human disease, 65.8% reported that it was both an animal and human disease, and 15.3% reported that it was neither an animal nor a human disease. Approximately 80.5% of participants reported that individuals acquired toxoplasmosis by changing cat litter. Our study findings revealed a low level of knowledge and awareness about toxoplasmosis among males. Therefore, there should be awareness programs to educate individuals about the risks of this deadly disease and to provide information on the major routes of transmission.

 knowledge attitude practices risk factor one health toxoplasmosis Pakistan Introduction

Toxoplasmosis is a zoonotic disease caused by the intracellular protozoan Toxoplasma gondii (1). T. gondii is an obligate intracellular parasite that naturally exists in one of three forms: (1) oocysts, which release sporozoites, are only produced in the small intestines of cats and are released into the environment through their feces; (2) tissue cysts, which release bradyzoites; and (3) tachyzoites, which are the proliferative form (2). Type I, II, and III strains of T. gondii have been identified in Europe, parts of Asia, and US where type II strain is mostly involved in human toxoplasmosis (3). Type I and type III strains are prevalent in Central and South America (4). Approximately 33% of the total human population has been affected by T. gondii (1). Countries in North America, Southeast Asia, Northern Europe, and Saharan African have low prevalence rates (10% to 30%), Central and Southern Europe have moderate prevalence rates (30% to 50%), and tropical African countries and Latin America have high prevalence rates of toxoplasmosis (5). The seroprevalence of toxoplasmosis was 29.45% from Southern Punjab, Pakistan (6). In Pakistan, Khyber Pakhtunkhwa has 40.6% of the seroprevalence of toxoplasmosis in women with poor obstetric history (7).

In humans, toxoplasmosis is transmitted by consuming raw or inadequately cooked meat (8), by inadvertently ingesting oocysts passed into feces by cats, either in a cat litter box or outdoors in the soil (9), and from mother to her unborn fetus (10). T. gondii infection, which is a life-threatening disease, results in retinal infection in both healthy and immunocompromised individuals (11). In immunocompromised individuals, toxoplasmosis is mostly asymptomatic (12); however, 10% of those infected may develop lymphadenitis, ocular toxoplasmosis (chorioretinitis), and mild flu-like and/or mononucleosis-like symptoms (13).

Due to their non-specificity, the clinical symptoms of toxoplasmosis are not reliable for diagnosis. While traditional diagnostic methods are based on serological tests and bioassays, a variety of molecular methods have been recently used for diagnosis of toxoplasmosis (14). Some of the diagnostic tests for toxoplasmosis include microscopy (15), bioassays (16), dye test (17), modified agglutination test (18), latex agglutination test (19), indirect hemagglutination test (20), indirect fluorescent antibody test (21), enzyme-linked immunosorbent assay (22), immunosorbent agglutination assay (23), immunochromatographic test (24), piezoelectric immunoagglutination assay (25), Western blot (26), and avidity test (27). Pharmaceutical interventions against toxoplasmosis include either a combination of pyrimethamine and sulfadiazine with folic acid or a combination of pyrimethamine and macrolide antibiotics or lincosamide. For congenital toxoplasmosis, pregnant women are treated with spiramycin (12).

Toxoplasmosis, which affects both animals and humans, causes major economic losses (28). In the livestock sector of Pakistan, different diseases cause annual economic loss of 79 billion Pakistani rupees (PKR) (29). Despite having such significant impact, very few studies have explored the prevalence of toxoplasmosis in Pakistan. Therefore, we conducted a study to determine the knowledge, attitudes, and practices of toxoplasmosis among university students of twin cities, Rawalpindi and Islamabad, Pakistan.

 Results Socio-Demographic Characteristics

Table 1 presents the sociodemographic characteristics of the participants (n = 400). Most of the participants (86%) were females. The majority of the participants (65.5%) were 18 to 25 years of age, 25.5% were 26 to 35 years of age, 5.5% were 36 to 45 years of age. Among the participants, 46.5% were from Punjabi, 15.3% were from Kashmiri, 7.8% were from Pathan, and 8% were from ethnicity. Approximately, 45% of the participants were in a Bachelor's program, 29.3% were in a master's program, 16.8% were in a PhD program.

Socio-demographic characteristics of participants.

Variable Characteristics Participants (N) Frequency (%)
Age (years) 18–25 262 65.5
26–35 102 25.5
36–45 22 5.5
>45 14 3.5
Sex Male 56 14.0
Female 344 86.0
Ethnicity Punjabi 186 46.5
Sindhi 13 3.3
Pathan 31 7.8
Blochi 25 6.3
Gilgiti 32 8.0
Kashmiri 61 15.3
Islamabad territory 35 8.8
Other 17 4.3
Religion Muslims 350 87.5
Non-muslim 50 12.5
Marital status Married 122 30.5
Single 278 69.5
Education Bachelors 180 45.0
Master 117 29.3
Ph.D. 67 16.8
Post Doc 36 9.0
Occupation Farmer (Household livestock) 68 17.0
Worker at livestock facilities 40 10.0
Other 292 73.0
Residence Rural 142 35.5
Urban 258 64.5
Income per month <15,000 PKR (including pocket money) 151 37.7
20,000–30,000 PKR 86 21.5
>30,000 PKR 163 40.8
Number of family members <5 79 19.8
5–10 295 73.8
11–15 26 6.5
Knowledge on Toxoplasmosis

Among the participants, 60% had heard or read about the disease, 23.3% had no knowledge about the disease, and 16.8% were not sure about the disease. We performed Chi square test to assess the relationship among the categorical variables. Out of 400 participants, 53.3% reported that toxoplasmosis was caused by a toxin, 13.8% reported that toxoplasmosis was not caused by a toxin, and 33% had no knowledge on the cause of toxoplasmosis. Only a limited (19.3%) number of participants had been tested for toxoplasmosis, 67.5% of the participants were aware that toxoplasmosis was caused by an infection, and 26.3% reported that they had no knowledge on the causes of toxoplasmosis. The majority (69.8%) of the participants thought that a transmission source was cat feces, and 75.3% were aware that parasites were shed in the feces of infected cats. Approximately 58.5% of the participants reported that toxoplasmosis could be caused by touching raw meat and contaminated soil/sand and 26.8% of the participants had no knowledge about this. A significant number (68%) of participants reported that pregnant women could develop serious complications from toxoplasmosis, and 48.5% reported that the fetus and newborn could develop serious complications from toxoplasmosis. The majority (71.3%) of the participants reported that toxoplasmosis was transmitted from animals to humans, and 64% of the participants believed that toxoplasmosis is symptomatic. Approximately 47.5% of the participants reported that toxoplasmosis could cause miscarriages or stillbirth (Table 2).

Knowledge of toxoplasmosis.

Variable Characteristics Participants (N) Frequency (%) Statistical analysis (Chi Square)
Have you heard or read about toxoplasmosis? Yes 240 60.0 X2= 23.449 df = 2 p < 0.00001
No 93 23.3
May be 67 16.8
Can bacteria infect animals? Yes 355 88.8 X2 = 144.7348 df = 2 p < 0.00001
No 14 3.5
Do not know 31 7.8
Is toxoplasmosis caused by a toxin? Yes 213 53.3 X2 = 22.8448 df = 2 p = 0.000011
No 55 13.8
Do not know 132 33.0
Have you ever been tested for toxoplasmosis? Yes 77 19.3 X2 = 39.9216 df = 1 p < 0.00001
No 323 80.8
Is toxoplasmosis an infection? Yes 270 67.5 X2 = 65.4362 df = 2 p < 0.00001
No 25 6.3
Do not know 105 26.3
Is the parasite shed in the feces of infected cats? Yes 301 75.3 X2 = 99.0611 df = 2 p < 0.00001
No 14 3.5
Do not know 85 21.3
Is the parasite present in raw or undercooked meat? Yes 311 77.8 X2 = 103.7767 df = 2 p < 0.00001
No 14 3.5
Do not know 75 18.8
Is the parasite present in unpasteurized milk? Yes 268 67.8 X2 = 58.9505 df = 2 p < 0.00001
No 29 7.3
Do not know 98 24.8
Can individuals acquire toxoplasmosis by clean up the cat litter box? Yes 279 69.8 X2 = 65.1131 df = 2 p < 0.00001
No 27 6.8
Do not know 94 23.5
Can toxoplasmosis be caused by touching raw meat? Yes 235 58.8 X2 = 25.2688 df = 2 p < 0.00001
No 58 14.5
Do not know 107 26.8
Can individuals acquire toxoplasmosis by touching sand/soil in the garden or yard? Yes 224 56.0 X2 = 26.4293 df = 2 p < 0.00001
No 52 13.0
Do not know 124 31.0
Do pregnant women develop serious complications from toxoplasmosis? Yes 272 68.0 X2 = 87.0261 df = 2 p < 0.00001
No 15 3.8
Do not know 113 28.2
Do unborn and/or newborn children develop serious complications from toxoplasmosis? Yes 251 62.7 X2 = 57.6997 df = 2 p < 0.00001
No 27 6.8
Do not know 122 30.5
Does toxoplasmosis in a pregnant women cause fever and flu-like symptoms? Yes 194 48.5 X2 = 42.8536 df = 2 p < 0.00001
No 33 8.3
Do not Know 173 43.3
Does toxoplasmosis in pregnant women cause swollen glands? Yes 160 40.0 X2 = 46.3457 df = 2 p < 0.00001
No 31 7.8
Do not know 209 52.3
Can toxoplasmosis in pregnant women cause no symptoms? Yes 153 38.3 X2 = 11.4422 df = 2 p = 0.003276
No 71 17.8
Do not know 176 44.0
Can toxoplasmosis be transferred from a pregnant woman to her fetus if she became infected during her pregnancy? Yes 186 46.5 X2 = 17.4235 df = 2 p = 0.000165
No 60 15.0
Do not know 154 38.5
Can toxoplasmosis be transferred from a pregnant woman to her fetus if she became infected before her pregnancy? Yes 164 41.0 X2 = 10.0036 df = 2 p = 0.006726
No 74 18.5
Do not know 162 40.5
Can an infant with toxoplasmosis with no signs of illness at birth develop illness later in life? Yes 218 54.5 X2 = 40.3357 df = 2 p = 0.00001
No 36 9.0
Do not know 146 36.5
Can an infant with toxoplasmosis be treated with medicine? Yes 209 52.3 X2 = 49.4146 df = 2 p = 0.00001
No 29 7.2
Do not know 162 40.5
In which stage of gestation is toxoplasmosis highly severe? First 31 7.8 X2 = 38.1639 df = 3 p = 0.00001
Second 56 14.0
Third 117 29.3
Do not know 196 49.0
Are you aware that pregnant women should not smoke? Yes 317 79.3 X2 = 96.641 df = 2 p < 0.00001
No 19 4.8
Do not know 64 16.0
Can women who have toxoplasmosis before they get pregnant transmit it to the baby? Yes 195 48.8 X2 = 15.8341 df = 2 p = 0.000364
No 64 16.0
Do not know 141 35.3
Can toxoplasmosis be treated in pregnant women? Yes 248 62.0 X2 = 60.5088 df = 2 p < 0.00001
No 25 6.3
Do not know 127 31.8
Do infants with toxoplasmosis develop vision problems? Yes 238 59.5 X2 = 48.0302 df = 2 p < 0.00001
No 32 8.0
Do not know 130 32.5
Should cat litter be replaced daily? Yes 283 70.8 X2 = 59.0899 df = 2 p < 0.00001
No 33 8.3
Do not know 84 21.0
Can pregnant women avoid toxoplasmosis by consuming thoroughly cooked meat? Yes 263 65.8 X2 = 57.3761 df = 2 p < 0.00001
No 29 7.2
Do not know 108 27.0
Can individuals avoid toxoplasmosis by washing and peeling all fruits and vegetables before consumption? Yes 270 67.5 X2 = 59.3376 df = 2 p < 0.00001
No 29 7.2
Do not know 101 25.3
Which is the diagnostic method of toxoplasmosis in the fetus? Ultrasound 244 61.0 X2 = 23.6343 df = 2 p < 0.00001
CT Scan 77 19.3
Do not know 79 19.8
Toxoplasma gondii is a Bacterium 37 9.3 X2 = 125.594 df = 5 p = 5
Virus 46 11.5
Parasite 221 55.3
Fungi 7 1.8
Insect 1 0.3
I am not sure 88 22.0
Can toxoplasmosis be transmitted from animals to humans? Yes 285 71.3 X2 = 88.1145 df = 2 p < 0.00001
No 16 4.0
Do not know 99 24.8
Is toxoplasmosis associated with symptoms? Yes 256 64.0 X2 = 37.3477 df = 2 p < 0.00001
No 47 11.8
Do not know 97 24.3
Does toxoplasmosis affect only pregnant women? Yes 154 38.5 X2 = 13.9087 df = 2 p = 0.000954
No 180 45.0
Do not know 66 16.5
Does toxoplasmosis cause miscarriage or stillbirth? Yes 190 47.5 X2 = 10.4531 df = 2 p = 0.005372
No 76 19.0
Do not know 134 33.5
Attitudes Toward Toxoplasmosis

Among the participants, 5.3% believed that toxoplasmosis was an animal disease, 13.8% thought that toxoplasmosis was a human disease, 65.8% thought it was both an animal and human disease, and 15.3% thought it was not either of them. Most of the participants (87.3%) routinely washed their hands after gardening. Approximately, 85.8% of the participants washed their hands after changing the cat litter and after handling raw meat. Most of the participants (89%) cooked meat wel-prior to consumption, and 86.3% avoided raw milk. A significant number of participants (86.5%) reported consuming untreated water, and the majority (80%) of the participants considered toxoplasmosis to be a dangerous disease. A small number (33.5%) of participants had consumed undercooked meat, and 64.5% had direct contact with cats. Approximately, 56.7% of participants had attended training related to livestock. A significant number (83%) of participants supported initiatives for the control of toxoplasmosis. There were no significant differences in the results when asked how health should be ensured when buying or receiving new livestock. Approximately 55% of the participants thought that toxoplasmosis-suspected cases should seek the advice of healthcare providers (Table 3).

Attitudes toward toxoplasmosis.

Variable Characteristics Participants (N) Frequency (%) Statistical analysis (Chi Square)
What is your perception about toxoplasmosis? Serious animal disease 21 5.3 X2 = 67.7315 df = 3 p < 0.00001
Serious human disease 55 13.8
Both 263 65.8
None 61 15.3
Do you routinely wash your hands after gardening? Yes 349 87.3 X2 = 68.8634 df = 1 p < 0.00001
No 51 12.7
Do you routinely wash your hands after changing the cat litter box? Yes 343 85.8 X2 = 60.7863 df = 1 p < 0.00001
No 57 14.2
Do you routinely wash your hands after handling raw meat? Yes 343 85.8 X2 = 60.7863 df = 1 p < 0.00001
No 57 14.2
Do you thoroughly cook meat before consumption? Yes 356 89.0 X2 = 79.7086 df = 1 p < 0.00001
No 44 11.0
Do you avoid consuming raw milk? Yes 345 86.3 X2 = 63.3665 df = 1 p < 0.00001
No 55 13.7
Do you avoid consuming untreated water? Yes 346 86.5 X2 = 64.6975 df = 1 p < 0.00001
No 54 13.5
Is toxoplasmosis dangerous? Yes 320 80.0 X2 = 89.0025 df = 2 p < 0.00001
No 26 6.5
Do not know 54 13.5
Can toxoplasmosis be transmitted by consuming inadequately washed vegetables and undercooked meat? Yes 308 77.0 X2 = 71.8426 df = 2 p < 0.00001
No 35 8.8
Do not know 57 14.2
Do you consume undercooked meat? Yes 134 33.5 X2 = 9.3647 df = 1 p = 0.002212
No 266 66.5
Do you have direct contact with a cat? Yes 258 64.5 X2 = 7.1107 df = 1 p = 0.007662
No 142 35.5
Are fruits and vegetables in contact with cat feces? Yes 200 50.0 X2 = 8.8076 df = 2 p = 0.012231
No 110 27.5
Do not know 90 22.5
Do you wash kitchen utensils after contact with raw meat and unwashed fruits and vegetables? Yes 327 81.8 X2 = 43.4781 df = 1 p < 0.00001
No 73 18.2
Do you wear personal protective equipment while handling your cat? Yes 258 64.5 X2 = 7.1107 df = 1 p = 0.007662
No 142 35.5
Have you attended any training, awareness session or workshop related to livestock? Yes 173 43.3 X2 = 1.4752 df = 1 p = 0.224526 not significant
No 227 56.7
Will you support any initiative to control toxoplasmosis? Yes 332 83.0 X2 = 48.3184 df = 1 p < 0.00001
No 68 17.0
Does toxoplasmosis affect the production of livestock? Yes 281 70.3 X2 = 55.2524 df = 2 p < 0.00001
No 36 9.0
Do not know 83 20.7
How can health be ensured when buying or receiving new livestock? Seek veterinary advice 139 34.8 X2 = 6.0507 df = 3 p = 0.109168 not significant
Rely on own experience 68 17.0
Acquire from known and/or trusted people 111 27.7
None 82 20.5
What should an individual with suspected toxoplasmosis do? Pray 34 8.5 X2 = 37.2797 df = 3 p < 0.00001
Visit health facility 220 55.0
Consuming herbal products 66 16.5
Visit local chemist and acquire medicine 80 20.0
Practices Toward Toxoplasmosis

Most of the participants (71%) fed their cats dry or commercial cat food and did not let their cats kill and eat rodents. Approximately, 61.8% of the participants reported that they avoided stray cats, and 70% of the participants did not allow someone else change the cat litter box. A significant number (83.3%) of participants boiled milk before consumption, and 87.8% ensured their houses were free of waste. Most participants (86.5%) kept foods covered in containers, and 78.3% separated sick animals from healthy ones. A significant number (72.8%) of participants used protective clothes while handling livestock (Table 4).

Practices toward toxoplasmosis.

Variable Characteristics Participants (N) Frequency (%) Statistical analysis (Chi Square)
Do you feed your cat dry or commercial food and not let it kill and eat rodents? Yes 284 71.0 X2 = 15.9079 df = 1 p = 0.000066
No 116 29.0
Do you avoid stray cats? Yes 247 61.8 X2 = 4.5799 df = 1 p = 0.03235
No 153 38.2
Do you let someone else change the cat litter box? Yes 280 70.0 X2 = 14.2602 df = 1 p = 0.000159
No 120 30.0
Do you change the cat litter box daily? Yes 323 80.8 X2 = 39.9216 df = 1 p < 0.00001
No 77 19.2
Do you have a vegetable garden at home? Yes 275 68.8 X2 = 12.3626 df = 1 p = 0.000438
No 125 31.2
Do you boil milk before consumption? Yes 333 83.3 X2 = 49.3434 df = 1 p < 0.00001
No 67 16.7
Do you ensure that your house is free of waste? Yes 351 87.8 X2 = 71.7934 df = 1 p < 0.00001
No 49 12.2
Do you store food in covered containers? Yes 346 86.5 X2 = 64.6975 df = 1 p < 0.00001
No 54 13.5
Do you keep newly purchased animals in quarantine for some time? Yes 236 59.0 X2 = 2.6469 df = 1 p = 0.103753 not significant
No 164 41.0
Do you separate sick animals from healthy animals? Yes 313 78.3 X2 = 32.0952 df = 1 p < 0.00001
No 87 21.7
Do you use any kind of protective clothing while handling livestock? Yes 291 72.8 X2 = 19.0916 df = 1 p = 0.000012
No 109 27.2
Risk Factors Associated With Toxoplasmosis

A significant number (80.5%) of participants thought that individuals could acquire toxoplasmosis by changing the cat litter, and 76.8% of participants responded that individuals could acquire toxoplasmosis by consuming raw/undercooked meat. Most participants (72.5%) believed that individuals could get toxoplasmosis by consuming raw milk, while 14.2% were not aware of this. Among the participants, 69.5% considered blood transfusion to be cause of toxoplasmosis, 13.7% considered that blood transfusion was not a cause of toxoplasmosis, and 16.8% had no knowledge about this. A significant number (68.3%) of participants thought toxoplasmosis could be transmitted by gardening without gloves. Among the participants, 47% believed that immunocompromised, pregnant women were at high risk of toxoplasmosis, 20.3% believed that pregnant women had a moderate risk of toxoplasmosis, 6.5% people reported that pregnant women had a low risk of toxoplasmosis, and 26.2% had no knowledge (Table 5).

Risk factors of toxoplasmosis.

Variable Characteristics Participants (N) Frequency (%) Statistical analysis (Chi Square)
Can individuals acquire toxoplasmosis by changing cat litter? Yes 322 80.5 X2 = 39.073 df = 1 p < 0.00001
No 78 19.5
Can individuals acquire toxoplasmosis by consuming raw/undercooked meat? Yes 307 76.8 X2 = 67.7466 df = 2 p < 0.00001
No 43 10.7
Do not know 50 12.5
Can individuals acquire toxoplasmosis by consuming raw milk? Yes 290 72.5 X2 = 52.0668 df = 2 p < 0.00001
No 53 13.3
Do not know 57 14.2
Can individuals acquire toxoplasmosis by consuming raw vegetables? Yes 276 69.0 X2 = 41.6118 df = 2 p < 0.00001
No 63 15.8
Do not know 61 15.2
Can individuals acquire toxoplasmosis through blood transfusions? Yes 278 69.5 X2 = 43.5633 df = 2 p < 0.00001
No 55 13.7
Do not know 67 16.8
Can individuals acquire toxoplasmosis by consuming untreated water? Yes 286 71.5 X2 = 48.9029 df = 2 p < 0.00001
No 55 13.7
Do not know 59 14.8
Can individuals acquire toxoplasmosis by gardening without gloves? Yes 273 68.3 X2 = 40.4536 df = 2 p < 0.00001
No 56 14.0
Do not know 71 17.7
What is the risk level of toxoplasmosis among immunocompromised, pregnant women? High 188 47.0 X2 = 36.8318 df = 3 p < 0.00001
Medium 81 20.3
Low 26 6.5
Do not know 105 26.2
One Health Knowledge of Toxoplasmosis

The majority (61.5%) of the participants knew about One Health, and 14% had no knowledge about One Health. Approximately 60.3% of participants knew about zoonosis, 26.5% were not aware of zoonosis, and 13.2% of participants were not sure about the concept of zoonosis. Out of 400 participants, 232 (58%) knew that toxoplasmosis is a zoonotic infection, and 18 participants (4.5%) had no knowledge on this. Only 8.8% of participants reported that toxoplasmosis was present in humans, 11% people reported that toxoplasmosis was present in livestock, 62.7% reported that toxoplasmosis was present in both humans and livestock, while 17.5% were not sure about this. Among the participants, 37.3% thought that toxoplasmosis causes blindness, 23.2% thought that toxoplasmosis did not cause blindness, and 39.5% were not sure about this (Table 6).

One health knowledge about toxoplasmosis among participants.

Variable Characteristics Participants (N) Frequency (%) Statistical analysis (Chi Square)
Do you know about one health? Yes 246 61.5 X2 = 29.2344 df = 2 p < 0.00001
No 56 14.0
Not sure 98 24.5
Do you have knowledge on zoonosis? Yes 241 60.3 X2 = 29.381 df = 2 p < 0.00001
No 106 26.5
Not sure 53 13.2
Is toxoplasmosis a zoonotic disease? Yes 232 58.0 X2 = 72.8102 df = 2 p < 0.00001
No 18 4.5
Not sure 150 37.5
How is toxoplasmosis transmitted? Soil 10 2.5 X2 = 93.52 df = 5 p = 0
Water 12 3.0
Livestock 56 14.0
a and b 21 5.3
a and c 224 56
Not sure 77 19.2
Which organisms does toxoplasmosis affect? Human 35 8.8 X2 = 51.988 df = 3 p < 0.00001
Livestock 44 11.0
Both human and livestock 251 62.7
Not sure 70 17.5
Does toxoplasmosis go away? Yes 211 52.8 X2 = 54.5757 df = 2 p < 0.00001
No 26 6.5
Not sure 163 40.7
Can toxoplasmosis-infected individuals go blind? Yes 149 37.3 X2 = 4.1335 df = 2 p = 0.126594 not significant
No 93 23.2
Not sure 158 39.5
Association Among Different Variables Based on ANOVA

We used one-way ANOVA to determine whether there were any statistically significant differences among the means of three or more independent groups. We used six specific independent variables, i.e., age, sex, ethnicity, education, religion, and marital status, and five dependent variables, i.e., knowledge, attitudes, practices, risk factors, and One Health. Our ANOVA results revealed that age was associated (p < 0.05) with attitudes and One Health; however, there were no significant associations with sex. Ethnicity was associated (p < 0.05) with knowledge and One Health; religion was associated (p < 0.05) with One health; and marital status was associated (p < 0.05) with knowledge, attitudes, risk factors, and One health. Likewise, the education of the participants was associated (p < 0.05) with knowledge, risk factors, and One Health (Table 7).

Association between demographic characteristics and knowledge, attitude, practices, one health, and risk factors (ANOVA).

Variable Knowledge Attitude Practices Risk factors One health
M SD SE P-value M SD SE P-value M SD SE P-value M SD SE P-value M SD SE P-value
Age (in years)
18–25 18.48 9.00 0.556 0.097 13.26 3.44 0.212 0.009 8.33 2.60 0.161 0.090 5.46 2.70 0.167 0.472 3.59 2.42 0.150 0.006
26–35 21.04 9.38 0.929 13.24 3.90 0.386 8.25 2.73 0.270 5.87 2.78 0.275 4.37 2.57 0.255
36–45 20.36 10.97 2.339 11.27 4.76 1.015 7.09 3.94 0.840 5.59 3.26 0.695 4.18 2.84 0.605
above 45 21.00 11.57 3.092 10.71 5.06 1.352 7.07 3.54 0.946 4.86 3.51 0.937 5.36 2.92 0.782
Gender
Female 19.38 9.37 0.505 0.769 13.15 3.68 0.198 0.219 8.30 2.69 0.145 0.060 5.60 2.73 0.147 0.414 3.92 2.50 0.135 0.441
Male 18.98 9.27 1.239 12.48 4.09 0.547 7.55 3.17 0.424 5.27 3.11 0.416 3.64 2.76 0.369
Ethnicity
Islamabad territory 22.14 7.87 1.330 0.009 13.66 3.23 0.545 0.313 8.66 2.62 0.443 0.664 6.40 2.45 0.414 0.220 4.74 2.33 0.394 <0.001
Kashmiri 16.62 7.75 0.993 12.82 4.08 0.522 8.11 2.07 0.266 4.87 2.60 0.333 2.82 1.94 0.248
Punjabi 19.13 9.40 0.689 13.44 3.31 0.243 8.25 2.56 0.188 5.77 2.67 0.196 3.93 2.61 0.192
Blochi 20.12 11.81 2.362 11.60 5.16 1.031 7.64 3.85 0.770 5.48 3.51 0.703 4.80 2.69 0.539
Gilgiti 23.47 9.48 1.676 12.59 4.25 0.751 7.81 3.59 0.634 5.25 3.03 0.535 5.22 2.38 0.421
Other 15.35 7.87 1.908 12.53 2.60 0.631 8.29 1.53 0.371 5.29 2.20 0.534 2.35 1.62 0.392
Pathan 19.03 10.64 1.911 12.68 4.63 0.831 7.87 4.04 0.725 5.10 3.40 0.611 3.32 2.68 0.481
Sindhi 21.31 7.28 2.020 12.54 3.45 0.958 9.23 1.48 0.411 5.54 2.63 0.730 4.23 2.20 0.611
Religion
Muslim 18.93 9.40 0.503 0.024 13.02 3.72 0.199 0.646 8.09 2.77 0.148 0.048 5.55 2.77 0.148 0.935 3.77 2.52 0.135 0.013
Non-muslim 22.10 8.49 1.201 13.28 3.96 0.560 8.92 2.65 0.375 5.52 2.93 0.414 4.72 2.47 0.349
Marital status
Married 21.54 9.85 0.891 0.002 12.43 4.49 0.406 0.026 8.20 2.99 0.271 0.997 6.00 2.75 0.249 0.032 4.69 2.53 0.229 <0.001
Single 18.35 8.96 0.537 13.33 3.34 0.200 8.20 2.67 0.160 5.35 2.78 0.167 3.53 2.46 0.147
Qualification
Bachelors 16.33 8.43 0.629 <0.001 12.89 3.83 0.285 0.565 8.31 2.57 0.192 0.870 5.02 2.72 0.203 0.005 3.07 2.22 0.166 <0.001
Masters 20.21 9.70 0.896 12.91 3.82 0.353 8.04 2.80 0.259 5.84 2.72 0.252 3.98 2.65 0.245
Ph.D 22.85 8.79 1.074 13.58 3.54 0.433 8.13 3.08 0.376 6.15 2.84 0.346 4.99 2.42 0.296
Post doc 24.83 8.42 1.404 13.33 3.46 0.576 8.25 3.06 0.511 6.17 2.79 0.465 5.58 2.22 0.370
Statistical Analysis Using Log-Linear Regression

Log-linear regression analysis involves using a dependent variable measured by frequency counts with categorical or continuous independent predictor variable. Log-linear analysis is a technique used in statistics to examine the relationship between more than two categorical variables. The technique is used for both hypothesis testing and model building. In this study, we used the independent variables age, gender, ethnicity, education, religion, and marital status and the dependent variables knowledge, attitudes, practices, risk factors, and One Health. We applied log-linear regression on age and the dependent variables and obtained different p-values, rate ratios, and R2McF. Mostly high R2McF values represent goodness of fit. With the dependent variable knowledge, we obtained p < 0.001, a rate ratio of 18.48, and an R2McF value of 0.0124. With attitude as the dependent variable, we obtained p < 0.001, a rate ratio of 13.256, and an R2McF value of 0.0241. With the dependent variable practices, we obtained p < 0.001, a rate ratio of 8.332, and an R2McF value 0.0119. With risk factors, we obtained p < 0.001, a rate ratio of 5.458, and an R2McF value of 0.00430. Finally, with One Health, we obtained p < 0.001, a rate ratio of 3.59, and an R2McF value of 0.0220. The highest and lowest R2McF values were obtained for attitudes and risk factors, respectively.

We applied a log-linear regression on the independent variable gender and the dependent variables. With knowledge, we obtained p < 0.001, a rate ratio of 19.378, and an R2McF value of 1.73e-4. With attitudes, we obtained p < 0.001, a rate ratio of 13.145, and an R2McF value of 0.00307. With practices, we obtained p < 0.001, a rate ratio of 8.302, and an R2McF value of 0.00633. With risk factors, we obtained p < 0.001, a rate ratio of 5.596, and an R2McF value of 0.00115. With One Health, we obtained p < 0.001, a rate ratio of 3.924, and an R2McF value of 0.00113. The highest and lowest R2McF values were obtained for knowledge and One Health, respectively.

We applied log-linear regression on the independent variable ethnicity and the dependent variables. With knowledge, we obtained p < 0.001, a rate ratio of 22.143, and an R2McF value of 0.0367. With attitudes, we obtained p < 0.001, a rate ratio of 13.657, and an R2McF value of 0.0168. With practices, we obtained p < 0.001, a rate ratio of 8.657, and an R2McF value of 0.00868. With risk factors, we obtained p < 0.001, a rate ratio of 6.400, and an R2McF value of 0.0161. With One Health, we obtained p < 0.001, a rate ratio of 4.743, and an R2McF value of 0.0672. The highest and lowest R2McF values were for One Health and practices, respectively (Table 8).

Association between demographic characteristics and knowledge, attitudes, practices, one health, and risk factors (log-linear regression).

Knowledge Attitude Practices Risk factor One health
Predictor 95% CI (Lower–upper) Rate ratio P R2McF 95% CI (Lower–upper) Rate ratio P R2McF 95% CI (Lower–upper) Rate ratio P R2McF 95% CI (Lower–upper) Rate ratio P R2McF 95% CI (Lower–upper) Rate ratio P R2McF
Intercept Lower 2.8884 Upper 2.945 18.48 <0.001 Lower 2.5512 Upper 2.6177 13.256 <0.001 Lower 2.0782 Upper 2.16206 8.332 <0.001 Lower 1.6453 Upper 1.749 5.458 <0.001 Lower 1.2147 Upper 1.342 3.59 <0.001
Age (in years)
26–35–18–25 Lower 0.0790 Upper 0.181 1.14 <0.001 0.0124 Lower −0.0644 Upper −0.0613 0.998 0.962 0.0241 Lower −0.0900 Upper 0.06905 0.990 0.796 0.0119 Lower −0.0222 Upper 0.169 1.076 0.133 0.00430 Lower 0.0841 Upper 0.309 1.22 <0.001 0.0220
36–45–18–25 Lower 4.33e-4 Upper 0.194 1.10 0.049 Lower −0.2909 Upper −0.0332 0.850 0.014 Lower −0.3237 Upper 0.00114 0.851 0.052 Lower −0.1601 Upper 0.208 1.024 0.798 Lower −0.0619 Upper 0.366 1.16 0.164
Above 45–18–25 Lower 0.0103 Upper 0.246 1.14 0.033 Lower −0.3763 Upper −0.0494 0.808 0.011 Lower −0.3654 Upper 0.03735 0.849 0.110 Lower −0.3599 Upper 0.127 0.890 0.347 Lower 0.1647 Upper 0.635 1.49 <0.001
Intercept Lower 2.9401 Upper 2.9881 19.378 <0.001 Lower 2.547 Upper 2.6052 13.145 <0.001 Lower 2.080 Upper 2.15321 8.302 <0.001 Lower 1.677 Upper 1.7667 5.596 <0.001 Lower 1.314 Upper 1.4206 3.924 <0.001
Gender
Male–female Lower −0.0854 Upper 0.0441 0.980 0.532 1.73e-4 Lower −0.131 Upper 0.0279 0.950 0.203 0.00307 Lower −0.197 Upper 0.00759 0.910 0.070 0.00633 Lower −0.183 Upper 0.0621 0.941 0.334 0.00115 Lower −0.222 Upper 0.0728 0.928 0.322 0.00113
Intercept Lower 3.0271 Upper 3.1679 22.143 <0.001 Lower 2.525 Upper 2.7039 13.657 <0.001 Lower 2.046 Upper 2.2710 8.657 <0.001 Lower 1.725 Upper 1.98725 6.400 <0.001 Lower 1.405 Upper 1.7088 4.743 <0.001
Ethnicity
Kashmiri–Islamabad territory Lower −0.3802 Upper −0.1932 0.751 <0.001 0.0367 Lower −0.177 Upper 0.0505 0.939 0.276 0.0168 Lower −0.208 Upper 0.0783 0.937 0.375 0.00868 Lower −0.447 Upper −0.09999 0.761 0.002 0.0161 Lower −0.733 Upper −0.3068 0.595 <0.001 0.0672
Punjabi–Islamabad territory Lower −0.2240 Upper −0.0686 0.864 <0.001 Lower −0.114 Upper 0.0815 0.984 0.743 Lower −0.171 Upper 0.0754 0.953 0.447 Lower −0.247 Upper 0.04107 0.902 0.161 Lower −0.356 Upper −0.0195 0.829 0.029
Blochi–Islamabad territory Lower −0.2080 Upper 0.0164 0.909 0.094 Lower −0.309 Upper −0.0174 0.849 0.028 Lower −0.306 Upper 0.0561 0.883 0.176 Lower −0.368 Upper 0.05738 0.856 0.152 Lower −0.223 Upper 0.2468 1.012 0.920
Gilgiti–Islamabad territory Lower −0.0422 Upper 0.1585 1.060 0.256 Lower −0.214 Upper 0.0515 0.922 0.231 Lower −0.270 Upper 0.0648 0.902 0.230 Lower −0.398 Upper 0.00197 0.820 0.052 Lower −0.119 Upper 0.3104 1.100 0.383
0ther–Islamabad territory Lower −0.5065 Upper −0.2259 0.693 <0.001 Lower −0.248 Upper 0.0753 0.917 0.295 Lower −0.243 Upper 0.1570 0.958 0.674 Lower −0.434 Upper 0.05490 0.827 0.129 Lower −1.046 Upper −0.3558 0.496 <0.001
Pathan–Islamabad territory Lower −0.2585 Upper −0.0443 0.860 0.006 Lower −0.208 Upper 0.0590 0.928 0.274 Lower −0.264 Upper 0.0734 0.909 0.268 Lower −0.431 Upper −0.02407 0.796 0.028 Lower −0.602 Upper −0.1101 0.701 0.005
Sindhi–Islamabad territory Lower −0.1757 Upper 0.0988 0.962 0.583 Lower −0.263 Upper 0.0923 0.918 0.346 Lower −0.147 Upper 0.2756 1.066 0.552 Lower −0.410 Upper 0.12094 0.865 0.286 Lower −0.419 Upper 0.1907 0.892 0.463
Intercept Lower 2.9164 Upper 2.965 18.93 <0.001 Lower 2.5375 Upper 2.596 13.02 <0.001 Lower 2.05433 Upper 2.128 8.09 <0.001 Lower 1.670 Upper 1.759 5.554 <0.001 Lower 1.2720 Upper 1.380 3.77 <0.001
Religion
Non-muslim–Muslim Lower 0.0914 Upper 0.219 1.17 <0.001 0.00967 Lower −0.0616 Upper 0.101 1.02 0.634 4.21e-4 Lower −0.00271 Upper 0.197 1.10 0.057 0.00668 Lower −0.132 Upper 0.120 0.994 0.923 1.13e-5 Lower 0.0873 Upper 0.364 1.25 0.001 0.0110
Intercept Lower 3.032 Upper 3.108 21.541 <0.001 Lower 2.4695 Upper 2.570 12.43 <0.001 Lower 2.0418 Upper 2.1657 8.20 <0.001 Lower 1.719 Upper 1.8642 6.000 <0.001 Lower 1.463 Upper 1.627 4.689 <0.001
Marital status
Single–married Lower −0.207 Upper −0.113 0.852 <0.001 0.0193 Lower 0.0103 Upper 0.130 1.07 0.022 0.00993 Lower −0.0742 Upper 0.0745 1.00 0.997 2.44e-8 Lower −0.203 Upper −0.0257 0.892 0.011 0.00766 Lower −0.386 Upper −0.180 0.753 <0.001 0.0320
Intercept Lower 2.757 Upper 2.829 16.33 <0.001 Lower 2.5161 Upper 2.5975 12.89 <0.001 Lower 2.067 Upper 2.1683 8.311 <0.001 Lower 1.5475 Upper 1.678 5.02 <0.001 Lower 1.039 Upper 1.206 3.07 <0.001
Qualification
Masters–bachelors Lower 0.159 Upper 0.267 1.24 <0.001 0.0816 Lower −0.0639 Upper 0.0657 1.00 0.978 0.00406 Lower−0.114 Upper 0.0487 0.968 0.430 0.00126 Lower 0.0522 Upper 0.251 1.16 0.003 0.0216 Lower 0.136 Upper 0.383 1.30 <0.001 0.0861
Ph.D–bachelors Lower 0.274 Upper 0.398 1.40 <0.001 Lower −0.0247 Upper 0.1286 1.05 0.184 Lower −0.120 Upper 0.0766 0.979 0.667 Lower 0.0870 Upper 0.320 1.23 <0.001 Lower 0.348 Upper 0.620 1.62 <0.001
Post doc–bachelors Lower 0.344 Upper 0.494 1.52 <0.001 Lower −0.0648 Upper 0.1317 1.03 0.504 Lower −0.132 Upper 0.1171 0.993 0.908 Lower 0.0596 Upper 0.353 1.23 0.006 Lower 0.436 Upper 0.759 1.82 <0.001
Discussion

Toxoplasmosis is a major global zoonotic disease that has a deleterious effect on human health, with severe consequences in immunocompromised, pregnant women (10). Consumption of contaminated raw meat, water, fruits, and vegetables; contact with cats; and exposure to soil contaminated with cat feces are the main transmission routes (11). Out of 400 participants, 240 (60%) were aware of toxoplasmosis. Similar findings have been reported in Northeast Ethiopia (1).

Our study findings revealed that 87.3 and 85.5% of participants washed their hands after gardening and changing the cat litter, respectively. Additionally, 89% of participants thoroughly cooked meat prior to consumption, and 86.3% avoided drinking raw milk. A study from Ethiopia reported that among pregnant women, 77.6% washed their hands after gardening, 64.7% washed their hands after changing the cat litter, and 62.2% washed their hands after handling raw meat. Furthermore, 85.9% of the pregnant women reported that they did not avoid drinking untreated water (1). In our study, 80% of participants considered toxoplasmosis to be a dangerous disease, and 33.5% reported that they had not consumed undercooked meat. In contrast, a study reported that 51.4% of participants did not consider toxoplasmosis to be a severe disease. Additionally, 48% individuals were unsure whether toxoplasmosis was spread via consumption of inadequately washed vegetables (30). Our study showed that 81.8% of participants washed their kitchen utensils after contact with raw meat or unwashed fruits and vegetables. Similar findings were obtained in Brazil, where 24.7% of pregnant women reported washing kitchen utensils (31). Approximately 30% of the participants did not allow anyone else to change the cat litter box. Similar findings have been reported in a study conducted in Northeast Ethiopia where 51.3% women responded that they did not allow someone else to change the cat litter box (1).

Most of the participants (76.8%) reported that toxoplasmosis was acquired by consuming raw/undercooked meat. These findings were consistent with those of a study carried out in Mexico, where more than half of the respondents correctly defined the routes of transmission: (1) consumption of raw or undercooked foods, unwashed fruits and vegetables and (2) direct contact with cats (32). In our study, 69.5% of participants considered blood transfusion to be a cause of toxoplasmosis. In one of the surveys, 27.7% of the participants did not assume that blood transfusion could spread toxoplasmosis, and 38.5% believed that it could be transmitted from the mother to her fetus (33). Approximately 68.3% of participants responded that gardening without gloves could be a transmission source of toxoplasmosis. In a study conducted in the US, 29% of the participants thought that toxoplasmosis could be transmitted by gardening without gloves (34). Our study findings showed that immunocompromised pregnant women had a high risk of toxoplasmosis similar to the findings of Desta who reported there is a high risk of toxoplasmosis in immunocompromised, pregnant women (77.9%) (1). The majority (58%) of participants reported that toxoplasmosis is a zoonotic infection. A previous study reported that 33.82% of participants were aware that toxoplasmosis is a zoonotic disease (1).

Strength, Limitations, and Future Recommendations

The limited amount of knowledge about toxoplasmosis emphasized to provide and promote health education regarding toxoplasmosis especially awareness regarding transmission of disease in the pregnant women. It is important to improve primary health care system of the country for the better control, management, and prevention of the disease. Moreover, it is stressed that in the study population to commence health education and awareness campaigns for the community and to design relevant policies for the guidance of the government and stakeholders to reduce the risk of disease. In the study design, the use of close questionnaire is one of the limitation, where free form response was not allowed. In our study included the participants from university which is not representative of the situation of whole country. The strength of the study is maximum number of female participants and preliminary study on the knowledge about toxoplasmosis among university students in Pakistan.

 Materials and Methods Study Area

We conducted a cross-sectional analysis in Islamabad and Rawalpindi district of Punjab, Pakistan, also known as twin cities. The terrain consists of plains and mountains in the metropolitan area of Islamabad and Rawalpindi. In the mountainous terrain of Margala hills is the northern part of the metropolitan area, while Rawalpindi is situated on the Pothohar plateau (35).

 Participants

The study participants included students from universities of the twin cities that were enrolled in different degree programs (Bachelors, Masters, Ph.D., and Post doc). The sample size was calculated using Raosoft software (http://www.raosoft.com/samplesize.html; 5% margin of error, 95% confidence level, and 50% response distribution). Four hundred questionnaires were randomly distributed and filled by the participants. We collected data from July through December 2020.

 Sample Size

A questionnaire was designed to access the knowledge, attitude, practices, risk factor and one health regarding toxoplasmosis. A total of 400 questionnaires were administrated. The questionnaire was categories into the following sections as demography (n = 17), knowledge (n = 34), attitude (n = 19), practices (n = 11), risk factors (n = 8), and one health (n = 7).

 Data Collection

We developed a structured questionnaire to collect the data. After obtaining verbal informed consent from the participants, we conducted interviews. A team was trained for interviews, data collection, and record keeping. A supervisor routinely coordinated the interview process to ensure adequate data collection and record maintenance. The purpose of study was explained to the participants. The questionnaire consisted of six sections. The first section was on the socio-demographics of the participants. The second section was on the knowledge on toxoplasmosis, including common signs, symptoms, and diagnostic tests used for toxoplasmosis. The third section was on the attitudes and perceptions toward toxoplasmosis. The fourth section was on practices performed when toxoplasmosis was either suspected or diagnosed. The fifth section was on major risk factors of the disease, and the sixth section was on One Health questions regarding toxoplasmosis.

 Statistical Analysis

We generated a database using Excel (Microsoft, Redmond, WA, USA) and calculated basic frequencies. We used descriptive statistics to initially analyze the data and classified the variables into independent and dependent variables. We performed statistical analysis using Jamovi software (version 1.6.7; https://www.jamovi.org) to observe the factors involved in the occurrence of toxoplasmosis. The relationship between various factors influencing knowledge, attitudes, and practices was analyzed. For data analysis, we used Chi square test, one-way analysis of variance (ANOVA), and log-linear regression.

 Conclusions

There is a low level of knowledge and awareness regarding toxoplasmosis among males. Therefore, there should be awareness programs to educate individuals about the risks of this deadly disease and to provide information on the major routes of transmission. Our study highlights the need of toxoplasmosis awareness to reduce the burden and economic impact of the disease.

 Data Availability Statement

The original contributions presented in the study are included in the article/supplementary material, further inquiries can be directed to the corresponding author/s.

 Ethics Statement

The studies involving human participants were reviewed and approved by the Ethics Committee of COMSATS University. The patients/participants provided their written informed consent to participate in this study.

 Author Contributions

HA and KS designed and supervised the study. TM and KS performed the data collection. KS, SS, SA, MA, HA, and JC conducted statistical and data analysis. SN drafted the manuscript. SS and JC performed critical revisions. All authors read and approved the final manuscript.

 Funding

This study was supported by the Fifth Round of Three-Year Public Health Action Plan of Shanghai (Grant No. GWV-10.1-XK13 to JC), the National Natural Science Foundation of China (Grant Nos. 81772225 and 81971969 to JC), and the Key Laboratory of Parasite and Vector Biology, National Health Commission of People's Republic of China (Grant No. WSBKFKT2017-01). The funders had no role in the study design, the data collection and analysis, the decision to publish, or the preparation of the manuscript.

 Conflict of Interest

The authors declare that the research was conducted in the absence of any commercial or financial relationships that could be construed as a potential conflict of interest.

 Publisher's Note

All claims expressed in this article are solely those of the authors and do not necessarily represent those of their affiliated organizations, or those of the publisher, the editors and the reviewers. Any product that may be evaluated in this article, or claim that may be made by its manufacturer, is not guaranteed or endorsed by the publisher.

The authors are thankful to Kaleem Imdad and Naseer Shah for their assistance during the preparation of this manuscript.

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Abbreviations WHO

World Health Organization

 NZDs

Neglected Zoonotic Diseases

 T. gondii

Toxolasma gondii

 DALYs

Disability Adjusted Life Years.