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J Vet Clin 2023; 40(3): 197-202

https://doi.org/10.17555/jvc.2023.40.3.197

Published online June 30, 2023

Canine Lymphoma as a Possible Human Lymphoma Model: A Case-Series Study

Kiavash Hushmandi1 , Saied Bokaie1,* , Darioush Shirani2 , Ali Taghipour3

1Division of Epidemiology & Zoonoses, Department of Food Hygiene and Quality Control, Faculty of Veterinary Medicine, University of Tehran, Tehran, Iran
2Department of Small Animals Internal Medicine, Faculty of Veterinary Medicine, University of Tehran, Tehran, Iran
3Department of Veterinary Clinical Sciences, Karaj Branch, Islamic Azad University, Karaj, Iran

Correspondence to:*Sbokaie@ut.ac.ir

Received: April 22, 2023; Revised: May 15, 2023; Accepted: May 30, 2023

Copyright © The Korean Society of Veterinary Clinics.

Canine lymphoma (cL) is the most common hematopoietic cancer in dogs. Various determinants have been evaluated to find the predisposing factors in both human and canine lymphoma. Due to common risk factors and similar pathways, cL is considered a potential model for non-Hodgkin lymphoma (NHL) in humans. In this case-series study, major hospitals in Tehran consented to take part in this study and between the years of 2020-2022, provided us with 52 cL cases which were approved by the attended pathologist. We designed a questionnaire and collected information about the dogs and their owners. Most of the owners were women, young (younger than 50 years old), had at least diplomas and interestingly were housewives or househusbands. Male dogs with middle to old age (more than 6 years) were mostly referred. The most common characteristics were neutered, normal BCS, purebred, urban but not industrial residence, previous tobacco smoke exposure but no history of previous fungicide or pesticide exposure. Also, most of them did not have any previous autoimmune or immunosuppressive diseases. Presented characteristics should be considered risk determinants but to approve their validity, they should be further evaluated in epidemiological studies.

Keywords: canine lymphoma, case-series, tehran, human model.

Canine lymphoma (cL) encompass a wide variety of neoplasms with a common origin: lymphocytes. They mostly occur in lymphoid tissue, for example, bone marrow, lymph nodes, and spleen; but practically they can arise in any tissue (37). Due to the absence of a cancer registry in the veterinary field, its true incidence is somewhat vague. However, most studies confirm cL as the most common cancer of hematopoietic origin of dogs and top 3 most common canine neoplasms (31,37). cL accounts for 84% of all canine hematopoietic neoplasms and 7-24% of all canine neoplasms (17,23). Also, due to many shared molecular and clinical characteristics between cL and human non-Hodgkin lymphoma (NHL) (22), cL can be used as a NHL model. There are also other advantages offered by this model which includes spontaneous occurrence with no genetic engineering or isogenic background, lifespan adapted disease chronology, shared environment with humans, and capability to organize dogs into specific breeds to select for specific predisposition or homogenous genetic background (15). Also, breed purity was evaluated in one study but there was not any significant difference (32). There is strong evidence that indicates lymphoma incidence is increasing in both human and canine species (5). In a study at Purdue University from 1987-1997, referred cL cases to veterinary institutes increased from 0.75% to 2.0% of total case load (37). Additionally, NHL accounts for 5% of all new cancer cases, making it the second fastest growing cancer in terms of human mortality (16).

There are common etiologies between NHL and cL. Autoimmune diseases are considered as a risk factor in human (2) and dogs (19). Of infectious etiologies, there are reports of canine lymphotropic retroviruses linked to lymphoma (30,35). Also, there has been a report of a gamma herpes-like agent in 5 cases of B-cell lymphoma (14). Hepatitis B virus (42), Helicobacter pylori, Chlamydia psittaci, hepatitis C virus (39), EBV, and HIV (7) have been associated with NHL. Furthermore, age, sex, occupational exposure to dioxin or routine exposure of tobacco smoke have been appointed as risk factors of NHL (9). All of the mentioned factors are shown to be a cL risk factor (21,26,38).

Although cL can occur in B or T cells, it’s most common in B cells (40). B cell lymphoma is also the most common subtype of lymphoma in humans (31). The incidence increases with age and seems to be more prevalent in middle-sized to large breeds (40). Also, early neutralization (<1 years old) is suggested to increase the risk of cL in golden retriever (36) and vizsla (41), whereas no link was existed in Labrador Retriever (12). Generally, intact female dogs are less represented with cL (40). The etiology of cL can be grouped into 4, i.e., genetic and molecular factors, infectious factors, environmental factors, and immunologic factors. Gene deregulation of expression has been observed in lymphoma cases, for example, loss of canine chromosome 14 and gains of chromosome 13 and 31 was the most common anomaly is one study (34). Also, alteration of death pathways, epigenetic changes, and alteration in the expression of tumor suppressor genes is shared findings in both humans and dogs (6,24,33). Infectious origin of cL is not a confirmed or popular idea in literature, however, Epstein-Barr virus was detected in some of cL studies (4,14) and Helicobacter infections is associated with human gastric mucosa-associated lymphoid tissue (MALT) lymphoma. Using herbicides, especially phenoxyacetic acid herbicides, have been linked to NHL and cL occurrence (13,28,29,32). One case-control study showed with 4 or more years of herbicide application, the cL risk increases to two fold (37). However, follow up studies did not validate the results of the former study (3,10,18). In another case-control study, industrial area residence and chemical use (solvents and paints) increased the risk of cL. Albeit pesticide use did not show any relevance to incidence (11). Still there is one study that linked the use of pesticide to cL incidence but did not find any relation with flea or tick control products (32). Vicinity to environmental waste (21,25), exposure to strong magnetic fields (27), and exposure to tobacco smoke (26) are other reported environmental factors that also need further investigations to prove their association. Immune suppression, whether due to immunosuppressing disease or using immunosuppressive medication, is shown to have an association with human lymphoma and cL. Cyclosporin treatment in dogs (1) and autoimmune disease (37) has been linked to cL (19).

Since there are no previous epidemiological study in Iran regarding the occurrence of cL, in this study we aimed to evaluate determinants of cL, determine its occurrence, and if possible, suggest it as an animal model for NHL. This study was accomplished between 2020-2022 and cases were collected in certain major hospitals of Tehran metropolis.

In this case-series study, 52 cL cases were referred to the determined hospitals of Tehran between 2020-2022. Their lymphoma was confirmed by the attended pathologist. Before field stage, we designed a questionnaire to collect pet and owner information. Information about the pet dog included age of cancer diagnosis, sex, reproduction status, body condition score (BCS), breed purity, residence, having a history of fungicide and pesticide use, immunosuppressive diseases, and exposure to tobacco smoke. BCS was assessed on 1-3 scale, which is lean, normal, and overweight, respectively. We also collected age, sex, level of education, and occupation of pet owners. Pet owners were divided into 5 age groups, 4 education and occupational groups. Immunohistochemistry was implemented to evaluate BCL2 expression at Imam hospital.

Of 52 cases and relevant pet owners, 32 (61.5%) were woman and 20 (38.5%) were men. Other demographic information is represented in Table 1.

Table 1 Demographic information of pet owners

Age (year)No.EducationNo.OccupationNo.
<4021 (40.4%)None19 (36.5%)None12 (23%)
41-5019 (36.6%)Primary4 (7.7%)Clerk6 (11.5%)
51-607 (13.5%)Diploma21 (40.4%)Housewife/husband24 (46%)
61-703 (5.5%)Bachelor and higher8 (15.4%)Self-employed10 (19.5%)
>702 (4%)----


Age of dogs were classified into 4 groups, which is shown in Fig. 1. Most of the referred cases were older than 6 years old.

Figure 1.Age of dogs at diagnosis (years old).

Results of sex and reproduction status is presented in Table 2. Neutered cases and males were overrepresented.

Table 2 Sex and reproduction status

SexNo.Reproduction statusNo.
Male28 (54%)Intact23 (44%)
Female24 (46%)Neutered29 (56%)


Table 3 represents measured criteria of all cases. Normal body, purebred, urban and non-industrial residence, no history of fungicide or pesticide use and immunosuppressive diseases, exposure to tobacco smoke and BCL2 expression were more referred.

Table 3 Evaluated criteria

CriteriaDivisionsNo.
BCS19 (17.3%)
230 (57.7%)
313 (25%)
BreedPure32 (61.5%)
Mix20 (38.5%)
Location of residenceSuburb17 (32.7%)
Urban26 (50%)
Rural9 (17.3%)
Residence in industrial areasYes11 (21%)
No41 (79%)
Fungicide useYes17 (32.7%)
No35 (67.3%)
PesticideYes20 (38.5%)
No32 (61.5%)
History of immunosuppressive diseaseYes13 (25%)
No39 (75%)
Exposure to tobacco smokeYes31 (60%)
No21 (40%)
BCL2 expressionYes33 (63.5%)
No19 (36.5%)

Individuals with diploma or more education (55.8% cumulative) comprised most of the referred cases. It seems that people with higher levels of education tend to be more sensitive on the well-being of their pets, but this matter has yet to be further investigated. Also, most of the pet owners were housewives/husbands (46%). May be this is because they have more interaction with their pets and have more compassion towards them. However, this should be further studied. Also, most of the pet owners were young (<50 years old; 77%).

Like any other type of cancer cL incidence raises with age, which is why it is more reported in middle-aged to older dogs (37). However, T-cell lymphoma has been observed at a lower age range (8). It is reported that cL rates in younger than one-year olds are approximately 1.5 cases per 100,000 dogs and 84 cases per 100,000 dogs for more than 10-years old dogs. In our study, most of the affected dogs were in the range of 6-9 years old (42.3%), which is in the agreement with previous data (8,37).

Sex is not proven to be a predisposition factor, yet intact females have reduced cL reports (38). Early neutralization (<1 year) has had various results on different breeds. Golden Retriever (36) and Vizsla (41) have increased incidence rates with early neutralization, while Labrador Retriever does not (12). Interestingly, women also have lower rates of NHL incidence than men (20) and NHL incidence in women increases at the age of 50 when menopause is usually reached. Thus, we can conclude that female hormones may be protective against lymphoma in both humans and dogs. Males (54%) and neutered (56%) dogs were slightly overrepresented in our study. Also, most of the referred dogs had normal body condition scores (57.7%).

Although having an urban residence is not shown to affect cL (32), living in industrial areas has been shown to impact cL incidence (11). Most of the referred cases of our study were from urban (50%) and non-industrial (79%) areas. The fact that the location of this study is not near industrial areas can explain why four fifth of referred cases are from non-industrial areas and other factors must have been effective in the occurrence of their cL.

Anti-apoptotic BCL-2 gene is one of the main studied genes occurring in cL cases. In our study, 63.5% of cases were detected as positive. According to the review study of Thomas et al. (33), BCL2 positivity varies with breed types, although they were mostly more than 50% positive, and our results are in the line with their results.

Most of the cases did not have a history of immune suppression diseases (75%). While a dysfunctional immune system or an autoimmune disease has been proven to have positive interference in developing cL (40), we suspect other factors caused the incidence of lymphoma in our cases.

One recent study indicated tobacco exposure can elevate the risk of cL incidence (26). In our study also most of the referred cases were exposed to tobacco smoke (60%), suggesting this factor as a probable cause of the referred cases. Since this study is a case series and only referred cases are recorded without any respective control group for comparison, findings may be random, and no definitive result can be extracted from the results.

Using fungicide (32.7%) and pesticide (38.5%) were not common in our cases. However, fungicides and pesticides use are shown to increase the risk of developing lymphoma (32). In one study pesticide use was not effective in cL incidence (11). Based on this information, we can conclude using fungicide and pesticide had minor effects in developing cL among the referred cases. In conclusion in two years of our study, most of the cases were presented after 6 years old (73%) and were predominantly males (54%). Most represented intrinsic characteristics included neutered, purebred, male, normal BCS, and having no history of immunosuppressive diseases. Among environmental factors, dogs with urban and no industrial residence, with no previous exposure to fungicides and pesticides consisted of most of the referred cases. However, most dogs had previous tobacco smoke exposure. Since we did not have any control subject to determine OR, we cannot state these factors as risk factors but their probable risk should be evaluated in further epidemiological studies.

The paper was extracted from the PhD. thesis of the first author, Department of Food Hygiene and Quality Control, Faculty of Veterinary Medicine, University of Tehran.

This study was approved by the Ethics Committee of the University of Tehran (Code: IR.UT.VETMED.REC.1401.003).

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Article

Original Article

J Vet Clin 2023; 40(3): 197-202

Published online June 30, 2023 https://doi.org/10.17555/jvc.2023.40.3.197

Copyright © The Korean Society of Veterinary Clinics.

Canine Lymphoma as a Possible Human Lymphoma Model: A Case-Series Study

Kiavash Hushmandi1 , Saied Bokaie1,* , Darioush Shirani2 , Ali Taghipour3

1Division of Epidemiology & Zoonoses, Department of Food Hygiene and Quality Control, Faculty of Veterinary Medicine, University of Tehran, Tehran, Iran
2Department of Small Animals Internal Medicine, Faculty of Veterinary Medicine, University of Tehran, Tehran, Iran
3Department of Veterinary Clinical Sciences, Karaj Branch, Islamic Azad University, Karaj, Iran

Correspondence to:*Sbokaie@ut.ac.ir

Received: April 22, 2023; Revised: May 15, 2023; Accepted: May 30, 2023

This is an open access article distributed under the terms of the Creative Commons Attribution Non-Commercial License (http://creativecommons.org/licenses/by-nc/4.0) which permits unrestricted non-commercial use, distribution, and reproduction in any medium, provided the original work is properly cited.

Abstract

Canine lymphoma (cL) is the most common hematopoietic cancer in dogs. Various determinants have been evaluated to find the predisposing factors in both human and canine lymphoma. Due to common risk factors and similar pathways, cL is considered a potential model for non-Hodgkin lymphoma (NHL) in humans. In this case-series study, major hospitals in Tehran consented to take part in this study and between the years of 2020-2022, provided us with 52 cL cases which were approved by the attended pathologist. We designed a questionnaire and collected information about the dogs and their owners. Most of the owners were women, young (younger than 50 years old), had at least diplomas and interestingly were housewives or househusbands. Male dogs with middle to old age (more than 6 years) were mostly referred. The most common characteristics were neutered, normal BCS, purebred, urban but not industrial residence, previous tobacco smoke exposure but no history of previous fungicide or pesticide exposure. Also, most of them did not have any previous autoimmune or immunosuppressive diseases. Presented characteristics should be considered risk determinants but to approve their validity, they should be further evaluated in epidemiological studies.

Keywords: canine lymphoma, case-series, tehran, human model.

Introduction

Canine lymphoma (cL) encompass a wide variety of neoplasms with a common origin: lymphocytes. They mostly occur in lymphoid tissue, for example, bone marrow, lymph nodes, and spleen; but practically they can arise in any tissue (37). Due to the absence of a cancer registry in the veterinary field, its true incidence is somewhat vague. However, most studies confirm cL as the most common cancer of hematopoietic origin of dogs and top 3 most common canine neoplasms (31,37). cL accounts for 84% of all canine hematopoietic neoplasms and 7-24% of all canine neoplasms (17,23). Also, due to many shared molecular and clinical characteristics between cL and human non-Hodgkin lymphoma (NHL) (22), cL can be used as a NHL model. There are also other advantages offered by this model which includes spontaneous occurrence with no genetic engineering or isogenic background, lifespan adapted disease chronology, shared environment with humans, and capability to organize dogs into specific breeds to select for specific predisposition or homogenous genetic background (15). Also, breed purity was evaluated in one study but there was not any significant difference (32). There is strong evidence that indicates lymphoma incidence is increasing in both human and canine species (5). In a study at Purdue University from 1987-1997, referred cL cases to veterinary institutes increased from 0.75% to 2.0% of total case load (37). Additionally, NHL accounts for 5% of all new cancer cases, making it the second fastest growing cancer in terms of human mortality (16).

There are common etiologies between NHL and cL. Autoimmune diseases are considered as a risk factor in human (2) and dogs (19). Of infectious etiologies, there are reports of canine lymphotropic retroviruses linked to lymphoma (30,35). Also, there has been a report of a gamma herpes-like agent in 5 cases of B-cell lymphoma (14). Hepatitis B virus (42), Helicobacter pylori, Chlamydia psittaci, hepatitis C virus (39), EBV, and HIV (7) have been associated with NHL. Furthermore, age, sex, occupational exposure to dioxin or routine exposure of tobacco smoke have been appointed as risk factors of NHL (9). All of the mentioned factors are shown to be a cL risk factor (21,26,38).

Although cL can occur in B or T cells, it’s most common in B cells (40). B cell lymphoma is also the most common subtype of lymphoma in humans (31). The incidence increases with age and seems to be more prevalent in middle-sized to large breeds (40). Also, early neutralization (<1 years old) is suggested to increase the risk of cL in golden retriever (36) and vizsla (41), whereas no link was existed in Labrador Retriever (12). Generally, intact female dogs are less represented with cL (40). The etiology of cL can be grouped into 4, i.e., genetic and molecular factors, infectious factors, environmental factors, and immunologic factors. Gene deregulation of expression has been observed in lymphoma cases, for example, loss of canine chromosome 14 and gains of chromosome 13 and 31 was the most common anomaly is one study (34). Also, alteration of death pathways, epigenetic changes, and alteration in the expression of tumor suppressor genes is shared findings in both humans and dogs (6,24,33). Infectious origin of cL is not a confirmed or popular idea in literature, however, Epstein-Barr virus was detected in some of cL studies (4,14) and Helicobacter infections is associated with human gastric mucosa-associated lymphoid tissue (MALT) lymphoma. Using herbicides, especially phenoxyacetic acid herbicides, have been linked to NHL and cL occurrence (13,28,29,32). One case-control study showed with 4 or more years of herbicide application, the cL risk increases to two fold (37). However, follow up studies did not validate the results of the former study (3,10,18). In another case-control study, industrial area residence and chemical use (solvents and paints) increased the risk of cL. Albeit pesticide use did not show any relevance to incidence (11). Still there is one study that linked the use of pesticide to cL incidence but did not find any relation with flea or tick control products (32). Vicinity to environmental waste (21,25), exposure to strong magnetic fields (27), and exposure to tobacco smoke (26) are other reported environmental factors that also need further investigations to prove their association. Immune suppression, whether due to immunosuppressing disease or using immunosuppressive medication, is shown to have an association with human lymphoma and cL. Cyclosporin treatment in dogs (1) and autoimmune disease (37) has been linked to cL (19).

Since there are no previous epidemiological study in Iran regarding the occurrence of cL, in this study we aimed to evaluate determinants of cL, determine its occurrence, and if possible, suggest it as an animal model for NHL. This study was accomplished between 2020-2022 and cases were collected in certain major hospitals of Tehran metropolis.

Materials and Methods

In this case-series study, 52 cL cases were referred to the determined hospitals of Tehran between 2020-2022. Their lymphoma was confirmed by the attended pathologist. Before field stage, we designed a questionnaire to collect pet and owner information. Information about the pet dog included age of cancer diagnosis, sex, reproduction status, body condition score (BCS), breed purity, residence, having a history of fungicide and pesticide use, immunosuppressive diseases, and exposure to tobacco smoke. BCS was assessed on 1-3 scale, which is lean, normal, and overweight, respectively. We also collected age, sex, level of education, and occupation of pet owners. Pet owners were divided into 5 age groups, 4 education and occupational groups. Immunohistochemistry was implemented to evaluate BCL2 expression at Imam hospital.

Results

Of 52 cases and relevant pet owners, 32 (61.5%) were woman and 20 (38.5%) were men. Other demographic information is represented in Table 1.

Table 1 . Demographic information of pet owners.

Age (year)No.EducationNo.OccupationNo.
<4021 (40.4%)None19 (36.5%)None12 (23%)
41-5019 (36.6%)Primary4 (7.7%)Clerk6 (11.5%)
51-607 (13.5%)Diploma21 (40.4%)Housewife/husband24 (46%)
61-703 (5.5%)Bachelor and higher8 (15.4%)Self-employed10 (19.5%)
>702 (4%)----


Age of dogs were classified into 4 groups, which is shown in Fig. 1. Most of the referred cases were older than 6 years old.

Figure 1. Age of dogs at diagnosis (years old).

Results of sex and reproduction status is presented in Table 2. Neutered cases and males were overrepresented.

Table 2 . Sex and reproduction status.

SexNo.Reproduction statusNo.
Male28 (54%)Intact23 (44%)
Female24 (46%)Neutered29 (56%)


Table 3 represents measured criteria of all cases. Normal body, purebred, urban and non-industrial residence, no history of fungicide or pesticide use and immunosuppressive diseases, exposure to tobacco smoke and BCL2 expression were more referred.

Table 3 . Evaluated criteria.

CriteriaDivisionsNo.
BCS19 (17.3%)
230 (57.7%)
313 (25%)
BreedPure32 (61.5%)
Mix20 (38.5%)
Location of residenceSuburb17 (32.7%)
Urban26 (50%)
Rural9 (17.3%)
Residence in industrial areasYes11 (21%)
No41 (79%)
Fungicide useYes17 (32.7%)
No35 (67.3%)
PesticideYes20 (38.5%)
No32 (61.5%)
History of immunosuppressive diseaseYes13 (25%)
No39 (75%)
Exposure to tobacco smokeYes31 (60%)
No21 (40%)
BCL2 expressionYes33 (63.5%)
No19 (36.5%)

Discussion

Individuals with diploma or more education (55.8% cumulative) comprised most of the referred cases. It seems that people with higher levels of education tend to be more sensitive on the well-being of their pets, but this matter has yet to be further investigated. Also, most of the pet owners were housewives/husbands (46%). May be this is because they have more interaction with their pets and have more compassion towards them. However, this should be further studied. Also, most of the pet owners were young (<50 years old; 77%).

Like any other type of cancer cL incidence raises with age, which is why it is more reported in middle-aged to older dogs (37). However, T-cell lymphoma has been observed at a lower age range (8). It is reported that cL rates in younger than one-year olds are approximately 1.5 cases per 100,000 dogs and 84 cases per 100,000 dogs for more than 10-years old dogs. In our study, most of the affected dogs were in the range of 6-9 years old (42.3%), which is in the agreement with previous data (8,37).

Sex is not proven to be a predisposition factor, yet intact females have reduced cL reports (38). Early neutralization (<1 year) has had various results on different breeds. Golden Retriever (36) and Vizsla (41) have increased incidence rates with early neutralization, while Labrador Retriever does not (12). Interestingly, women also have lower rates of NHL incidence than men (20) and NHL incidence in women increases at the age of 50 when menopause is usually reached. Thus, we can conclude that female hormones may be protective against lymphoma in both humans and dogs. Males (54%) and neutered (56%) dogs were slightly overrepresented in our study. Also, most of the referred dogs had normal body condition scores (57.7%).

Although having an urban residence is not shown to affect cL (32), living in industrial areas has been shown to impact cL incidence (11). Most of the referred cases of our study were from urban (50%) and non-industrial (79%) areas. The fact that the location of this study is not near industrial areas can explain why four fifth of referred cases are from non-industrial areas and other factors must have been effective in the occurrence of their cL.

Anti-apoptotic BCL-2 gene is one of the main studied genes occurring in cL cases. In our study, 63.5% of cases were detected as positive. According to the review study of Thomas et al. (33), BCL2 positivity varies with breed types, although they were mostly more than 50% positive, and our results are in the line with their results.

Most of the cases did not have a history of immune suppression diseases (75%). While a dysfunctional immune system or an autoimmune disease has been proven to have positive interference in developing cL (40), we suspect other factors caused the incidence of lymphoma in our cases.

One recent study indicated tobacco exposure can elevate the risk of cL incidence (26). In our study also most of the referred cases were exposed to tobacco smoke (60%), suggesting this factor as a probable cause of the referred cases. Since this study is a case series and only referred cases are recorded without any respective control group for comparison, findings may be random, and no definitive result can be extracted from the results.

Using fungicide (32.7%) and pesticide (38.5%) were not common in our cases. However, fungicides and pesticides use are shown to increase the risk of developing lymphoma (32). In one study pesticide use was not effective in cL incidence (11). Based on this information, we can conclude using fungicide and pesticide had minor effects in developing cL among the referred cases. In conclusion in two years of our study, most of the cases were presented after 6 years old (73%) and were predominantly males (54%). Most represented intrinsic characteristics included neutered, purebred, male, normal BCS, and having no history of immunosuppressive diseases. Among environmental factors, dogs with urban and no industrial residence, with no previous exposure to fungicides and pesticides consisted of most of the referred cases. However, most dogs had previous tobacco smoke exposure. Since we did not have any control subject to determine OR, we cannot state these factors as risk factors but their probable risk should be evaluated in further epidemiological studies.

Source of Funding

The paper was extracted from the PhD. thesis of the first author, Department of Food Hygiene and Quality Control, Faculty of Veterinary Medicine, University of Tehran.

Ethical Considerations

This study was approved by the Ethics Committee of the University of Tehran (Code: IR.UT.VETMED.REC.1401.003).

Acknowledgements

We would like to thank all individuals who helped us in the process of producing this paper.

Conflicts of Interest

The authors have no conflicting interests.

Author Contribution

All authors equally contributed to preparing this article.

Fig 1.

Figure 1.Age of dogs at diagnosis (years old).
Journal of Veterinary Clinics 2023; 40: 197-202https://doi.org/10.17555/jvc.2023.40.3.197

Table 1 Demographic information of pet owners

Age (year)No.EducationNo.OccupationNo.
<4021 (40.4%)None19 (36.5%)None12 (23%)
41-5019 (36.6%)Primary4 (7.7%)Clerk6 (11.5%)
51-607 (13.5%)Diploma21 (40.4%)Housewife/husband24 (46%)
61-703 (5.5%)Bachelor and higher8 (15.4%)Self-employed10 (19.5%)
>702 (4%)----

Table 2 Sex and reproduction status

SexNo.Reproduction statusNo.
Male28 (54%)Intact23 (44%)
Female24 (46%)Neutered29 (56%)

Table 3 Evaluated criteria

CriteriaDivisionsNo.
BCS19 (17.3%)
230 (57.7%)
313 (25%)
BreedPure32 (61.5%)
Mix20 (38.5%)
Location of residenceSuburb17 (32.7%)
Urban26 (50%)
Rural9 (17.3%)
Residence in industrial areasYes11 (21%)
No41 (79%)
Fungicide useYes17 (32.7%)
No35 (67.3%)
PesticideYes20 (38.5%)
No32 (61.5%)
History of immunosuppressive diseaseYes13 (25%)
No39 (75%)
Exposure to tobacco smokeYes31 (60%)
No21 (40%)
BCL2 expressionYes33 (63.5%)
No19 (36.5%)

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Vol.41 No.3 June 2024

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