Fungal isolation in a veterinary hospital environment and evaluation of environmental disinfectionAbstract
The presence of fungi in veterinary hospital environments is a constant concern, due to the ability of these organisms to cause infections in animals that frequent them and in humans who work there. This study aimed to investigate the presence and diversity of fungi in a veterinary hospital environment, especially on objects originating from the Pre-anesthesia Medication Room (PMR) and the Surgical Center (SC) of a university veterinary clinic. Samples were collected from objects belonging to these environments and used for the isolation and purification of fungi, before and immediately after the hygiene and disinfection procedure of the environment. A total of 115 colonies were isolated, 88 (76.5%) in the PMR and 27 (23.5%) in the SC. Of these, 74 (64.3%) were isolated before cleaning (53.0-71.6% in PMR and 21.0-28.4% in SC) and 41 (35.7%) after cleaning (35.0-85.4% in PMR and 6-14.6% in SC). Eleven genera were identified, the most prevalent being Trichophyton spp. (53.9%), Microsporum spp. (18.3%) and Cladosporium spp. (11.3%). The diversity, uniformity, and richness of fungal species were higher in PMR after cleaning (1-D = 0.69; H’ = 1.433; DMg = 1.406) and in SC before cleaning (1-D = 0.7892; H’ = 1.76; DMg = 1.642). The Wilcoxon test did not show any statistically significant difference before and after cleaning, thus demonstrating that cleaning is not being efficient in both environments. Cleaning was shown to be inefficient in both environments. It is essential to establish standards for diluting antiseptics, perform internal quality controls through frequent microbiological tests, and conduct periodic training, thus ensuring greater patient safety.
Keywords:
anemophiles; dermatophytes; surgical center; veterinary clinic
Resumo
A presença de fungos em ambientes hospitalares veterinários é uma preocupação constante, devido à capacidade desses organismos causarem infecções em animais que frequentam e nos seres humanos que laboram no local. O objetivo desse estudo foi investigar a presença e a diversidade de fungos em ambiente veterinário hospitalar, especialmente em objetos oriundos da sala de medicação pré-anestésica (MPA) e do centro cirúrgico (CC) de uma clínica veterinária universitária. As amostras foram coletadas de objetos pertencentes a esses ambientes e empregadas para o isolamento e purificação de fungos, antes e logo após o procedimento de higiene e desinfecção do ambiente. Foram isoladas 115 colônias sendo 88 (76,5%) na MPA e 27 (23,5%) no CC. Destas, 74 (64,3%) foram isoladas antes da limpeza (53-71,6% na MPA e 21-28,4% no CC) e 41 (35,7%) após a limpeza (35-85,4% na MPA e 6-14,6% no CC). Foram identificados 11 gêneros sendo os mais prevalentes Trichophyton spp. (53,9%), Microsporum spp. (18,3%) e Cladosporium spp. (11,3%). A diversidade, a uniformidade e a riqueza de espécies fúngicas foi maior na MPA após a limpeza (1-D = 0,69; H’ = 1,433; DMg = 1,406) e no CC antes da limpeza (1-D = 0,7892; H’ = 1,76; DMg = 1,642). O teste de Wilcoxon não demonstrou diferença estatística significativa antes e após a limpeza, demonstrando assim que a limpeza não está sendo eficiente nos ambientes. A limpeza mostrou-se ineficiente em ambos os ambientes. É essencial estabelecer padrões para a diluição de antissépticos, realizar controles de qualidade internos por meio de ensaios microbiológicos frequentes e conduzir capacitações periódicas, garantindo assim maior segurança aos pacientes.
Palavras-chave:
anemófilos; dermatófitos; centro cirúrgico; clínica veterinária
1. Introduction
Fungi are eukaryotic, ubiquitous, heterotrophic, unicellular, and/or multicellular organisms that can remain viable for long periods in ambient air or on surfaces (Lima et al., 2017). They are widely found in nature, and their conidia and fragments of vegetative mycelium become viable portions of these organisms during the process of aerial dissemination, and can be found in the air, water, soil, domestic and wild animals, surfaces, excreta, and various foods such as dairy products, beverages and cheeses (Mezzari et al., 2003; Carmo et al., 2017). Therefore, the proliferation of fungi in biological systems is an important issue for public health, since many of these infections refer to resistant microorganisms (Garcia et al., 2013).
The presence of fungi in veterinary hospital environments is a constant concern due to their ability to cause animal infections and diseases (Silva et al., 2023). In hospital environments, the concentration of fungi is higher due to the presence of diseases, organic materials, and conditions favorable to their growth (Hofling and Gonçalves, 2016). Among the different types of fungi, filamentous fungi are particularly relevant in veterinary hospital environments and can be found on several surfaces, such as walls, floors, and medical equipment (Santos et al., 2007; Cordeiro et al., 2021). This situation becomes more complex since there are no disinfection protocols in veterinary environments developed by the Ministry of Livestock, Agriculture, and Livestock, as is the case in human health services (Brasil, 2012).
The transmission of the fungi occurs through direct contact with the infected animal, contaminated objects, or even through the air. In a veterinary hospital environment, where there is a large circulation of people and animals, the presence of pathogenic fungi increases the risk of infections and complications for patients. In addition, these fungi may be resistant to conventional antifungal treatments, making the control and prevention of these infections even more challenging (Silva et al., 2023).
The genera with the highest prevalence in health units are Aspergillus and Penicillium, which are considered anemophilous (Cordeiro et al., 2021), that is, they are dispersed through the air. They are carried by the wind and enter the hospital environment through windows, doors and ventilation systems. Once inside the hospital, they settle on surfaces and multiply, posing a risk to the health of animals (Silva et al., 2023). It is important to emphasize that these airborne fungi are potentially dangerous and can cause allergies, respiratory diseases, meningitis, mycoses, and invasive and contagious infections (Oliveira et al., 2016). In general, animals are hosts to various fungal species, including, for example, dermatophytes, which colonize the skin, nails, hair, or even internal organs, causing zoonotic infections (Bonaccorsi, 2019).
The presence of fungi can be an indication of health problems, requiring treatment, since without adequate therapy these animals contribute to the spread of the disease in veterinary hospital environments (Silva et al., 2023). It is worth mentioning that even non-pathogenic fungi, which are present in the environment, can cause harm to the health of an immunocompromised organism, as is the case of aspergillosis, caused by the genus Aspergillus (Silva et al., 2017). Therefore, this work aims to identify fungi isolated from objects belonging to a veterinary hospital environment and verify whether the disinfection procedure is effective.
2. Materials and Methods
2.1. Characterization and collection site
This is an experimental, descriptive, cross-sectional study conducted at a university veterinary clinic located in Araguaína, northern Tocantins, Brazil (-7.08151º S, -48.19898º W). This clinic serves the population of the municipality by offering clinical and surgical care services, performing diagnostic imaging, and clinical pathology exams.
2.2. Environmental disinfection
Regarding the sanitizing agents used, 70.0% alcohol Start® is the standard for medical materials containing stainless steel and countertops; quaternary ammonia Vet+20® 1:50 is used on floors, walls, and ceilings; the chemical sanitizing agent based on benzalkonium chloride Vet+600® is also used to clean floors and windows.
2.3. Sample collection and processing
Samples were collected from objects from two environments of the university veterinary clinic: Pre-anesthesia Medication Room (PMR) and Surgical Center (SC), during the rainy season between March and May 2022 – whose average relative humidity was 84.7% and 73.2%, respectively (INMET, 2023). Objects that were handled most by professionals, patients and companions were strategically selected. The following objects were sampled from the PMR: cabinet, doorknob, grooming machine, SC support table, patient table, and squeeze bottle; and from the SC: cabinet, silicone breathing balloon, trachea, patient table, squeeze bottle, and door. The justification for collecting samples from the SC door is based on the absence of doorknobs, as in the PMR. The samples were collected on a single day, per sector, with one sample collected from each object before and another immediately after cleaning the site.
The samples were obtained with sterile swabs soaked in 0.85% saline solution, which was rubbed on the surface of the object and deposited in properly identified test tubes containing Brain Heart Infusion Broth (BHI) (Brasil, 2013). The area collected from the object was 10% of the size of the surface, not exceeding 100 cm2; in cases where the surface was reduced, a sample of the entire area was collected. The samples were then sent to the Laboratory of Hygiene and Public Health of the Universidade Federal do Norte do Tocantins (UFNT) in Araguaína – TO, Brazil, for processing.
2.4. Sample processing
The samples were subcultured by stripping onto Petri dishes containing Sabouraud dextrose agar (SDA) supplemented with chloramphenicol. They were incubated for 10 days at a temperature of 25±2 °C with daily observation to verify the growth of filamentous fungi. At the end of the incubation period, a count of colony-forming units (CFU) was performed.
2.5. Isolation and Identification
The fungi were isolated through successive subcultures until a pure culture was obtained, incubating the plates at 25 ± 2 °C, for five to ten day (Saleem et al., 2018; Silva et al., 2023). The macroscopic characterization was performed (Brasil, 2013) by grouping the colonies into morphotypes. From each object in the analyzed environments, one representative for every five identical morphotypes was subjected to the microcultivation technique according to Riddell (1950) for microscopic analysis, to visualize and identify the lowest taxonomic level of the fungus by comparing the visualized structures with those available in the literature (Pizzirani Kleiner et al., 1998; Alcântara et al., 2001; Faia, 2011, Brasil, 2013).
2.6. Statistical analyses
The percentage of CFU found per environment, object, and genus was evaluated. In addition, the Wilcoxon Matched-Pairs Test was performed to assess whether the mean population ranks before and after cleaning differed. The OpenEpi program was also used to evaluate the distribution of fungal frequency. To quantify the diversity and richness of the samples, the alpha diversity indices were calculated – Simpson Index of Diversity (1-D), Shannon (H), and Margalef (DMg) diversity (Simpson, 1949; Shannon, 1948; Hammer et al., 2001), calculated in the PAST program version 4.0.
3. Results and Discussion
A total of 115 CFU were isolated, 88 (76.5%) from PMR and 27 (23.5%) from SC, 16 different morphotypes and 10 distinct genera, the most prevalent being Trichophyton (62 CFU, 54.0%), Microsporum (21 CFU, 18.3%) and Cladosporium (13 CFU, 11.3%) (Table 1).
Fungal isolated from objects originating from the pre-anesthetic medication room and surgical center of a university veterinary clinic in northern Tocantins, ranked by quantity of CFU of each morphotype identified, before and after cleaning the environment, in the year 2022.
In PMR, before cleaning, 53 CFU with six morphotypes and four genera were isolated, the most prevalent being Trichophyton spp. with 35 CFU (66.0%), Microsporum spp. (14 CFU, 26.4%) and Cladosporium spp. (3 CFU, 5.7%). After cleaning, 35 CFU with six morphotypes and six genera were isolated, of which the most prevalent were Trichophyton (17 CFU, 48.6%), Cladosporium and Microsporum with seven CFU (20.0%) each. It was possible to observe a decrease in CFU, the number of morphotypes remained the same, but there was a greater quantity of genera identified after cleaning. Although hygiene and disinfection reduced the quantity of isolated fungi, two genera were found only after cleaning, Acremonium and Epidermophyton. A possible explanation for the situation is that during the cleaning procedure, these fungi may have been carried from other objects where collections were not performed, where cleaning was performed incorrectly, or even after cleaning the floor leading to the suspension of fungal spores.
In the SC before cleaning, 21 CFU with eight mold types and six genera were isolated, with the most prevalent being Trichophyton and Aspergillus, both with 30.0% (6 CFU) each. After cleaning, six CFU were isolated, with three morphotypes and two genera: Trichophyton with four CFU (66.7%) and Penicillium with two CFU (33.2%). Some fungi only grew in one environment, such as Curvularia spp. and Aspergillus spp., which were isolated only in the SC. On the other hand, only in the PMR there was growth of Acremonium spp. and Epidermophyton spp. It is clear that in the SC there was a greater reduction in the amount of CFU and genera compared to the PMR. The SC is a place where there is greater restriction on the movement of people and, because it performs more invasive procedures, it can raise greater concern among both cleaning staff and veterinary professionals and technicians who perform surface disinfection procedures on objects more cautiously and diligently. Despite this, it is important to pay attention to the presence of fungi that were found exclusively in the SC, such as Aspergillus spp., Curvularia spp. and Microsporum spp., because several invasive procedures are performed there and can contaminate and aggravate the animal's health condition. The absence of these fungi in the PMR does not determine their absence in the environment; it only indicates that there was no isolation of these genera in the objects observed (Saleem et al., 2018).
There are disinfectant materials that can contribute to the inefficiency of the cleaning process, especially if cleaning cloths are reused on contaminated surfaces. In a systematic analysis carried out in the state of Tocantins by Lourenzo et al. (2020), only 14.3% of cleaning of human hospital surfaces occurs with disposable cloths, which would be more recommended for applying cleaning and disinfection products. Cross-contamination also occurs due to the lack of hand hygiene among health professionals, who can carry microorganisms from one environment to another. In the case of the SC, the use of sterile surgical gloves also reduces this type of contamination, which occurs at a frequency of 13.0% to 34.6% (Gonçalves et al., 2016). Considering the amount of Trichophyton spp. identified in the PMR room and in the SC, this occurrence can be explained by the ability of dogs to carry dermatophyte fungi even when they are apparently healthy, after all, these pathologies have a highly contagious nature and great importance for public health, since they are zoonoses (Paryuni et al., 2020). Overall, 59.1% of the fungi isolated in the PMR correspond to the genus Trichophyton, while in the SC the percentage of Trichophyton drops to 37.0%. If all dermatophyte fungi are considered in both environments, the values reach 84 CFU (73.0%), since these genera are widely present in domestic animals (Subelj et al., 2014), as is the case of Microsporum canis, which in addition to dogs, is also endemic in felines. Most young animals may be clinically affected, but adults may be asymptomatic (Hermoso de Mendoza et al., 2010; Costa et al., 2013).
Similarly, epidemiologically, there are species of Trichophyton such as Trichophyton mentagrophytes that are frequently present in rodents, dogs, horses, and other animals (Lagowski et al., 2019). Another predominant class observed in this study is the anemophilous fungi: Aspergillus, Cladosporium, Curvularia, Fusarium, and Penicillium, with 27 CFU (23.5%). These fungi have high atmospheric dispersion facilitated by their spores and easy cultivation (Sobral, 2023), a characteristic that justifies such results. Together, dermatophytes and anemophiles correspond to 96.5% of the fungi found.
In human hospitals, the most commonly found filamentous fungi are mainly from the genera Aspergillus, Penicillium, and Cladosporium (Morais et al., 2016). It is possible to observe in other studies such as that of Lobato et al. (2009) that the presence of the genus Cladosporium and Aspergillus spp are common in human hospital environments. In this study, analyses of the ambient air of a hospital in Rio Grande do Sul were performed and 75.0% of the findings corresponded to Cladosporium. The present study also observed CFUs of the genus Cladosporium that were possibly dispersed in the ambient air of the PRM. It is worth mentioning that one of the hypotheses for this contamination may be related to the lack of routine cleaning of the air conditioning. The genus Cladosporium was also found in samples collected from the surface of the door and oil pan of the SC.
Based on studies such as these, it is clear how important the cleaning team and healthcare professionals are to properly sanitize the surgical center environment. However, there is little description in the literature about the cleaning of pre-surgical environments and few microbiological analyses in these environments, especially with fungi in a veterinary environment (Paula et al., 2017).
Regarding the values found in the evaluated indexes, it is possible to observe greater diversity in terms of species richness in the PMR after cleaning, according to the Magalef index (DMg = 1.406) compared to the result before cleaning (DMg = 0.7556). In the Surgical Center, the opposite occurred, before cleaning there was greater diversity in terms of richness (DMg = 1.642) than after cleaning (DMg = 0.5581). Richness is seen as the presence of rarer fungi, therefore, it is possible to justify the results by supplementing them with the analysis of Table 1. It can be observed that in the PMR after cleaning, rarer fungi were found in the environment, genera that represent less than 3.0% of the total sample collected in the PMR, such as Acremonium (2 CFU), Epidermophyton spp. (1 CFU) and Penicillium spp. (1 CFU). On the other hand, it can be observed that the most common fungi, such as Trichophyton spp. and Microsporum spp. have a reduction in CFUs of approximately 50.0%. In the SC, the results are the opposite, since rarer fungi in the environment, such as Curvularia spp. (2 CFU) and Fusarium spp. (1 CFU), were only observed before cleaning. After cleaning the SC, only two genera were found, Penicillium and Trichophyton, which represent, in general, 55.0% of the CFU isolated in the SC.
Another analysis performed was the application of Simpson's diversity index to the data. The index showed greater diversity in PMR after cleaning (1-D = 0.69) than when PMR was collected before cleaning (1-D = 0.5). Regarding the Shannon index, it was also higher after cleaning the PMR (H´ = 1.433) than before cleaning (H’ = 0.8914), thus indicating that there is a greater probability of finding rare species when collecting two samples randomly after cleaning than when PMR was collected before cleaning (Table 2). In SC, the Simpson's diversity index was higher before cleaning (1-D = 0.7892) than after cleaning (1-D = 0.5333), just as the Shannon index was also higher before cleaning (H’ = 1.76) than before cleaning (H’ = 0.7198).
Values of diversity indices related to fungi in the hospital environment of a veterinary clinic in the city of Araguaína, TO, from March to May 2022 in the Surgical Center (SC) and Pre-anesthetic Medication Room (PMR).
This occurred in research by Fonseca et al. (2019). With disinfection, it is possible to observe a reduction in the microbial load, resulting in lower diversity indicators after cleaning, since in this way the amount of common fungi is reduced and the amount of rare fungi is zeroed, leading to lower diversity. The PMR presenting new fungal genera after cleaning is what led to divergent results and this can be seen as a concern since these fungi may be being carried from other environments and other objects. When applying the Wilcoxon test to the data (Table 3), it is possible to observe that there is no statistical difference before and after the standard operating cleaning procedure in the SC (p>0.05), in the PMR (p>0.05) or in general in the environments (p>0.05). Therefore, with the increase in diversity in the PMR and the lack of statistical difference before and after cleaning, it is possible to state that cleaning in the environments is not effective. Because these are environments where various invasive surgical techniques are performed and where animals with compromised immune systems due to previous diseases are found, it is essential to review disinfectant dilution techniques, cleaning methods and training for the entire team at the university veterinary clinic.
Comparisons of the number of colonies before and after the standard operating procedure for cleaning and disinfection of a university veterinary clinic in Araguaína - TO, from March to May 2022.
When observing growth by objects, concerning those collected in the PMR, both the squeeze bottle and the doorknob did not show fungal growth in either collection and the cabinet was the place with the highest growth (50 CFU), as shown in Table 4. The justification for this may be the excessive movement carried out in the location by the entire surgical team, where various reusable veterinary hospital medical products are stored which can be a factor for cross-contamination (Costa et al., 2013; Lagowski et al., 2019). In the PMR support cabinet, before cleaning, 30 CFU with four morphotypes and three different genera were isolated, of which the most prevalent were Trichophyton 15 CFU (50.0%) and Microsporum 14 CFU (46.6%). After cleaning, 20 CFU with three morphotypes and three genera were isolated, the most prevalent were Trichophyton 12 CFU (60.0%) and Aspergillus 7 CFU (35.0%).
Colony-forming units (CFUs) of filamentous fungi isolated from objects in the Pre-Anesthesia Medication Room, collected before and after the standard operating procedure for cleaning and disinfection of a veterinary clinic in Araguaína - Tocantins, between March and May 2022.
The cabinet corresponds to 57.0% of the isolates in the PMR, followed by the SC support table with 19 CFU (21.6%), the clipper with 13 CFU (14.7%), and the patient table with 6 CFU (6.8%). The SC support table serves as a support for transferring materials to the SC, where there is also a lot of handling by the surgical team. Objects such as the grooming machine and the patient's table were identified as belonging to a single genus: Trichophyton, widely known as a dermatophyte present in canines and felines (Paryuni et al., 2020).
Table 5 presents the results of the genera isolated by object in the SC. Only the surgical focus did not show growth (Table 5), possibly because it was handled with sterile gloves before the surgical procedure began and also due to the high temperatures that come from the LED lighting and fall on the aluminum, reaching temperatures above ideal levels, including on the support where it was collected. These temperatures hinder mesophilic microbial growth (Carvalho et al., 2019).
Colony-forming units (CFUs) of filamentous fungi isolated from objects in the Surgical Center, collected before and after the standard operating procedure for cleaning and disinfection of a veterinary clinic in Araguaína - Tocantins, between March and May 2022.
Before cleaning the doorknob, two CFUs with a morphotype of one genus, Cladosporium, were isolated. After cleaning, one CFU was isolated, identified as Penicillium sp. As in the PMR, in the SC the largest number of CFUs was collected in the cabinet, with nine CFUs belonging to three different genera, the most prevalent being Trichophyton (6 CFUs, 66.7%) and Aspergillus (2 CFUs, 22.2%). After cleaning, four CFUs were isolated, all with a single morphotype of the genus Trichophyton. Also presenting a high number of isolates were the patient's table with five CFUs (18.5%), the door with 4 CFUs (15%), and the oil bottle with three CFUs (11%), all places where there is a lot of handling by the surgical team, which can carry fungi from one environment to another, leading to cross-contamination. In the SC, collections were also performed on the silicone trachea, which presented only one CFU in the collection performed before the cleaning procedure, which was identified as Fusarium sp. Similarly, a sample was collected from the external surface of the silicone breathing balloon, which showed 1 CFU in the sample collected after the cleaning procedure, which was identified as Penicillium spp. A possible explanation for fungal growth after cleaning is primarily based on the fact that Penicillium spp. is a fungus that is easy to spread in the environment because it has light and aerodynamic spores that facilitate its suspension and movement by air currents (Pires, 2021).
A factor that may contribute to the spread of anemophilous fungi such as Penicillium spp. and Aspergillus spp. is the fact that the silicone balloon, squeeze bottle and trachea are cleaned by veterinary professionals, interns and assistants. Due to the lack of adequate training for these professionals, cleaning carried out without caution can cause cross-contamination between environments, between objects, patients and even between professionals.
Another essential analysis to observe is the way in which objects are cleaned in the veterinary clinic, with 70.0% alcohol, benzalkonium chloride and quaternary ammonia. 70% alcohol has widely known microbicidal activities and several studies demonstrate that although alcohol does not completely eliminate microorganisms, it does achieve a satisfactory reduction (Bernardi and Costa, 2017). Quaternary ammonia has an effective action when left for at least 10 minutes with microorganisms at room temperature, on inanimate, hard and non-porous surfaces. It has a high bacteriostatic and fungicidal power, intensified by its long residual power (Sobestiansky, 2002), and is widely used in veterinary clinics and hospitals, presenting good results in cleaning and disinfecting surfaces (Santos et al., 2007).
According to Souza et al. (2021), factors such as lack of motivation, lack of equipment or damaged or inappropriate equipment, lack of sanitizing agents, lack of Personal Protective Equipment (PPE), and fear of exposure to biological materials may contribute to the lack of quality in the disinfection and cleaning of hospital surfaces. Currently, the only manual on the subject at a national level, prepared by the National Health Surveillance Agency, is the “Manual for Cleaning and Disinfection of Surfaces”, however, this is aimed at human health services (Brasil, 2012). Therefore, it is extremely important that the Ministry of Livestock, Agriculture, and Supply develop public policies and protocols for disinfecting veterinary environments. As can be seen in Table 1, the fungi with the highest number of morphotypes found were Trichophyton, Aspergillus, and Penicillium. By observing the reduction in fungal load in PMR from 53 CFUs before cleaning to 35 CFUs after cleaning, and also observing the reduction in SC, from 21 CFUs before cleaning to 6 CFUs after cleaning, it is possible to determine that there is a reduction in the number of CFUs in the environments, however, statistically the cleaning of the place is not being efficient (p>0.05).
4. Conclusion
Through the isolation of objects from the university veterinary clinic, it was observed that the disinfection procedure was not efficient (p>0.05) in eliminating filamentous fungi, despite a reduction in the absolute number of CFU. The number of CFU and genera isolated in the PMR and SC should be viewed with some concern since these environments are critical for animal health and for the employees present at the site under study.
It is up to the cleaning team and local managers to develop an action plan to inhibit fungal growth, with standardization of disinfectant dilution, periodic training on surface cleaning, and constant microbiological monitoring. It is also important to raise awareness about aseptic practices and the appropriate use of personal protective equipment (PPE), both for the cleaning team and for veterinarians, interns, and assistants who are responsible for sanitizing medical-hospital materials. Using disposable cloths, carefully choosing effective disinfectants, and regularly supervising these practices are essential aspects to ensure the safety and health of both animals and professionals involved in surgical procedures. In addition, frequent monitoring of microorganisms in the environment is essential as a preventive approach to reduce risks related to contamination in clinical settings, providing a safe surgical environment free from potential health threats.
Acknowledgements
This study was supported by the School of Veterinary Medicine of the Federal University of Northern Tocantins (EMVZ-UFNT), by the management of the Veterinary Clinic (HVET) at this University, in addition to funding from the PROCAD Amazônia program and the Alvorecer-UFNT Project, and, the development of this research was supported by financial support from PROPESQ/UFNT, Notice No. 010/2024.
Data Availability Statement
All data generated and analyzed during this study are included in this publish article and its supplementary information files.
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Editor:
Takako Matsumura Tundisi
