Open-access Multidrug-resistant Staphylococcus spp. isolated from dogs and cats attended at veterinary hospital in the Caatinga biome

Staphylococcus spp. multirresistentes isolados de cães e gatos atendidos em hospital veterinário no bioma da Caatinga

Abstract

Antimicrobial resistance (AMR) in bacteria isolated from companion animals is concerning, as human-animal interaction in nosocomial or household environments may favor sharing of these microorganisms and resistance genes, highlighting the need for constant investigations. The objective of this study was to evaluate the antimicrobial susceptibility profile of Staphylococcus spp. isolated from clinical samples, including swabs from surgical wounds, skin, ears and noses, as well as contents of submandibular nodules, collected from dogs and cats treated at a veterinary hospital in the Caatinga biome. Phenotypic and genotypic tests for antimicrobial resistance, biofilm formation, and enterotoxin genes were carried out. Overall, of 129 samples, 34 (26.4%; 95% CI = 18.8 – 34%) were identified as Staphylococcus spp. and, among these, 15 isolates (44.1%) of six species showed antimicrobial resistance profile. The most frequent isolates were S. aureus, S. intermedius, and S. pseudintermedius with 26.67% frequency. Isolated bacteria demonstrated the presence of important resistance genes such as vanA (40%), vanB (13.33%), and mecA (6.67%). The highest resistance rates among isolates were for penicillin (n = 15 isolates; 100%) and tetracycline (n = 12 isolates; 80%). Nine (60%) of the 15 isolates (four S. aureus, two S. intermedius, two S. pseudintermedius, and one S. epidermidis) were classified as multidrug-resistant (MDR). The other six isolates were resistant to one or two antibiotic classes. One canine isolate was positive for the methicillin-resistant S. aureus (MRSA) profile. No genes for enterotoxin production or biofilm were detected. These results reinforce the need for the prudent use of antimicrobials in veterinary medicine, as well as the rigorous adoption of biosafety practices. Moreover, the relevance of the Caatinga biome as a setting for monitoring antimicrobial resistance should be considered.

Keywords:
multidrug resistance; pets; One Health; veterinary hospital; methicillin-resistant Staphylococcus aureus

Resumo

A resistência antimicrobiana (RAM) em bactérias isoladas de animais de companhia é preocupante, visto que a interação humano-animal em ambientes hospitalares ou domésticos pode favorecer a disseminação desses microrganismos e genes de resistência, ressaltando a necessidade de investigações constantes. O objetivo deste estudo foi avaliar o perfil de suscetibilidade antimicrobiana de Staphylococcus spp. isolados de amostras clínicas, incluindo swabs de feridas cirúrgicas, pele, ouvido e nariz, além de conteúdo de nódulos mandibulares, coletados de cães e gatos atendidos em um hospital veterinário no bioma da Caatinga. Foram realizados testes fenotípicos e genotípicos para resistência antimicrobiana, formação de biofilme e genes de enterotoxinas. No total, de 129 amostras, 34 (26,4%; IC 95% = 18,8 – 34%) foram identificadas como Staphylococcus spp. e, entre estas, 15 isolados (44,1%) de seis espécies apresentaram perfil de resistência antimicrobiana. Os isolados mais frequentes foram S. aureus, S. intermedius e S. pseudintermedius, com frequência de 26,67%. As bactérias isoladas demonstraram a presença de importantes genes de resistência, como vanA (40%), vanB (13,33%) e mecA (6,67%). As maiores taxas de resistência entre os isolados foram para penicilina (n = 15 isolados; 100%) e tetraciclina (n = 12 isolados; 80%). Nove (60%) dos 15 isolados (quatro S. aureus, dois S. intermedius, dois S. pseudintermedius e um S. epidermidis) foram classificados como multirresistentes (MDR). Os outros seis isolados foram resistentes à uma ou duas classes de antibióticos. Um isolado canino apresentou perfil positivo para Staphylococcus aureus resistente à meticilina (MRSA). Não foram detectados genes para produção de enterotoxinas ou formação de biofilme. Esses resultados reforçam a necessidade do uso prudente de antimicrobianos na medicina veterinária, bem como a adoção rigorosa de práticas de biossegurança. Além disso, deve-se considerar a relevância do bioma Caatinga como um ambiente para o monitoramento da resistência antimicrobiana.

Palavras-chave:
resistência a múltiplos medicamentos; animais de estimação; Saúde Única; hospital veterinário; Staphylococcus aureus resistente à meticilina

1. Introduction

Antimicrobial resistance (AMR) is a problem of global concern, being characterized by the World Health Organization (WHO) as one of the top 10 global public health threats (Tang et al., 2023). The overuse of antimicrobials is pointed out as the main cause of selection of resistant bacteria, and the post-pandemic period of COVID-19 was a determining factor for the increase in the use of these drugs, mainly in human medicine (Bandyopadhyay and Samanta, 2020; WHO, 2020a). The large-scale use of antibiotics as prophylactic methods and growth promoters in food-producing animal herds is widely considered one of the main pillars for the dispersion of AMR in the human-animal context, underestimating the participation of small animals (Allel et al., 2023). However, investigations highlight the presence of resistant bacteria in companion animals, with an increasing number of these pathogens of importance in dogs and cats (Pomba et al., 2017).

The genus Staphylococcus spp. is frequently associated with opportunistic infections, such as skin and soft tissue infections in humans and animals. The occurrence of multidrug resistance among these bacteria generates serious implications for the treatment of infections, since the presence of the mecA gene or its homologue mecC confers resistance to most β-lactam antibiotics, with the exception of 5th generation cephalosporins for human use (Morris et al., 2017), also limiting therapy in veterinary medicine (Di Cerbo et al., 2019). In such cases, critical antibiotics for human health may be required for animal treatment, demonstrating the interconnection between resistant pathogens in humans and animals (Bandyopadhyay and Samanta, 2020). Estimates highlight that in the United States, 70% of antibiotics for human treatment are also used in the veterinary medicine field (Bellato et al., 2022).

The Caatinga is the only biome found exclusively in Brazil; it is located primarily in the Northeast region and is characterized by challenging conditions, such as intense solar radiation, soils with high temperatures and salinity, as well as water and nutrient scarcity (Lacerda Júnior et al., 2017). These characteristics can exert intense selective pressure on microbial communities, favoring the development of adaptive mechanisms for survival (Araujo et al., 2021; Fernandes et al., 2025). These strategies may be genetically linked to determinants of antimicrobial resistance which, through co-selection processes, can contribute to the maintenance of the environmental resistome, making their investigation essential for understanding the dynamics of the spread of this resistance (Delgado-Baquerizo et al., 2022; González Román et al., 2025).

The mechanisms by which bacteria acquire resistance to antimicrobials in general are complex and multi-causal, designating AMR as a "silent pandemic", deeming the rapid evolution of microorganisms opposed to the limited introduction of new antimicrobials (Prestinaci et al., 2015). Thus, the objective of this work was to isolate bacteria of the genus Staphylococcus from dogs and cats in the clinical routine of a university veterinary hospital located in the Caatinga biome, northeastern Brazil, as well as to identify antimicrobial resistance genes in these bacteria.

2. Material and Methods

2.1. Study location and sample collection

From February 2022 to March 2023, 129 clinical samples were collected from dogs and cats, of which 76 (58.9%) were from dogs and 53 (41.1%) from cats. The animals came from the medical and surgical clinical routine care at the Prof. Dr. Ivon Macedo Tabosa University Veterinary Hospital (HVU) of the Center for Health and Rural Technology (CSTR), Federal University of Campina Grande (UFCG), Patos Campus - Paraíba, in the northeastern semiarid region, Brazil. The animals came from municipalities covered by the Caatinga biome. The biological materials collected were: surgical wound swab: 30/129 (23.26%); urine: 28/129 (21.71%); ear swab: 20/129 (15.50%); purulent abscess secretion: 12/129 (9.30%); back skin wound swab: 12/129 (9.30%); right thoracic limb skin wound swab: 6/129 (4.65%); nasal swab: 4/129 (3.10%); bone implant plate swab: 3/129 (2.33%); ocular swab: 3/129 (2.33%); rectal swab: 2/129 (1.55%); oral swab: 2/129 (1.55%); tail skin wound swab: 2/129 (1.55%); face skin wound swab: 2/129 (1.55%); vaginal secretion swab: 1/129 (0.78%); mandibular nodule content: 1/129 (0.78%); subcutaneous fluid: 1/129 (0.78%). Samples were packed into tubes with Stuart transport medium (Interlab, São Paulo, São Paulo, Brazil) and transported under refrigeration (2–8 °C) to the microbiology laboratory for processing.

2.2. Isolation and identification of Staphylococcus spp.

The samples were enriched in Brain Heart Infusion broth (KASVI, São José dos Pinhais, Paraná, Brazil) at 37°C for 24 hours and subsequently seeded on mannitol salt agar (Difco Laboratories Inc., Detroit, USA), and after cultivation the plates were incubated at 37°C (± 1°C) for 24-48 hours, and the isolated colonies were processed for Gram staining, catalase and coagulase tests, and mannitol fermentation. Species confirmation was performed using the Matrix-Assisted Laser Desorption/Ionization -- Time of Flight (MALDI-TOF) technique (Bier et al., 2017).

2.3. Phenotypic test of antimicrobial resistance

In vitro antimicrobial susceptibility was evaluated by the disk diffusion method on Müller-Hinton agar, as recommended by the Clinical and Laboratory Standards Institute (CLSI, 2021). The inoculum concentration corresponded to the turbidity of the 0.5 McFarland scale. After seeding, plates were kept at an incubation temperature of 37°C (± 1°C) for 24 hours and the results were interpreted by measuring the inhibition zones (CLSI, 2021). The antimicrobials evaluated were: clindamycin (30μg), erythromycin (30μg), sulfamethoxazole/trimethoprim (10μg), gentamicin (30μg), amikacin (30 μg), tetracycline (30 μg), cefoxitin (30 μg), oxacillin (30μg), penicillin (30 μg), norfloxacin (30 μg), chloramphenicol (30 μg), and linezolid (10μg). S. aureus ATCC 25923 strain was used as standard control.

2.4. Molecular detection of antimicrobial resistance, biofilm formation, and enterotoxin genes

Isolates that showed antimicrobial resistance profile on phenotypic tests were selected for the molecular analysis. For bacterial DNA extraction, the Dneasy Blood and Tissue kit (Qiagen, Hilden, Germany) was used on BHI broth culture samples, according to the manufacturer's recommendations. Detection of antimicrobial resistance, biofilm formation, and enterotoxin genes were carried out by PCR for the genes SEA, SEB, SEC, SED, SEE, femA, blaZ, mecA, mecC, icaD, TetL, TetM, TetK, TetO, TetS, vanA, and vanB, as previously described (Clark et al., 1993; Dutka-Malen et al., 1995; Mehrotra et al., 2000; Arciola et al., 2001; Ng et al., 2001; Rosec and Gigaud, 2002; Haveri et al., 2005; Paterson et al., 2012; Pedroso et al., 2018), using specific primers (Table 1). Reference strains S. aureus ATCC25923, ATCC13565, ATCC14458, ATCC19095, ATCC23235, ATCC27664, and USA400 were used as positive controls, and ultrapure water as negative control.

Table 1
Resistance genes analyzed and function, primer sequences, amplicon sizes in base pairs (bp), and respective references.

2.5. Data analysis

The adherence G-test was used to compare the frequencies of isolated bacteria according to species, and the adherence chi-square test was used to compare the frequencies of isolated bacteria between dogs and cats. The binomial 95% confidence interval (95% CI) was calculated for the frequency of Staphylococcus spp. The significance level deemed was 5% (P ≤ 0.05) and analyses were ran using BioEstat 5.4 software (Ayres et al., 2007).

3. Results

Overall, of the 129 samples, 34 (26.4%; 95% CI = 18.8 – 34%) were identified as Staphylococcus spp. and, among these, 15 isolates (44.1%) of six species showed antimicrobial resistance profile. Twelve (80%) out of the 15 isolates were coagulase-positive (CoPS) and three (20%) coagulase-negative (CoNS). The Staphylococcus spp. species identified were four (26.7%) S. pseudintermedius, four (26.7%) S. aureus, four (26.7%) S. intermedius, one (6.7%) S. epidermidis, one (6.7%) S. felis, and one (6.7%) S. schleiferi (Table 2). Staphylococcus spp. were identified in 10 (66.7%) samples from dogs and in five (33.3%) samples from cats, however, there was no statistical difference between the frequencies (P = 0.302). The species isolated from dogs were S. intermedius (four isolates; 40%), S. aureus (three isolates; 30%), and S. pseudintermedius (three isolates; 30%). In cats, the species isolated were S. schleiferi (one isolate; 20%), S. aureus (one isolate; 20%), S. felis (one isolate; 20%), S. epidermidis (one isolate; 20%), and S. pseudintermedius (one isolate; 20%).

Table 2
Staphylococcus spp. species, number of positive samples and frequency (%).

The antimicrobials with the highest frequencies of resistant bacteria were penicillin (n = 15 isolates; 100%) and tetracycline (n = 12 isolates; 80%). Nine (60%) of the 15 isolates (four S. aureus, two S. intermedius, two S. pseudintermedius, and one S. epidermidis) were categorized as multidrug-resistant (MDR) to the classes of penicillins, tetracyclines, cephamycins, and lincosamides.

In molecular analysis, the most frequent resistance genes were blaZ and vanA, detected in 15 (100%) and 6 (40%) isolates, respectively. The genes TetM, TetL, TetK, vanB, and mecA were detected in five (33.3%), four (26.7%), four (26.7%), two (13.3%), and one (6.7%) isolates, respectively (Table 3). No enterotoxin or biofilm-associated genes were detected.

Table 3
Staphylococcus isolates, animal species, biological samples, resistance genes and antimicrobial susceptibility profile. In the “antimicrobial susceptibility profile” section, white cells represent susceptibility, gray cells represent intermediate resistance, and black cells represent resistance.

4. Discussion

The genus Staphylococcus spp. is commonly found in the skin and mucous membranes microbiota of humans and animals; however, some species can cause important opportunistic infections for both human and animal medicine (Kowalewicz et al., 2023). In this study, Staphylococcus spp. with antimicrobial resistance profiles were isolated from dogs and cats in the clinical routine of a veterinary hospital in the Caatinga biome. S. pseudintermedius, S. aureus, and S. intermedius were the most frequently isolated coagulase-positive species (CoPS), while S. epidermidis, S. felis, and S. schleiferi were the most prevalent coagulase-negative species (CoNS). S. pseudintermedius was one of the most common isolates in canine and feline conditions. This microorganism is considered an opportunistic pathogen in healthy dogs, being responsible for most cases of pyoderma (Lynch and Helbig, 2021; Rana et al., 2022). In felines, although not being part of the microbiota, this bacterium has been isolated from healthy and sick cats, mainly in cases associated with household cohabitation with dogs (Bierowiec et al., 2021; Ma et al., 2020).

Colonization of the skin and mucous membranes of companion animals by S. pseudintermedius, especially dogs, is directly related to the recovery of this bacterium in human clinical samples (Small et al., 2021; Glajzner et al., 2023). Its zoonotic potential is highly recognized by the European Food Safety Authority (EFSA, 2023), being associated with infections of the skin, soft tissues, and invasive procedures, especially among hospitalized patients who have or had prior contact with companion animals (Moses et al., 2023).

S. aureus was also a frequent isolate, considered a ubiquitous microorganism, capable of colonizing and infecting humans and animals (Bruce et al., 2022). In dogs and cats, this bacterium is mainly associated with pustular dermatitis and food poisoning (Algammal et al., 2020). In human pathogenesis, these bacteria are involved in cases of community-acquired and hospital-acquired skin and soft tissue infections, as well as more severe cases such as endocarditis and bacteremia (Olaniyi et al., 2017). There are data on the isolation of highly resistant strains of S. aureus among pet owners and domestic animals, as well as evidence of the transmission of these microorganisms between these groups, demonstrating the need for holistic approaches to mitigate the spread of AMR (Das et al., 2023; Jin et al., 2023).

Another member of CoPS that showed a higher isolation frequency was S. intermedius. Considered a common constituent of the animal microbiota, it is quite related to cases of pyoderma and external otitis. Although not frequent in human infections, methicillin-resistant S. intermedius was isolated from a case of tenosynovitis caused after bites from a feline with a history of antibiotic therapy for severe pyoderma (Takeuchi et al., 2023). CoNS, once considered only as common human and animal microbiota, are becoming increasingly important pathogens in nosocomial infections related to biofilm formation on catheters, prostheses, and medical devices (Fišarová et al., 2019). Furthermore, CoNS are reservoirs of resistance and virulence genes, evidencing their importance in the transfer of these genes to different bacteria, including CoPS species (Rossi et al., 2017).

S. epidermidis and S. felis are deemed important pathogens in small animals, mainly in skin and ear infections in dogs, as well as lower urinary tract diseases, otitis, and eye infections in cats (Thomson et al., 2022). In humans, S. epidermidis is related to cases of endocarditis, septicemia, wound, bone and joint infections (Abdel-Moein and Zaher, 2020). Although rare, S. felis was isolated from a human surgical site infection, showing clonal similarity with isolates from one of the felines that cohabited with the patient, denoting intra-household sharing, as well as its zoonotic potential (Sips et al., 2023).

S. schleiferi is a bacterium with variable coagulase, being classified as S. schleiferi subsp. schleiferi (coagulase-negative) and S. schleiferi subsp. coagulans (coagulase-positive), currently reclassified as S. coagulans (Madhaiyan et al., 2020). Nosocomial infections related to medical devices, wounds, and surgical sites, in addition to bacteremia, endocarditis, and urinary tract infections, are problems attributed to S. schleiferi in human pathogenesis (Naing et al., 2023). There is evidence of a case of human bacteremia and osteomyelitis, in which S. schleiferi was isolated from both the patient and her dog, which had purulent otitis, demonstrating its zoonotic capacity (Yarbrough et al., 2017). Considered an opportunistic bacterium in dogs, mainly pyoderma, external otitis, and superficial folliculitis, the occurrence of S. schleiferi in pyogenic infections in cats is rare (Morris et al., 2017). Interestingly, in this research, the only isolate of S. schleiferi came from a clinical sample of a nasal swab from a feline, showing that, although uncommon, this bacterium can colonize and cause infections in different anatomical sites and in animal species different from the usual, and may even remain in the hospital environment, maximizing the chances of nosocomial infections.

In Brazil, there are still few studies exploring the antimicrobial susceptibility profile of Staphylococcus spp. related to companion animals. In this research, the frequency of phenotypic resistance of Staphylococcus spp. isolates was highest for penicillin, followed by tetracycline, consistent with previous results (Souto Sobrinho et al., 2024). A similar resistance profile was reported in Staphylococcus spp. from healthy dogs and cats in the Southern region of Brazil, with 61.8% of isolates resistant to penicillin and less than 20% to tetracycline (Silva et al., 2025). These results can be explained by the frequent use of these antibiotics in veterinary medicine, both in companion animals and in food-producing and exotic animals (Caneschi et al., 2023).

In terms of northeastern Brazil, studies exploring the resistance of Staphylococcus spp. in companion animals are few. Resistance of these bacteria to β-lactams has been reported in large animals (Krewer et al., 2015), as well as in cases of canine external otitis, of which 11.47% were methicillin-resistant with multidrug-resistant profile (Carvalho et al., 2019). Furthermore, resistant strains of S. aureus were recovered from the veterinary environment and professionals, as well as from pet owners and their animals in a veterinary hospital located in the Atlantic Forest biome area in northeastern Brazil (Leite et al., 2023).

Multidrug resistance (MDR) is an emerging public health concern and there are data on the high prevalence of MDR Staphylococcus spp. isolates in companion animals. Dogs and cats can be important reservoirs of these bacteria, evidencing that the transmissibility of these microorganisms among pets, owners, and health professionals is a pillar for the dissemination of AMR (Araújo et al., 2024; Marco-Fuertes et al., 2024; Thomson et al., 2022).

The origin of multidrug resistance in Staphylococcus spp. was largely attributed to the selective pressure of methicillin use in humans, but there is evidence of the isolation of methicillin-resistant S. aureus (MRSA) from European hedgehogs in the pre-antibiotic era, suggesting that the co-evolutionary adaptation of S. aureus was associated with hedgehogs colonized by dermatophyte fungi. The evolutionary history of these microorganisms connects the One Health scenarios, demonstrating that the use of this approach is essentially necessary for understanding and managing AMR (Larsen et al., 2022).

In this study, 60% of isolates showed multidrug resistance, mainly S. aureus. Methicillin resistance, in line with the multidrug resistance presented by S. aureus strains, tends to increase, with a global frequency of 40.7% (Couto et al., 2016). The antimicrobial susceptibility profile of S. aureus from 1999 to 2018 demonstrated an increasing rate of resistance to penicillin (81.8%), of which more than half of the isolates were MRSA (56.4%) and 14.5% were MDR (Costa et al., 2022).

A study carried out in southeastern Brazil showed that 48.11% of animals were positive for methicillin-resistant Staphylococcus (MRS) and of these, 38.7% were dogs and 10.4% were cats (Sfaciotte et al., 2025). Consistent with these results, the canine isolates in the present study also showed a higher resistance rate and one canine S. aureus isolate was positive for the MRSA profile. Although MRSA was originally recovered from nosocomial and community infections, recent evidence highlights human-animal cohabitation as a source of reciprocal exchange and dispersion of these microorganisms (Abrudan et al., 2023).

The blaZ gene was detected in all Staphylococcus spp. isolates, consolidating the high frequency of resistance to β-lactams, also described in other studies (Bellato et al., 2022; Moses et al., 2023). The second most frequent gene was vanA, and according to the WHO, methicillin-resistant S. aureus with reduced susceptibility to vancomycin is considered a high-priority global pathogen (WHO, 2020b). In this research, one canine S. aureus isolate simultaneously presented the mecA, vanA, and vanB genes, being phenotypically resistant to oxacillin. Vancomycin resistance is concerning cause of mortality when the pathogenic agent is MRSA (Wijesekara et al., 2017). Furthermore, it has been reported that the use of Avoparcin (a vancomycin analog) in livestock farming favored the resistance of Enterococcus to vancomycin (VRE) of the vanA type. The global burden of VRE in food products of animal origin was estimated at 11.7% in 2021 (Lawpidet et al., 2021). Consequently, VRE can colonize the intestinal microbiota of humans and animals through these foods, favoring the spread of this gene to other microorganisms through the food chain.

High-level vancomycin resistance in S. aureus was described in 2002, being acquired through the Tn1546 transposon containing the plasmid vanA gene from Enterococcus faecalis (CDC, 2002; Gardete and Tomasz, 2014). In general, S. aureus was the main species carrying the vanA gene in this research, followed by S. pseudintermedius. Regarding the latter, although a rare finding, there are reports of strains of canine origin showing intermediate resistance to vancomycin (Moreira et al., 2020), as well as the recovery of a resistant strain from a healthy dog (Viñes et al., 2022). However, S. aureus is the pathogen most correlated with this resistance, given that vancomycin is the "last resort" antibiotic for severe MRSA infections in humans (Wijesekara et al., 2017).

In the present study, phenotypic tests for vancomycin resistance were not performed, which constitutes a major limitation, since it was not possible to assess whether these genes were functionally expressed. However, the vanA and vanB genes are plasmid-borne and easily disseminated through horizontal transfer (Gardete and Tomasz, 2014; González Román et al., 2025). The presence of these genes in bacteria isolated from companion animals has great epidemiological relevance, given the low use of vancomycin in veterinary medicine, raising the possibility of resistance gene exchange between microorganisms from the nosocomial environment and the human-companion animal relationship, highlighting the importance of the One Health approach in the AMR context.

5. Conclusion

The results obtained from the isolation of resistant strains of Staphylococcus spp. in dogs and cats treated in veterinary clinical routine reinforce the need for the prudent use of antimicrobials in veterinary medicine, as well as the rigorous adoption of biosafety practices. The detection of these bacteria in companion animals highlights the role of these hosts as potential reservoirs of bacteria carrying resistance genes, evidencing the importance of the One Health approach. The increasing exchange of resistance determinants between human and animal microorganisms underscores the urgency of integrated strategies to avoid the spread of antimicrobial resistance in different ecosystems. Moreover, the relevance of the Caatinga biome as a setting for monitoring antimicrobial resistance should be considered.

Acknowledgements

Fundação de Apoio à Pesquisa do Estado da Paraíba (FAPESQ), for the financial support (financial code: 47340.673.29278.09082021) and the Conselho Nacional de Desenvolvimento Científico e Tecnológico (CNPq) – Brasil, for the fellowship.

Data Availability Statement

The data that support the findings of this study are available on request from the corresponding author.

  • Ethics and consent
    This study was approved by the Animal Use Ethics Committee of the Federal University of Campina Grande (UFCG), under protocol no. 18/2022.

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Edited by

  • Editor:
    Takako Matsumura Tundisi

Publication Dates

  • Publication in this collection
    21 Aug 2026
  • Date of issue
    2026

History

  • Received
    04 Apr 2026
  • Accepted
    03 July 2026
Creative Common - by 4.0
This is an Open Access article distributed under the terms of the Creative Commons Attribution license (https://creativecommons.org/licenses/by/4.0/), which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.
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