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Dear Label_Name,

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I am writing on behalf of an international publishing house, Science and Education Publishing, USA (http://www.sciepub.com).

Science and Education Publishing (SciEP) is a multidisciplinary open access publisher of Journals covering the fields of Science, Technology and Medicine. All SciEP publications are subject to high-quality peer review, editorial and production processes and are freely available online.

Welcome to the April, 2013 edition of SciEP newsletter, providing monthly summaries of articles on science & education related topics of interest to scientist and professionals. The mission of our journals is to provide an open access forum for publishing new findings on issues pertinent to scientific and academic field. We also invite you to submit original research papers, review articles, short reports, or case studies are considered for publication in our Multidisciplinary Journals.

American Journal of Public Health Research
DOI: 10.12691/ajphr-1-1-3

The Implementation of a Tele-Homecare System with Service Oriented Architecture and HL7 Message Transmission Standard
Ching-Sung Wang

American Journal of Medical and Biological Research
DOI: 10.12691/ajmbr-1-1-2

The Influence of Ethanol on Pyruvate Kinases Activity in Vivo, in Vitro, in Silico
Lelevich Sergey Vladimirovich, Khrustalev Vladislav Victorovich, Barkovsky Eugene Victorovich, Shedogubova Tatyana Aleksandrovna

American Journal of Medical Sciences and Medicine
DOI: 10.12691/ajmsm-1-1-1

Clinical and Histological Features in Wegener Granulomatosis
Li Cavoli Gioacchino, Passantino Rita, Bono Luisa, Tortorici Calogera, Ferrantelli Angelo, Giammarresi Carlo, Rotolo Ugo

American Journal of Infectious Diseases and Microbiology
DOI: 10.12691/ajidm-1-1-2

The Curse of Lymphatic Filariasis: Would the Continual Use of Diethylcarbamazine Eliminate this Scourge in Papua New Guinea?
Anne Lanham, Lillian Mwanri

We have released issues of some journals on February 2013.
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American Journal of Medical Sciences and Medicine
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American Journal of Cancer Prevention
American Journal of Medicine Studies
American Journal of Infectious Diseases and Microbiology
American Journal of Cardiovascular Disease Research
American Journal of Biomedical Research
American Journal of Mechanical Engineering
American Journal of Microbiological Research
Journal of Preventive Medicine
American Journal of Food and Nutrition
American Journal of Hypertension Research
American Journal of Sports Science and Medicine
Journal of Cancer Research and Treatment
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Journal of Biomedical Engineering and Technology
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Isolation and Molecular Detection of Antibiotic Resistant Staphylococcus aureus from Pet Birds of Mymensigh City Corporation Areas, Bangladesh

Sharmin Sultana Royal, Sanzila Hossain Sigma, Md. Nahid Ashraf, Sabrina Sultana Rimi, Samia Affroze, Salauddin Yousup, Jayedul Hassan, Mahbubul Pratik Siddique, Md. Shafiqul Islam*

Department of Microbiology and Hygiene, Faculty of Veterinary Science, Bangladesh Agricultural University, Mymensingh-2202, Bangladesh

Abstract: Background: Pet bird (ornamental bird) rearing is gradually increasing in Bangladesh. Pet serves as a best friend and confidant for elderly and young people. For unemployment, pet bird farming acts as an income source. Many people are directly or indirectly involved in this business through pet rearing, breeding, and selling. Antibiotic resistance is a global public health concern. Pet birds are considered one of the reservoirs or carriers of AMR bacteria in humans. As a result, it is necessary to know the risks associated with antibiotic-resistant bacteria for humans who are directly involved in pet bird rearing. This research was performed for the isolation and molecular detection of antibiotic-resistant Staphylococcus aureus (MRSA) from pet birds. Methodology: A total of 169 feces samples, including pigeon (n = 57), budgerigar (n = 56), and cockatiel (n = 56), were collected from different pet shops in Mymensingh city corporation. The bacterial isolates were identified using staining and biochemical assays, followed by molecular identification using PCR. Isolated organisms were then tested for antibiotic sensitivity using disk diffusion methods with ten frequently used antibiotics. Results: Among the 169 samples, 35 (20.71%) were positive for Staphylococcus spp. by conventional and molecular tests. The prevalence of the nuc gene was 33.34% in pigeons, 22.23% in budgerigar, and 7.14% in cockatiel. The prevalence of the mecA gene in S. aureus was 28.57% in pigeons. But no mecA gene was found in budgerigar or cockatiel. S. aureus isolates were resistant to methicillin (100%), vancomycin (71.43%), cotrimoxazole (85.71%), and tetracycline (71.43%). Conclusion: It can be concluded that pet birds harbor enteric bacteria that are resistant to most antibiotics used in our study, and the presence of such antibiotic resistant bacteria in pet birds might pose a potential threat to humans and animals’ health.

Keywords: pet birds, antibiotic resistance, Staphylococcus aureus

Received December 25, 2023; Revised January 28, 2024; Accepted February 04, 2024

Citation: Sharmin Sultana Royal, Sanzila Hossain Sigma, Md. Nahid Ashraf, Sabrina Sultana Rimi, Samia Affroze, Salauddin Yousup, Jayedul Hassan, Mahbubul Pratik Siddique, Md. Shafiqul Islam, Isolation and Molecular Detection of Antibiotic Resistant Staphylococcus aureus from Pet Birds of Mymensigh City Corporation Areas, Bangladesh. American Journal of Microbiological Research, 12 (1). 1-6. January 2024. doi:10.12691/ajmr-12-1-1

1. Introduction

A bird that is kept and raised solely for decorative purposes is referred to as a "pet bird." This group mostly consists of Passeriformes (commonly known as songbirds, biz canaries, finches, and sparrows) and Psittaciformes (parrots, parakeets, budgerigars, and love birds). According to statistical research conducted by the American Veterinary Medicine Association (AVMA), 11 to 16 million companion and exotic birds were found in the United States in 2007 [1]. In Bangladesh, pet ownership has turned into a self-sustaining industry, with animals being bred for a number of reasons, including their worth as breeding stock [2].

Zoonotic pathogens are infectious agents that may infect humans via direct contact, food, drink, the environment, or uncommon agents such as viruses, bacteria, parasites, or other unknown substances. Due to our intimate relationship with pets, they pose a potential public health hazard around the world. For example, veterinary hospitals for pet animals and birds can spread zoonotic infections, including Escherichia coli, Staphylococcus aureus, and others [3]. A vast number of individuals in the United States are hospitalized on account of staphylococcal food poisoning every year [4]. Methicillin-resistant S. aureus (MRSA), for example, has emerged as a serious veterinary disease because pets can serve as a reservoir for human MRSA infections. Over the past 10 years, human MRSA cases have been drastically raised in hospitals [5]. A bunch of studies revealed that circulating MRSA clones in dogs and cats are similar to those in humans, specifically the hospital-acquired clones [5,6]. MRSA can be transferred between pets and their owners [7,8,9,10,11,12].

Antimicrobial resistance is a warning burning globally, and it gets worse in developing countries, where the spread of antimicrobial-resistant organisms is often caused by complicated social, cultural, and behavioral factors. [13]. Adding antibiotics to the feed of commercial birds is a common practice in Bangladesh. Some common feed antibiotics are penicillin, oxytetracycline, doxycycline, azithromycin, amoxicillin, cephalexin, etc. The popular reason for using feed antibiotics is to increase efficiency and as a growth promoter to prevent cases of infectious diseases [14]. Pet bird sales are rising in Bangladesh. So, dealers utilize various strategies to make their pets more enticing. This mentality leads them to combine medications with bird feed, unknowingly completing the antibiotic resistance cycle. Multiple research investigations have been carried out on animals, revealing a clear connection between the widespread application of antibiotics and the emergence of antibiotic-resistant bacterial species. However, there is a lack of knowledge and research on antibiotic resistant bacteria from pet animals and birds in Bangladesh, despite the historical recognition of these creatures as a significant source of human health concerns. Thus, this research might have a significant influence in assessing the antibiotic resistance of bacteria found in pet birds.

2. Materials and Methods

2.1. Collection of Samples

A total of 169 samples (feces) were collected from pet shops in Mymensingh city, comprising 57 pigeons, 56 budgerigars, and 56 cockatiels, respectively. All the samples for the present study were collected aseptically using sterile instruments and transferred carefully into an ice box containing ice packs. All the samples were brought to the bacteriology laboratory of the Department of Microbiology and Hygiene, BAU, Mymensingh, for the isolation and identification of bacteria.

2.2. Isolation and Identification

Nutrient broth was used for primary enrichment, and then selective media were inoculated and incubated for the whole night at 37°C. After primary culture of the organism, a 10-fold dilution was made to prevent overgrowth of organisms. After that, 100 µl was inoculated onto nutrient agar, MSA, and blood agar. The colonies showed typical cultural characteristics of S. aureus and were selected for subculture on selective and differential media to confirm the isolation [15]. Morphological characteristics were identified by Gram’s staining according to the method described by Merchand and Packer [16].

2.3. Molecular Identification

2.3.1. DNA Extraction

The boiling method was used for the extraction of genomic DNA from each S. aureus isolate [17, 18].

2.3.2. Molecular Detection of Staphylococcus Spp. and Staphylococcus aureus by PCR

Detection of Staphylococcus spp. and Staphylococcus aureus, was done by targeting tuf and nuc genes according to the methods described by Martineau et al. (2001) [19] and Kalorey et al. (2007) [20].

2.4. Antimicrobial Susceptibility Testing

The antimicrobial sensitivity/resistance for the mentioned eight isolates was evaluated using eight antimicrobials that represent three groups: carbapenems (Imipenem, Ertapenem, and Meropenem), cephalosporins (Ceftazidime, Cefotaxime, Ceftriaxone, and Cefpodoxime), and macrolides (Azithromycin).

Cefotaxime/Clavulanic acid (30/10 mcg) and Ceftazidime/Clavulanic acid (30/10 mcg) discs showed an increase of ≥5 mm in the zone of inhibition as compared to cefotaxime or ceftazidime alone, indicating the production of ESBLs. By following the Clinical and Laboratory Standards Institute (CLSI) guidelines, antibiogram result was interpreted [21].

2.5. Determination of Methicillin Resistant Gene

2.5.1. Amplification of mecA Gene by PCR

Primers designed from mecA genes were used to detect methicillin resistance. The total volume of the PCR mixture was 25 µl, consisting of 12.5 µl of the PCR master mixture, 1 µl of each primer, 1 µl of template DNA, and 9.5 µl of nuclease-free water. The thermal profile of the PCR of the mecA gene was 95 °C for 5 minutes for initial denaturation, followed by 30 cycles of 95 °C for 1 minute for denaturation, 55 °C for 45 seconds for annealing, 72 °C for 1 minute for elongation, and 72 °C for 10 minutes for final extension. The holding temperature was 4 °C [22].

3. Results

This study aimed to determine the prevalence and molecular identification of pathogenic Staphylococcus aureus and their antimicrobial resistance patterns. Considering this, a total of 169 feces samples were collected from 57 pigeons, 56 budgerigars, and 56 cockatiels.

3.1. Molecular Detection of Staphylococcus Spp. and S. aureus by PCR

PCR was performed to confirm the Staphylococcus spp. by using specific primers designed for the tuf gene (Figure 1). Out of 35 tuf gene-positive Staphylococcus spp., only 7 were found positive for the nuc gene (Table 1, Figure 2, and Figure 3). A 279-bp band appeared after PCR and electrophoresis for nuc gene.

Figure 1. Amplification of tuf gene (884-bp) for Staphylococcus genus. Lane M: 100 kb DNA ladder (Thermofisher), Lane 1-11: Positive for tuf gene of Staphylococcus, Lane NC: Negative control, Lane PC: Positive control. PCR products were electrophoresed in 1.5% LE agarose at 100 volt for 30 minutes at TAE buffer.

Figure 2. Amplification of nuc gene (279-bp) for S. aureus. Lane M: 100 kb DNA ladder (Thermofisher), Lane PC: Positive control, Lane NC: Negative control, Lane 1-7: Positive for nuc gene of S. aureus. PCR products were electrophoresed in 1.5% LE agarose at 100 volt for 30 minutes at TAE buffer.

Figure 3. Prevalence of nuc gene in Pigeon, Budgerigar and Cockatiel.

Table 1. Prevalence of S. aureus in Pigeon, Budgerigar and Cockatiel

3.2. Molecular Detection of mecA for by PCR

Out of 7 samples, only 2 were positive for the mecA gene (Table 2, Figure 4 and Figure 5). A 533-bp band appeared after PCR and electrophoresis for the mecA gene.

Figure 4. Amplification of mecA gene (533-bp) for methicillin resistance. Lane NC: Negative control, Lane M: 100 kb DNA ladder (Thermofisher), Lane PC: Positive control, Lane 1-2: Positive for mecA gene of S. aureus. PCR products were electrophoresed in 1.5% LE agarose at 100 volt for 30 minutes at TAE buffer.

Table 2. Distribution of mecA gene of S. aureus (total=7) isolates with their prevalence

Figure 5. Prevalence of mecA gene of S. aureus isolates in pigeon, budgerigar, cockatiel.

3.3. Antibiogram Profile of S. aureus Isolates

The nuc gene-positive S. aureus isolates were found to be resistant to methicillin (100%), vancomycin (71.43%), intermediate to ampicillin (57.14%), Ciprofloxacin (57.14%), sensitive to Cotrimoxazole (85.71%), Tetracycline (71.43%), and chloramphenicol (57.14%) (Table 3, Table 4 and Figure 6).

Table 3. Antibiogram profile of S. aureus isolates

Table 4. S. aureus isolates resistance to number of antibiotics

Figure 6. Antibiogram profile of S. aureus isolate

4. Discussion

Pets have been a major conduit for zoonotic infections to infect humans since the dawn of humanity [23]. S. aureus, an opportunistic pathogen that usually inhabits the skin and mucosa of healthy individuals, can produce a variety of infections, such as food poisoning, skin diseases, wound colonization, and respiratory infections, and poses a unique capacity to induce clotting [24]. This study aimed to isolate and identify the pathogenic S. aureus from pet birds. This study also focused on the antimicrobial resistance patterns of isolated bacteria. In the current study, Staphylococcus spp. was found to be 20.71% of the isolated bacteria from pet birds. Staphylococcus spp. is ubiquitous in aviaries and, under favorable conditions, acts as an opportunistic pathogen. It may cause omphalitis, femoral head necrosis, infected hocks, and stifle joints secondary to bumblefoot in pet birds.

The molecular detection of Staphylococcus spp. was done by using the tuf gene. The nuc gene primers were used to confirm the S. aureus isolates, as reported by Kalorey et al. [20] and Haque et al. [25] and. The current study found that pet pigeons (7.10%) had a higher prevalence of pathogenic S. aureus than budgerigar (3.57%) and cockatiel (1.79%), respectively. Because of this, pet birds could be a significant reservoir for pathogenic staphylococci infections, which may be passed from animals to humans via zoonotic transmission. As a result, pet birds could be considered a major reservoir for pathogenic staphylococci infections that can be transmitted to humans through zoonotic interaction transmission. In contrast, pet birds could also play a major role in transmitting staphylococci because of their frequent with their owner as well as their environment, as described by Jung et al. [26], Damborg et al. [27], Maia et al. [28], and Truong et al. [29]. Aside from that, habits like grooming of birds and hand-feeding of pet birds could raise the risk of zoonotic disease transmission to owners [27,30]. Therefore, this indicates a high possibility of co-colonization of S. aureus between pet birds and their owners.

Methicillin (100%), Vancomycin (71.43%) resistance was observed in the isolated S. aureus, and intermediate resistance to Ampicillin (57.14%) and Ciprofloxacin (57.14%) was seen. Cotrimoxazole (85.71%), tetracycline (71.43%), and chloramphenicol (57.14%) were sensitive. Bagheri et al. [31], Gharsa et al. [32], Ho et al. [33], Dressler et al. [34], and Loeffler et al. [35] found antibiogram profiles that were almost identical. Because resistant isolates could be superbugs, methicillin and vancomycin resistance in S. aureus is a big issue for civilization. To confirm the resistance, this study also looked at the distribution of bacterial resistance genes in S. aureus isolates. For S. aureus, the prevalence of the mecA genes was 28.57% in our investigation; however, no isolates tested positive for the mecC, vanA, vanB, or vanC genes. Akter et al. [36] also used mecA and mecC primers to detect the presence of methicillin resistance genes in their study. In another study, Shahid et al. [37] detected vancomycin resistance in S. aureus from a food processing environment using vanA, vanB, and vanC primers, which may result from contaminated human hands [38,39].

It can be concluded that if these bacteria can enter the food chain, it can cause serious illness to individuals, and treatment for those patients using those antibiotics would not be successful.

5. Conclusion

Pet birds are the closest friends ever to their owners because they are able to create a strong emotional bond with their owners while also representing their social norms and physical well-being. As a result, the number of people raising pet birds around the world is increasing. The goal of this study was to examine the prevalence of S. aureus as well as their antibiotic resistance patterns. S. aureus isolates were identified using morphological, staining, culture, and biochemical features. PCR was used to identify pathogenic bacteria with the antibiogram profile of positive isolates. S. aureus had a higher prevalence (7.10% in pigeons), followed by 3.57% in budgerigar and 1.79% in cockatiel, respectively. The prevalence of the mecA gene in S. aureus was 28.57% in pigeons. But no mecA gene was found in budgerigar or cockatiel. S. aureus isolates were resistant to methicillin (100%) and vancomycin (71.43%). Resistance to vancomycin (71.43%) of S. aureus isolates from pet bird samples is a noteworthy outcome of this study that is alarming for civilization. However, cotrimoxazole (85.71%) and tetracycline (71.43%) are sensitive to S. aureus treatment. In Bangladesh, there has been an increase in the demand for pet birds for cage-rearing. Drug-resistant germs progressively grow in pet birds. The aim of the current investigation was to extract and characterize bacterial pathogens from domesticated birds using their antibiogram. As a result of this research, we now have a clear image of pet birds (pigeons, budgerigars, and cockatiels) carrying harmful germs, posing a risk of illness transmission to their owners. To protect the health of both humans and their pets, professional veterinarians should check and vaccinate pet birds on a regular basis.

Conflict of Interest

The authors assert that they do not possess any conflicts of interest.

Acknowledgments

The authors wish to express gratitude to the Ministry of Science and Technology, Government of the People’s Republic of Bangladesh, for awarding the National Science and Technology (NST) fellowship to Sharmin Sultana Royal.

References

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