Indian Journal of Animal Research

  • Chief EditorK.M.L. Pathak

  • Print ISSN 0367-6722

  • Online ISSN 0976-0555

  • NAAS Rating 6.50

  • SJR 0.263

  • Impact Factor 0.4 (2024)

Frequency :
Monthly (January, February, March, April, May, June, July, August, September, October, November and December)
Indexing Services :
Science Citation Index Expanded, BIOSIS Preview, ISI Citation Index, Biological Abstracts, Scopus, AGRICOLA, Google Scholar, CrossRef, CAB Abstracting Journals, Chemical Abstracts, Indian Science Abstracts, EBSCO Indexing Services, Index Copernicus
Submit

Full Research Article

Cave Bats as Carriers of Extended Spectrum Beta-lactamase Produced by Escherichia coli from the Island of Lombok, Indonesia

Alfiana Laili Dwi Agustin1, Mustofa Helmi Effendi2,*, Wiwiek Tyasningsih3, Aswin Rafif Khairullah4, Kunti Tirtasari1, Ikechukwu Benjamin Moses5, Siti Rani Ayuti6
1Doctoral Program of Veterinary Science, Faculty of Veterinary Medicine, Universitas Airlangga, Jl. Dr. Ir. H. Soekarno, Kampus C Mulyorejo, Surabaya 60115, East Java, Indonesia.
2Division of Veterinary Public Health, Faculty of Veterinary Medicine, Universitas Airlangga, Jl. Dr. Ir. H. Soekarno, Kampus C Mulyorejo, Surabaya 60115, East Java, Indonesia.
3Division of Veterinary Microbiology, Faculty of Veterinary Medicine, Universitas Airlangga, Jl. Dr. Ir. H. Soekarno, Kampus C Mulyorejo, Surabaya 60115, East Java, Indonesia.
4Research Center for Veterinary Science, National Research and Innovation Agency (BRIN), Jl. Raya Bogor Km. 46 Cibinong, Bogor 16911, West Java, Indonesia.
5Department of Applied Microbiology, Faculty of Science, Ebonyi State University, Abakaliki 480211, Nigeria.
6Faculty of Veterinary Medicine, Universitas Syiah Kuala, Jl. Tgk. Hasan Krueng Kalee No. 4, Kopelma Darussalam, Kota Banda Aceh 23111, Aceh, Indonesia.

ABSTRACT

Background: Escherichia coli is a Gram-negative commensal bacterium that normally resides in the digestive tract of humans and animals which is used as an indicator of the extended-spectrum beta-lactamase (ESBL) gene in an individual and can carry out gene transfer. Transmission of ESBL E. coli from wild animals has not been given much attention even though wild animals can act as vectors that spread ESBL in the environment so that it can pose a risk to public health. This research aims to identify the blaTEM gene which codes for ESBL in E. coli from bats that live in caves in Lombok, Indonesia. 

Methods: A total of 135 samples from bat rectal swabs were cultured on Eosin Methylene Blue Agar media and biochemical suspects were identified using the Indole, Methyl red, Voges-Proskauer, Citrate + and H2S (IMVIC) test. The E. coli bacteria obtained were tested for sensitivity using 7 classes of antibiotics, namely amoxicillin, ciprofloxacine, sulfamethoxazole/trimethoprim, tetracycline, gentamicin, cefotaxime and azithromycin. Bacteria that show multidrug resistance are subjected to PCR testing to detect the blaTEM gene.

Result: Of the 135 test samples, it was found that 97 (71.85%) samples were positive for E. coli, 12 (12.37%) samples were Multidrug Resistance (MDR) and 2 (2.06%) samples had the blaTEM gene as the ESBL coding gene in bats that live in caves on the island of Lombok, Indonesia. The presence of the blaTEM gene in E. coli from bats can be indicated as a reservoir for MDR and ESBL transmission so that it can have an impact on public health.

INTRODUCTION

Escherichia coli is a Gram-negative commensal bacterium that normally resides in the digestive tract of humans and animals which is used as an indicator of the ESBL gene in an individual and can transvert the gene in other bacterial species (Effendi et al., 2022). Extended spectrum beta-lactamase (ESBL) is an enzyme produced by Enterobacteriaceae which has experienced antimicrobial resistance (AMR) which can hydrolyze third generation cephalosporins including cefotaxime, ceftazidim ceftriaxone and monobactam (Ansharieta et al., 2021). The blaTEM, blaSHV, blaCTX-M and blaOXA genes are the types that often appear to encode ESBL (Wardhana et al., 2021). The blaTEM and blaSHV genes only have a few differences in amino acid substitutions that have unique characteristics carried by transposons, which makes it difficult to treat Enterobacteriaceae ESBL infections (Stone et al., 2023).
       
The presence of the ESBL gene in wild animals were contamination bacterial was contain ESBL gen from humans and animals in environmental pollution, wastewater treatment plants, food, agriculture, fisheries (fertilizer from feces, water, hospital waste and raw vegetables) (Rojas-Sereno et al., 2023; Loayza et al., 2020). The incidence of antibiotic resistance of E. coli in wildlife in Indonesia has been reported in land mammals (Lagerstrom et al., 2021; Nisa et al., 2021), birds (Huy et al., 2021; Umar et al., 2018) and bats (Mustika et al., 2024). Test from 115 samples swab broiler chicken in Indonesia showed that 33, 04% was multi-drug resistance (MDR) and from 65 wastewater samples showed that 36,92% resistance to antibiotics amoxicillin, ampicillin, sulbactam, cefazolin, cefotaxime, ceftazidime, ceftriaxone, cefepime, aztreonam, gentamicin, ciprofloxacin and trimethoprim/sulfamethoxazole (Yanestria et al., 2022). The Escherichia coli isolated from chicken in wet markets showed that was resistant to antibiotics aztreonam, chloramphenicol and gentamicin (Effendi et al., 2021a). CTX-M-15 is the enzyme most widely distributed as the cause of ESBL-producing E. coli, while the aac resistance gene conferring resistance to aminoglycosides (tobramycin and amikacin) and ciprofloxacin is often detected in association with CTX-M-15 (Banerjee et al., 2013). In line with research conducted by Wibisono et al., (2021), 80% (8/10) isolated MDR have gen CTX-M. Gen ESBL produced from E. coli is useful for understanding pathogenesis and public health (Effendi et al., 2022; Zahra et al., 2024). Apart from CTX-M, blaTEM is a gene found as an ESBL E. coli in bats (Graces et al., 2019).
       
It is estimated that there are 230 bat species in Indonesia or around 21% of the bat species in the world. Of these species, 77 species are grouped into the Megachiroptera suborder and 153 species are grouped into the Microchiroptera suborder. Lombok Island is an island that has quite a high diversity of bat species (Mustika et al., 2024). Bats are natural reservoir hosts and a source of infection for several microorganisms and have the potential to become vectors for the spread of zoonotic diseases (Allocati et al., 2016). Several bacteria such as Salmonella spp., Pasturella spp., E. coli, Leptospira sp. and Bartonella spp. has been isolated from bats in various countries around the world (Allocati et al., 2013).
       
Bats are generally found in caves and residential areas (Garces et al., 2019). Caves are a roosting place for several types of bats (Az-Zahra et al., 2023). The presence of bats in caves can act as a key provider of ecosystem energy for organisms in the cave (Medellin et al., 2017). A cave is a space formed by water-dissolving activity and has spatial divisions based on light intensity. The characteristic of caves is the diversity of habitats within them (Wasti et al., 2021). Based on a research survey conducted by Mustika et al., (2024) there are two caves in Lombok that have various bat species, namely Lawah Cave and Saung Pengembur Cave. These two caves are caves that are always visited by foreign and domestic tourists.
       
The proximity of humans and wild animals is often associated with cross-contamination and transmission of ESBL-producing E. coli because transmission from wild animals is often underestimated, even though wild animals are definitely a vector of resistance (Nicolas-Chanoine et al., 2014). The aim of this research is to determine the level of susceptibility to ESBL-producing E. coli in wild bats on the island of Lombok, Indonesia. It is hoped that the research results will illustrate the potential of bats as a reservoir for the spread of ESBL-producing E. coli on public health.

MATERIALS AND METHODS

Ethical approval
 
The ethical clearance committee of the Faculty of Veterinary Medicine at Universitas Airlangga, Indonesia provided consent for the use of animals (No. 1.KEH.046.03.2023).
 
Study area and sample collection
 
The research was conducted from September 2023 to November 2023. Samples were obtained by swabbing the rectum of live bats caught from caves on the island of Lombok, namely Gua Lawah in West Lombok and Saung Pengembur cave in Central Lombok. Bats were caught using mist nets 20 × 20 mm mesh from 4 pm to 10 pm (McDougall et al., 2021). The nets were always monitored and if any bats were caught in the net they were taken periodically and placed in the cage. Bats caught were handled for rectal swabs. The sampling in this research was approved by the West Nusa Tenggara Natural Resources and Conservation Agency.
       
Sample collection was carried out by cleaning the hairs around the anus using 70% isopropyl alcohol to avoid bacterial contamination from the hair, A sterile cotton swab was inserted into the rectum and rotated for a few moments to ensure that bacteria adhered to the cotton swab (Adesiyun et al., 2009). The swab were placed in transport media (Oxoid, UK) to be taken to the laboratory.
 
Isolation and identification of E. coli
 
Using Eosin Methylene Blue Agar (EMBA) medium (HI MEDIA M317), E. coli bacteria were isolated by inoculating sample on media and then incubating for 18 to 24 hours at 37°C. Gram staining and the biochemical assays. Indole, Methyl red, Voges-proskauer, citrate (IMVIC) and H2S were used to identify E. coli (Dameanti et al., 2023; Debbarma et al., 2023). Bacterial isolation and sensitivity test were done at the laboratory of bacteriology, Faculty of Veterinary Medicine, Airlangga University.
 
Antibiotic sensitivity test
 
The sensitivity test used the disk diffusion method (diffusion test) on Mueller-Hinton Agar (MHA) media (HiMedia M173) adapted to the Clinical Laboratory Standards Institute (CLSI) 2020. The antibiotic disk (Oxoid, England) used in this study belonged to seven classes, including amoxicillin 25 µg (AML) (Oxoid, UK), ciprofloxacine 5 µg (CIP) (Oxoid, UK), sulfamethoxazole/trimethoprim 25 µg (SXT) (Oxoid, UK), tetracycline 30 µg (TE) (Oxoid, UK), gentamicin 10 µg (CN) (Oxoid, UK), cefotaxime 30 µg (CTX) (Oxoid, UK), azithromycin 15 µg (AZM) (Oxoid, UK). One to two colonies were taken from EMBA media using a sterile tube, then placed in physiological NaCl and opacity adjusted to Mc Farland standard 0.5 (1.5 × 108 CFU/ml). A loopful of bacterial suspension was smeared on the mueller hinton agar (MHA) media all over with a sterile swab. Incubated the plate  in an aerobic environment for 16-18 hours at 35°C and interpretation of the findings was done using CLSI 2020 to modify the inhibitory zone’s diameter (Foti et al., 2023; Debbarma et al., 2024). When bacteria in an isolate were resistant to three or more distinct antibiotic classes, the isolate was deemed Multidrug Resistance (MDR). Presumptive ESBL is known if there are bacterial resistance to ≥3 types of antibiotics from different groups (Wibisono et al., 2020).
 
blaTEM gene detection
 
Presumptive ESBL strains were then continued with molecular screening for  the blaTEM gene by DNA extraction using QIAamp® DNA kit (QIAGEN, Germany). blaTEM primers used in this study can be seen in Table 1. Thermal cycle pre-denaturation temperature was 96°C for 5 minutes followed by denaturation for 1 minute at 96°C, 35 cycles of annealing at 58°C for 1 minute and extension at 72°C for 1 minute. Amplification ended with final extension at 72°C for 10 minutes. After that, the amplicons were visualized by electrophoresis using 2% agarose gel. PCR test was taken in gastrointestinal laboratoty, Institute of Tropical Disease, Airlangga University.
 

Table 1: Primer arrangement used in the PCR method.

RESULTS AND DISCUSSION

The result of isolation and identification of Escherichia coli showed that 97 (71.85%) were positive E. coli from 135 sampeles of rectum swabs based on morphological culture, Gram staining and biochemical tests (Table 2). E. coli produce metallic green bacterial colonies on EMBA media (Fig 1). Gram staining revealed the presence of Gram negative short rods. The IMViC test revealed bacterial strains to be positive for indole, MR and motility, but negative for indole and citrate utilization tests, motile MR positive thus confirming isolates to be E.coli by biochemical tests.
 

Table 2: Results of isolation and identification of E. coli.



Fig 1: E. coli bacteria purified after biochemical tests.


       
Based on the outcomes of the antibiotic resistance test, the antibiogram revealed that, out of the 97 E. coli isolates, 20 (20.62%) were resistant to one class of antibiotics and 24 (24.74%) resistant to two classes. Twelve isolates (12.37%) that exhibited resistance to three or four different antibiotic classes were identified as MDR (Table 3 and Fig 2). The dominant antibiotic resistance pattern was CIP - AML - SXT - AZM - TE with 6 isolates (Table 4). Following the detection of the blaTEM gene, it was determined that 12 E. coli isolates were multidrug resistant based on the findings of the sensitivity test. Two E. coli isolates tested positive for blaTEM based on the results of the electrophoresis. The two isolates are with sample codes 2.31 and 2.70 (Fig 3).
 

Table 3: Zone of inhibition in the sensitivity test using the disk diffusion test method.


 

Fig 2: Sensitivity test of E. coli bacteria isolates.



Table 4: Results of identification of multidrug resistant E. coli bacteria.


 

Fig 3: Detection of the blaTEM gene encoding ESBL in E. coli bacteria from bat rectal swabs.


       
Research into antibiotic resistance in wild animals has recently begun to be carried out because the uncontrolled movement of these wild animals can have serious impacts on public health. AMR research in wild animals, such as bats, can provide an overview of the exposure received by wild animals and the potential for spread of ESBL from wildlife to the environment. Bats have the ability to fly an average distance of 26.14 km (0.33-97.57 m) (Randhawa et al., 2020). The small amount of research on wild animals can make the picture of the spread of ESBL in the environment still not very clear, there are only a few studies on MDR from bats in Indonesia, including research conducted by Masrukhin et al., (2021) on bat isolates in Gunung Halimun Salak National Park.
       
Multidrug resistance to antibiotics in Gram-negative bacteria resulting from treatment or exposure to antibiotics in the environment can be found in E. coli, Enterobacter spp., Pseudomonas aeruginosa, Klebsiella pneumoniae and Acinebacter baumannii (Ramatla et al., 2024; Riwu et al., 2022). The macrolide antibiotic Azithromycin is an antibiotic that often appeared as a cause of resistance in this study. Beta-lactam and macrolide antibiotics are antibiotics that are often used to treat bacterial respiratory tract infections in humans (Ríos et al., 2024). In Japan, from 82 nasal swab samples from human patients, it was found that 23 Klebsiella pneumonia bacteria and E. coli had the ESBL gene, 15 E. coli isolates from 44 patients were known to produce ESBL, where the proportion of administration using carbapenem, cephem and macrolide antibiotics was very significant (Matsumoto et al., 2023). From food product etawa milk in Indonesia found that 100% of samples was DDST test were found blaTEM gene (Tyasningsih et al., 2022). mefB is an ARGs of E. coli in poultry in kwara state, north central nigeria which mutates to cause resistance to macrolide antibiotics (erythromycin, azithromycin and tylosin) (Al-Mustapha et al., 2023). The antibiotic azithromycin is a macrolide antibiotic which is widely used for therapy in humans and livestock. The macrolide antibiotic functions to inhibit bacterial proteins between gram-negative and gram-positive bacteria. This antibiotic is used for the treatment of respiratory and digestive, genital and skin infections (Monahan et al., 2023).
       
Of the 97 E. coli isolates, 25 samples were found to be resistant to the antibiotic amoxicillin. Amoxicillin is a beta-lactam antibiotic that is used to treat pathogenic bacteria by inhibiting cell wall synthesis. Amoxicillin is often used for treatment because it is more easily absorbed than other antibiotics (Zhang et al., 2023). The high incidence of AMR on cattle farms can occur in cows that have not yet been weaned, because the immune system is not yet fully formed and antibodies from colostrum have begun to decline so the risk of infection becomes very high (Merle et al., 2023). Research conducted by Ningtyas et al., (2024) on water sources in chicken farms in West Lombok showed that the isolated E. coli bacteria were resistant to penicillin (100%) and tetracycline (75%) antibiotics, the researchers believe that the bacteria that have developed resistance come from chickens on the farm. The similarity of antibiotic resistance of E. coli bacteria in humans, animals and the environment show that the closeness between humans, animals and the environment makes the circulation of antibiotic resistance unavoidable (Barker et al., 2023).
       
All samples in this study showed susceptibility to the antibiotics cefotaxime (100%) and gentamicin (98.97%). The antibiotic gentamicin is an aminoglycoside antibiotic which has recently been used to treat Gram-negative and Gram-positive bacterial infections in the field of veterinary medicine. Amoxicillin and cefotaxime are indicators of resistance to the beta-lactam class of antibiotics which can carry the ESBL gene (Paramitadevi et al., 2024). In contrast to the results of research on isolates from bats in Peru, more than 60% of the isolates were resistant to second and third generation penicillin and cephalosporin antibiotics (Benavides et al., 2022). The discovery of this pattern of antibiotic resistance is important for antibiotic management and the need for health service providers to choose the antibiotics that will be used for therapy as an effort to maximize treatment (Oboodi et al., 2024; Farizqi et al., 2023).
       
The discovery of E. coli bacteria in samples of bats that are MDR in this study and were detected to have the blaTEM gene is very risky for public health because bats are wild animals that can live anywhere and defecate any where so the risk of bat feces contamination of the environment is very large. Extended-spectrum beta-lactamase (ESBL) can be caused by the resistance of E. coli bacteria to beta-lactam antibiotics or bacterial plasmids that are resistant to aminoglycoside antibiotics, trimethoprim, quinolones, sulphonamides, chloramphenicol  and tetracycline (Haddadin et al., 2023). The Temoneria (TEM) and sulfhydryl variable (SHV) genes were genes that were very frequently found in patients in hospitals from 1980-1990, then cefotaxime (CTX-M) became dominant due to the widespread use of third-generation cephalosporins (Nahar et al., 2023). Of the 12 test samples that experienced multidrug resistance, two samples were found to be positive for the blaTEM gene. In line with research on bats in Nigeria, the blaTEM and multi-DHA genes were the predominant genes detected in resistant E. coli bacteria (Modupe et al., 2022).
       
In Indonesia, the blaTEM gene is the dominant gene (70%) in ESBL E. coli in broiler chickens (Effendi et al., 2021b), but it is different in layer chickens where blaCTX is the dominant gene that appears as the cause of ESBL followed by blaTEM and blaSHV (Wibisono et al., 2020). The blaTEM gene confers resistance to early cephalosporin antibiotics and penicillins by excessively hydrolyzing the β-lactam ring and causing resistance to carbapenems and cephamycin (Ibrahim et al., 2023). The blaTEM gene (83.8%) is the gene that often appears as the cause of ESBL in poultry in North Central Nigeria, samples show MDR to the antibiotics sulfamethoxazole, trimethoprim, tetracycline and ampicillin (Al-Mustapha et al., 2023). The blaTEM-1B gene was 65% (n=13) the gene that appeared as the gene causing resistance to E. coli isolates from dogs in San Francisco and 70% (n=25) in dog owners, followed by blaTEM104 in one person without appearing in dogs lookout (Walas et al., 2024).
       
The blaTEM gene can be found on DNA plasmids, the presence of the gene on the plasmid can facilitate gene transfer between different bacteria, other beta-lactamase genes are derivatives of blaTEM (Sah et al., 2024). Data on antibiotic resistance and ESBL genes detected in this study can be used as reference data as literature for doctors and veterinarians as an illustration of AMR and ESBL in wild animals which can contaminate the human environment.

CONCLUSION

The level of antibiotic resistance in wildlife reflects the level of resistance in the environment, humans and animals. blaTEM is a gene detected from non-human E. coli isolates in Lombok, Indonesia. The one health approach is very important to implement for human, animal and environmental health as a step to prevent the spread of the discovered ESBL genes. Genetic characterization of ESBL genes can be used to identify potential zooanthroponotic and zoonotic risks that are beneficial to public health and bat health.

ACKNOWLEDGEMENT

Researchers would like to thank the Faculty of Veterinary Medicine, Airlangga University for all the facilities provided during conducting research. This research was supported by funding for Doctoral Dissertation research from the Center for Higher Education Fund (BBPT) and Indonesia Endowment Funds for Education (LPDP), with grant number from Keputusan Kepala Pusat Layanan Pembiayaan Pendidikan Kementerian Pendidikan, Kebudayaan, Riset, dan Teknologi Nomor 00087/J5.2.3./BPI.06/9/2022. BPI ID Number: 202209090573.

CONFLICT OF INTEREST

All authors declare no conflict of interest.

REFERENCES


  1. Adesiyun, A.A., Stewart-johnson, A., Thompson, N.N. (2009). Isolation of enteric pathogensy from bats in Trinidad. Journal of Wildlife Diseases. 45: 952-961. doi: 10.7589/ 0090-3558-45.4.952.

  2. Allocati, N.,  Petruccil, A.G., Di Giovanni, P.,  Masulli, M., Di Ilio, C., De Laurenzi, V. (2016). Bat-man disease transmission: zoonotic pathogens from wildlife reservoirs to human populations. Cell Death Discovery. 2(2016): 66048. doi: 10.1038/cddiscovery.2016.48.

  3. Allocati, N., Masulli, M., Alexeyev, M.F., Di Ilio, C. (2013). Escherichia coli in Europe: An overview. International Journal of Environmental Research and Public Health. 10: 6235- 6254. doi: 10.3390/ijerph10126235. 

  4. Al-Mustapha, A., Raufu, I.A., Ogundijo, O.A., Odetokun, I.A., Tiwari, A., Brouwer, M.S.M., Adetunji, V., Heikinheimo, A. (2023). Antibiotic resistance genes, mobile elements, virulence genes and phages in cultivated ESBL-producing Escherichia coli of poultry origin in Kwara State, North Central Nigeria. International Journal of Food Microbiology. 389: 11086. doi: 10.1016/j.ifoodmicro.2023.110086.

  5. Ansharieta, R., Effendi, M.H., Plumeriastuti, H. (2021). Genetic Identification of shiga toxin encoding from cases of multidrug resistance (MDR) Escherichia coli Isolated from Raw Milk. Tropical Animal Science Journal. 44: 10- 15. doi: 10.5398/tasj.2021.44.1.10.

  6. Az-Zahra, N., Alifah, F., Noormafaza, A., Nurrohimah, K., Novitasari, N., Maharani, F.E., Oktaviani, V.I., Jasinda, R.C., Azzahra, S.A., Siagian, S.D.A., Prakarsa, T.B.P. (2023). Cave bats (Yangochiroptera and Yinpterochiroptera) in gunung sewu geopark: Study of Karst caves in Wonogiri Regency. Indonesian Journal of Bioscience. 1: 15-23. doi:10.21831/ijobi.v1i1.107.

  7. Banarjee, R., Strahilevitz, J., Johnson, J.R., Nagwekar, P.P., Schora, D.M., Shevrin, I., Du, H., Peterson, L.R., Robicsek, A. (2013). Predictors and molecular epidemiology of community-Onset Extended-Spectrum β-Lactamase- producing Escherichia coli Infection in a mid western community. Infection Control and Hospital Epidemiology. 34: 947-953. doi: 10.1086/671725.

  8. Barker, T., Capone, D., Amato, H.K., Clark, R., Henderson, A., Holcomb, D.A. (2023). Public toilets have reduced enteric pathogen hazards in San Francisco. PLOS Water. 2: e0000152. doi: 10.1101/2023.02.10.23285757.

  9. Benavides, J.A., Godreuil, S., Opazo-Capurro, A., Mahamat, O.O., Oravcova, K., Streicker, D.G., Shiva, C. (2022). Long- term maintenance of multidrug-resistant Escherichia coli carried by vampire bats and shared with livestock in Peru. Science of the Total Environment. 810: 152045. doi: 10.1016/j.scitotenv.2021.152045.

  10. Clinical and Laboratory Standard Institute (CLSI) (2020) Performance Standards for Anti-Microbial Susceptibility Testing. 30th Edition, M100. https://clsi.org/media/3481/m100ed30_sample.pdf.

  11. Dameanti, F.N.A.E.P., Yanestria, S.M., Widodo, A., Effendi, M.H., Plumeriastuti, H., Tyasningsih, W., Sutrisno, R., Akramsyah, M.A. (2023). Incidence of Escherichia coli producing Extended-spectrum beta lactamase in wastewater of dairy farm in east Java, Indonesia. Biodiversitas. 24: 1143- 1150. doi: 10.13057/biodiv/d240254. 

  12. Debbarma, B., Ralte, L., Motina, E., Lalmuanpuia, J., Tolenkhomba, T.C. and Roychoudhury, P. (2024). Comparative Study on the Prevalence of Escherichia coli and its Antibiogram in Saum from three different storage places in House hold at Mizoram. Asian Journal of Dairy and Food Research. 43(2): 327-332. doi: 10.18805/ajdfr.DR-2104.

  13. Debbarma, M., Deka, D. and Roychoudhury, P. (2023). Enumeration, serotypes and virulence genes associated with shigatoxigenic (STEC) and enterotoxigenic (ETEC) escherichia coli from beef and chicken of mizoram, India. Asian Journal of Dairy and Food Research. 42(2): 247-254. doi: 10.18805/ ajdfr.DR-1950. 

  14. Effendi, M.H., Faridah, H.D., Wibisono, F.M., Wibisono, F.J., Nisa, N., Fatimah, Ugbo, E.N. (2022). Detection of virulence factor encoding genes on Escherichia coli from broiler chicken in Blitar District, Indonesia. Biodiversitas. 23: 3437-3442.  doi: 10.13057/biodiv/d230716.

  15. Effendi, M.H., Tyasningsih, W., Yurianti, Y.A., Rahmahani, J., Harijani, N., Plumeriastuti, H. (2021a). Presence of multidrug resistance (MDR) and extended-spectrum beta-lactamase (ESBL) of Escherichia coli isolated from cloacal swabs of broilers in several wet markets in Surabaya, Indonesia. Biodiversitas. 22: 304-310. doi: 10.13057/biodiv/d220137.

  16. Effendi, M.H., Wibisono, F.J., Witaningrum, A.M., Permatasari, D.A. (2021b). Identification of BlaTEM and BlaSHV genes of extended spectrum beta lactamase (ESBL) Producing Escherichia coli from broiler chicken in Blitar, Indonesia. Systematic Reviews in Pharmacy. 12: 976-981. doi: 10.31838/srp.2021.1.136.

  17. Farizqi, M.T.I., Effendi, M.H., Adikara, R.T.S., Yudaniayanti, I.S., Putra, G.D.S., Khairullah, A.R., Kurniawan, S.C., Silaen, O.S.M., Ramadhani, S., Millannia, S.K., Kaben, S.E., Waruwu, Y.K.K. (2023). Detection of extended-spectrum β- lactamase-producing Escherichia coli genes isolated from cat rectal swabs at Surabaya Veterinary Hospital, Indonesia. Veterinary World. 16: 1917-1925. doi: 10.14202/vetworld.

  18. Foti, M., Grasso, R., Fisichella, V., Mascetti, A., Marco, C., Grasso, M., Spena, M.T. (2023). Antimicrobial resistance in physiological and potentially pathogenic bacteria Isolated in Southern Italian Bats. Animals. 13: 966. doi: 10.3390/ ani13060966.

  19. Garces, A., Correia, S., Amorim, F., Pereira, J.E., Igrejas, G. Poeta, P. (2019). First report on extended-spectrum beta-lactamse (ESBL) producing Escherichia coli from European free- tailed bats (Tadarida teniotis) in Portugal: A one-health approach of a hidden contamination proble. Journal of Hazardous Materials. 370: 219-224. doi: 10.1016/j.jhazmat. 2017.12.053.

  20. Haddadin, R.N., Collier, P.J., Haddadin, S. (2023). Phenothypic ESBL and non-phenotypic ESBL isolated of Klebsiella pneumoniae exhibit differing responses to induced antimicrobial resistance and subsequent antimicrobial cross-resistance. Journal of Applied Microbiology. 134: lxac082. doi: 10.1092/jambio/lxac082.

  21. Huy, H.L., Koizumi, N., Nuradji, H., Susanti, Noor, S.M., Dharmayanti, N.P.L.I., Haga, T., Hirayama, K., Miura, K. (2021). Antimicrobial resistance in Escherichia coli isolated from brown rats and house shrews in markets, Bogor, Indonesia. The Journal of Veterinary Medical Science. 83: 531-534. doi: 10.1292/jvms.20-0558.

  22. Ibrahim, D.R., Dodd, C.E.R., Stekel, D.J., Meshioye, R.T., Diggle, M., Lister, M., Hobman, J.L. (2023). Multidrug-resistant ESBL-producing E. coli in clinical samples from the UK. Antibiotics. 12: 169. doi: 10.3390/antibiotics12010169.

  23. Lagerstrom, K.M. and Hadly, E.A. (2021). The under-investigated wild side of Escherichia coli: genetic diversity, pathogenecity and antimicrobial resistance in wild animals. Proceedings: Biological Sciences. 288: 20210399. doi: 10.1098/rspb.2021.0399.

  24. Loayza, F., Graham, J.P., Trueba, G. (2020). Factors obscuring the role of E. coli from domestic animals in the global antimicrobial resistance crisis: An Evidence-based Review. International Journal of Environmental Research and Public Health. 17: 3061. doi: 10.3390/ijerph17093061.

  25. Masrukhin, Saputra, S., Rizal, S., Sushadi, P.S., Supriatna, N. (2021). Identification and antibiotic resistance profile of bacteria from fruit bat (Chironax melanochepalus). Advances in Biological Sciences Research. 14: 478-484. doi: 10.2991/absr.k.210621.081.

  26. Matsumoto, H., Komiya, K., Ichihara, S., Nagaoka, Y., Yamanaka, M., Nishiyama, Y., Hiramatsu, K., Kadota, J.I. (2023). Factors associated with Extended-spectrum â-lactamase

  27. -producing enterobacteria Isolated from respiratory samples. Internal Medicine. 62: 2043-2050. doi: 10.2169/internalmedicine.0690-22.

  28. McDougall, F.K., Boardman, W.S.J., Power, M.L. (2021). Characterization of beta-lactam-resistant Escherichia coli from Australian fruit bats indicates anthropogenic origin. Microbial Genomics. 7: 000571. doi: 10.1099/mgen.0.000571.

  29. Medellin, R.A., Wiederholt, R., Lopez-Hoffman, L. (2017). Conservation relevance of bat caves for biodiversity and ecosystem services. Biological Conservation. 211: 45-50. doi: 10.1016/j.biocon.2017.01.012.

  30. Merle, R., Weise, S., Gorisek, L., Baer, J., Robe, C., Frese, A., Jensen, K.C. (2023). The therapy frequency of antibiotics and phenothypical resistance of Escherichia coli in calf rearing sites in Germany. Frontiers in Veterinary Science. 10: 1152246. doi: 10.3389/fvets.2023.1152246.

  31. Modupe, A.O., Olifunke, O.A., Abike, T.O., Oluwayemisi, O.A., Oladiran, F. (2022). Molecular characterization of resistance and virulance genes in Escherichia coli isolated from bats (Eidolon helvum) faeces in onsu state, Nigeria. Journal of Advance in Microbiology. 22: 37-48. doi: 10.9734/JAMB/2022/V22i230436.

  32. Monahan, C., Morris, D., Nag, R., Cummins, E. (2023). Risk ranking of macrolide antibiotics-release levels, resistance formation potential and ecological risk. Science of the Total Environment. 859: 160022. doi: 10.1016/j.scitotenv.2022.160022.

  33. Mustika, Y.R., Kinasih, K.N., Effendi, M.H., Puspitasari, Y., Kurniawan, S.C., Khairullah, A.R., Samodra, M.E.E., Hasib, A., Agustin, A.L.D., Moses, I.B., Silaen, O.S.M. (2024). Molecular detection of extended-spectrum β- lactamase-producing Escherichia coli from bat caves on Lombok Island. Open Veterinary Journal. 14: 699-706. doi: 10.5455/OVJ.2024.v14.i2.10.

  34. Naelasari, D.N., Koendhori, E.B., Dewanti, L., Sulistiawati, Sarassari, R., Kuntaman, K. (2018). The prevalence of Extended spectrum β-lactamase (ESBL) producing gut bacterial floral among patients in dr. Soetomo hospital and primary health care in Surabaya. Folia Medica Indonesiana.  54: 256-262. doi: 10.20473/fmi.v54i4.10708.

  35. Nahar, A., Islam, A.K.M.A., Islam, M.N., Khan, M.K., Khan, M.S., Rahman, A.K.M.A., Alam, M.M. (2023). Molecular characterization and antibiotic resistance profile of ESBL- producing Escherichia coli isolated from healthy cow raw milk in smallholder dairy farms in Bangladesh. Veterinary World. 16: 1333-1339. doi: 10.14202/vetworld.2023.1333-1339.

  36. Nicolas-Chanoine, M.H., Bertrand, X., Madec, J.Y. (2014). Escherichia coli ST131, an intriguing clonal group. Clinical Microbiology Reviews. 27: 543-574. doi: 10.1128/CRM. 00125-13.

  37. Ningtyas, N.S.I., Agustin, A.L.D., Hr, M., Fibrianti, B.S. (2024). Resistance of Escherichia coli Isolated from water sources on west lombok farms to antibiotics. Veterinary Medicine Journal. 35: 1-8. doi: 10.20473/mkh.v35i1.2024.1-8.

  38. Nisa, S.A., Safitri, R.A.N., Inayah, N., Nditasari, A., Purwantisari, S., Ferniah, R.S., Achmadi, A.S., Nugraha, T.P., Saputra, S. (2021). Potential zoonotic faecal bacteria from sunda porcupine (Hystrix javanica) and their antimicrobial resistance profiles. Microbiology Indonesia. 15: 61-68. doi: 10.5454/mi.15.2.4.

  39. Oboodi, R., Hashemi, Z., Jaafarzadeh, E., Yazdani, N., Barzegar, H. (2024). Bacterial etiology and antibiotic susceptibility profile in neonatal sepsis. Archives of Pediatric Infectious Diseases. 12: e136487. doi: 10.51812/apid-136487.

  40. Pramitadevi, Y.V., Priadi, C.R., Rahmatika, I., Rukmana, A., Moersidik, S.S. (2024). Resistance profil of Escherichia coli isolated from stool, feed and compost sources antibiotics in Sukabumi. E3S Web of Conferences. 485: 07001. doi: 10.1051/e3sconf/202448507001.

  41. Ramatla, T., Tutubala, M., Motlhaping, T., de Wet, L., Mokgokong, P., Thekisoe, O., Lekota, K. (2024). Molecular detection of Shiga toxin and extended-spectrum beta-lactamase (ESBL)-producing Escherichia coli isolates from sheep and goat. Molecular Biology Reports. 51: 57. doi: 10.1007/ s11033-023-08987-0.

  42. Randhawa, N., Bird, B.H., VanWormer, E., Sijali, Z., Kilonzo, C., Msigwa, A., Ekiri, A.B., Samson, A., Epstein, J.H., Wolking, D.J., Smith, W.A., Martinez-lopez, B., Kazwala, R., Mazet, J.A.K. (2020). Fruit bats in flight: A look into the movements of the ecologically important eidolon helvum in Tanzania. One Health Outlook. 2: 1-14. doi: 10.1186/s42522-020-00020-9.

  43. Ríos, E., Pérez, M., Sanz, J.C., Delgado-Iribarren, A., Rodríguez- Avial, I. (2024). Efficacy of delafloxacin alone and in combination with cefotaxime against cefotaxime non- susceptible invasive isolates of Streptococcus pneumoniae. Revista Española de Quimioterapia. 37: 158-162. 

  44. Riwu, K.H.P., Effendi, M.H., Rantam, F.A., Khairullah, A.R., Widodo, A. (2022). A Review: Virulence factors of Klebsiella pneumonia as emerging infection on the food chain. Veterinary World. 15(9): 2172-2179. doi: 10.14202/vetworld.2022.2172-2179.

  45. Rojas-Sereno, Z.E., Streicker, D.G., Suarez-Yana, T., Lineros, M., Yung, V., Godreuil, S., Benadives, J.A. (2023). Detection of antimicrobial-resistant Enterobacterales in insectivorous bats from Chile. Royal Society Open Science. 10: 231177. doi: 10.1098/rsos.231177.

  46. Sah, R.K., Dahal, P., Parajuli, R., Giri, G.R., Tuladhar, E. (2024). Prevalence of blaCTX-M nad blaTEM genes in cefotaxime-resistance Escherichia coli recovered from tertiary care at central nepal: A descriptive cross-sectional study. Canadian Journal of Infectious Diseases and Medical Microbiology. 2024: 5517662. doi: 10.1155/2024/5517622.

  47. Stone, T.J., DeWitt, M., Johnson, J.W., Beardsley, J.R., Munawar, I., Palavecino, E., Luther, V.P., Ohl, C.A., Williamson, J.C. (2023). Analysis of infections among patients with historical culture positive for extended-dpectrum beta- lactamase (ESBL) producing Escherichia coli or Klebsiella pneumoniae: Is ESBL-targeted therapy always needed? Antimicrobial Stewardship and Health care Epidemiology. 3: e47. doi: 10.1017/ash.2022.363. 

  48. Tyasningsih, W., Ramandinianto, S.C., Ansharieta, R., Witaningrum, A.M., Permatasari, D.A., Wardhana, D.K., Effendi, M.H., Ugbo, E.N. (2022). Prevalence and antibiotic resistance of Staphylococcus aureus and Escherichia coli isolated from raw milk in East Java, Indonesia. Veterinary World. 15(8): 2021- 2028. doi: 10.14202/vetword.2022.2021-2028.

  49. Umar, S., Maiyah, A.T., Shareef, M., Qadir, H., Nisa, Q.U., Abbas, S. (2018). Susseptibility of avian pathogenic Escherichia coli from Zoo birds in Indonesia to antibiotics and desinfectants. Journal of Pharmaceutical Sciences. 31: 593-598.

  50. Walas, W., Muller, N.F., Parker, E., Henderson, A., Capone, D., Brown, J., Barker, T., Graham, J.P. (2024). Application of phylodynamics to identify spread of antimicrobial- resistant Escherichia coli between human and cannies in a urban environment. Science of the Total Environment. 916: 170139. doi: 10.1016/j.scitotenv.2024.170139.

  51. Wardhana, D.K., Safitri, D.A., Annisa, S., Harijani, N., Estoepangestie, A.T.S., Maghfiroh, L. (2021). Prevalence of Extended- Spectrum Beta-Lactamases in producing Escherichia coli in beef sold in traditional markets in Surabaya, Indonesia. Biodiversitas. 22: 2789-2793. doi: 10.13057/biodiv/ d220542.

  52. Wasti, I.G., Khan, F.A.A., Bernard, H., Hassan, N.H., Fayle, T., Seelan, J.S.S. (2021). Fungal communities in bat guano, speleothem surfaces and cavern water in Madai cave, Northern Borneo (Malaysia). Mycology. 12: 188-202. doi: 10.1080/21501203.2021.1877204.

  53. Wibisono, F.J., Sumiarto, B., Untari, T., Effendi, M.H., Permatasari, D.A., Witaningrum, A.M. (2020). Short Communication: Pattern of antibiotic resistance on extended-spectrum beta-lactamases genes producing Escherichia coli on laying hens in Blitar, Indonesia. Biodiversitas. 21: 4631- 4635.

  54. Wibisono, F.J., Sumiarto, B., Untari, T., Effendi, M.H., Permatasari, D.A., Witaningrum, A.M. (2021). Molecular identification of CTX gene of extended spectrum beta-lactamases (ESBL) producing Escherichia coli on layer chicken in Blitar, Indonesia. Journal of Animal and Plant Sciences. 31: 954-959. doi: 10.36899/JAPS.2021.4.0289.

  55. Yanestria, S.M., Dameanti, F.N.A.E.P., Musayannah, B.G., Pratama, J.W.A., Witaningrum, A.M., Effendi, M.H., Ugbo, E.N. (2022). Antibiotic resistance pattern of Extended- Spectrum β-Lactamase (ESBL) producing Escherichia coli isolated from broiler farm environment in Pasuruan district, Indonesia. Biodiversitas. 23: 4460-4465. doi: 10.13057/biodiv/d230911.

  56. Zahra, R.L.A., Prayudi, S.K.A., Suprayogi, T.W., Wardhana, D.K. Effendi, M.H., Khairullah, A.R. and Kurniawan, S.C. (2024). Identification of the genotypes of extended- spectrum β-lactamase producing Escherichia coli in the small Intestine of broiler chickens at a traditional market in surabaya, Indonesia. Asian Journal of Dairy and Food Research. doi: 10.18805/ajdfr.DRF-376.

  57. Zhang, J., Wu, M., Diao, S., Zhu, S., Song, C., Yue, J., Martins, F.S., Zhu, P., Lv, Z., Zhu, Y., Yu, M., Sy, S.K.B. (2023). Pharmacokinetic/pharmacodynamic evaluation of aztreonam/amoxicillin/clavulanate combination against New Delhi Metallo-β-lactamase and serine- β-lactamase co-producing Escherichia coli and Klebsiella pneumoniae. Pharmaceutics. 15: 251. doi: 10.3390/pharmaceutics15010251.
Reviewed By

Download Article
In this Article
    Contact us
    Follow us

    Editorial Board

    View all (0)