Prevalence and Phenotypic and Genotypic Patterns of Antibiotic Resistance of <i>Acinetobacter baumannii</i> Strains Isolated from Fish, Shrimp, and Lobster Samples

Hasiri, Zahra; Rahimi, Ebrahim; Momtaz, Hassan; Shakerian, Amir

doi:https://doi.org/10.1155/2023/6245225

Journal of Food Processing and Preservation

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Abstract Introduction Materials and Methods Results Discussion Conclusion Data Availability Conflicts of Interest Authors’ Contributions References Copyright Related Articles

Research Article | Open Access

Volume 2023 | Article ID 6245225 | https://doi.org/10.1155/2023/6245225

Prevalence and Phenotypic and Genotypic Patterns of Antibiotic Resistance of Acinetobacter baumannii Strains Isolated from Fish, Shrimp, and Lobster Samples

Zahra Hasiri,¹Ebrahim Rahimi,¹Hassan Momtaz,²and Amir Shakerian³

Academic Editor: Ali Akbar

Received18 Oct 2022

Revised15 Jan 2023

Accepted17 May 2023

Published25 May 2023

Abstract

Acinetobacter baumannii has emerged as a significant hospital pathogen, quickly becoming resistant to commonly prescribed antimicrobials. The present survey was done to evaluate the prevalence, antibiotic resistance pattern, and distribution of antibiotic resistance genes amongst the A. baumannii strains isolated from fish, shrimp, and lobster samples. Four-hundred and fifty seafood samples (100 g each) were collected from Shiraz, Iran. Acinetobacter baumannii was determined using culture and biochemical tests. Pattern of antibiotic resistance and distribution of antibiotic resistance genes were determined using the disk diffusion and polymerase chain reaction, respectively. A. baumannii contamination rate amongst the examined seafood samples was 4.44%, with the higher contamination rate of fish samples (7.85%). A. baumannii isolates harbored the maximum resistance rate against tetracycline (85%), ampicillin (85%), gentamicin (70%), and erythromycin (60%). Resistance rates toward trimethoprim-sulfamethoxazole, ciprofloxacin, ceftazidime, and azithromycin were 55%, 45%, 35%, and 30%, respectively. The minimum rates of resistance were obtained against imipenem (10%) and chloramphenicol (15%). The most commonly detected antibiotic resistance genes were bla_CITM (75%), bla_SHV (70%), tetA (70%), qnrA (55%), bla_VIM (50%), and aac(3)-IV (50%). aadA1, sul1, dfrA1, qnr, bla_VIM, bla_SIM, bla_OXA-51, bla_OXA-23, and bla_OXA-58 genes were detected in 40%, 30%, 45%, 50%, 35%, 25%, 30%, and 20% of isolates, respectively. The role of seafood samples as a potential reservoirs of antibiotic-resistant A. baumannii strains was determined. However, further investigations are required to identify additional epidemiological features of A. baumannii in seafood samples.

1. Introduction

Seafoods are noteworthy nutrient, marketing, and economic foodstuffs worldwide. Seafoods are rich sources of different nutrient molecules, including proteins, minerals, fatty acids, and even vitamins [1]. Their routine consumption will decrease the risk of diverse metabolic and nutrition diseases [2]. However, seafood human manipulation at the ports and also their own filter feeding manner may increase the risk of microbial contamination and subsequent foodborne diseases [3].

Acinetobacter baumannii (A. baumannii) is a Gram-negative, rod-shaped, aerobic, nonfermentative, catalase-positive, and oxidase-negative bacterium with ubiquitous and saprophytic nature [4, 5]. A. baumannii have appeared as an imperative nosocomial pathogen because of its high survival rate in the environment [6]. In the hospital cases, A. baumannii is responsible for the occurrence of diverse infections, particularly meningitis, endocarditis, pneumonia, peritonitis, skin, burn and wound, urinary and respiratory tract infections, and bacteremia [7]. Rendering its high resistance to environmental conditions, A. baumannii can exist in water and foodstuffs [8]. A. baumannii strains have also been rarely isolated from meat [9], vegetable [10], and milk [11] samples. Some Acinetobacter species are also responsible for different types of infections in marine animals and cause economic burden to the fish, shrimp, and lobster farming [12, 13]. However, information about the A. baumannii clonality in food is scarce, which may bold the role of foods in transmission of this pathogen into the human population.

Many studies showed an emergence of antibiotic resistance amongst the A. baumannii strains of different sources [14]. In this regard, high resistance rate of A. baumannii strains against diverse antibiotic groups, including tetracycline, penicillins, aminoglycosides, quinolones, macrolides, carbapenems, and phenicols, has been reported several times [15]. Many studies showed that the genes that encode resistance toward streptomycin (aadA1), gentamicin (aac(3)-IV), tetracyclines (tetA and tetB), sulfonamide (sul1), beta-lactams (bla_CITM and bla_SHV), chloramphenicol (cmlA and cat1), trimethoprim (dfrA1), quinolones (qnrA), carbapenems (bla_VIM, bla_IMP, and bla_SIM), and oxacillins (OXA-51-like, OXA-23-like, OXA-24-like, and OXA-58-like) are mainly responsible for the occurrence of antibiotic resistance [16, 17]. Determination of the antibiotic resistance pattern of A. baumannii strains may help a lot in finding the best therapeutic approaches and changing the infection epidemiology.

Contamination of various type of foods by A. baumannii is largely reported [18–20]. A. baumannii was recovered from various raw meat including sheep, goat, cow, and camel [21–23]. Recently, Ababneh et al. also reported that A. baumannii was recovered from fresh products including vegetables and fruits [24]. However, few studies report the presence of A. baumannii in seafood. Isolated studies have reported the presence of A. baumannii carrying resistance genes (Oxa-23) in some seafood species, but their prevalence has not been determined [25, 26]. In Iran, only one study reported the presence of A. baumannii in seafood, and a low prevalence of 5.6% was found [27]. Regarding the clinical significance of A. baumannii as an emerging foodborne pathogen, thus, the present study was aimed at assessing the prevalence and phenotypic (disk diffusion) and genotypic (detection of antibiotic resistance genes) patterns of antibiotic resistance of A. baumannii strains isolated from fish, shrimp, and lobster samples.

2. Materials and Methods

2.1. Samples

From May to September 2020, 450 seafood samples including shrimp (), fish (), and lobster () samples were randomly collected from fish market centers at Shiraz, Iran. Each sample (100 g from the dorsal muscle) was collected separately in highly hygienic condition using sterile tissue forceps in laboratory tubes containing peptone water solution (Merck, Germany). Samples were healthy and fresh and all were caught from the Persian Gulf, Iran. All samples were transferred to laboratory using cool boxes at 4°C.

2.2. Isolation and Identification of A. baumannii

The A. baumannii strains were isolated by microbial culture and identified using different biochemical tests and polymerase chain reaction (PCR) method. For this purpose, 10 g of seafood meat samples was homogenized in 90 mL of nutrient broth using a stomacher (Stomacher 400 Circulator, Seward, Norfolk, UK) for about 1 min. All media were incubated at 37°C overnight with agitation. Then, 10 μL of enriched media was inoculated onto selective ChromID ESBL agar (bioMérieux, France) and incubated for 24 h at 37°C. White colonies in selective ChromID ESBL agar were considered presumptive A. baumannii and transferred onto tryptic soy agar (TSA, Merck, Germany) plates supplemented with sheep blood (5%, Merck, Germany). Media were incubated for 24 h at 37°C. A. baumannii colonies were further identified using the biochemical tests, including Gram staining, citrate, catalase, oxidase, urease, malonate consumption, sugar oxidation and fermentation, indole production, and motility [28]. Species identification was done using gelatin liquefaction, glucose oxidation, arginine hydrolysis, hemolysis on blood agar, growth at 37°C and 42°C, and chloramphenicol susceptibility test [28]. Final confirmation of A. baumannii isolates was done using the PCR (targeted the 16S-23S ribosomal DNA of A. baumannii) [29]. For this aim, 16S-23S ribosomal DNA was targeted using the forward: 5-CATTATCACGGTAATTAGTG-3 and reverse: 5-AGAGCACTGTGCACTTAAG-3 (208 bp) primers [29].

2.3. Antibiotic Resistance Examination

A. baumannii antibiotic resistance pattern was assessed by the simple disk diffusion. The Kirby-Bauer disk diffusion method on the Mueller-Hinton agar (MHA, Merck, Germany) rendering the Clinical and Laboratory Standard Institute (CLSI) guidelines was applied [30]. A. baumannii resistance was examined against tetracycline (30 μg/disk) (T30), erythromycin (15 μg/disk) (E15), azithromycin (15 μg/disk) (Az15), ceftazidime (30 μg/disk) (Cft30), gentamicin (10 μg/disk) (G10), ciprofloxacin (5 μg/disk) (Cip5), trimethoprim/sulfamethoxazole (25 μg/disk) (Tr-Sul), chloramphenicol (30 μg/disk) (C30), imipenem (30 μg/disk) (I30), and ampicillin (10 μg/disk) (A10) (Oxoid, UK). After superficial culture of A. baumannii on the MHA plates, antibiotic discs were placed in plates with significant distance from each other. Media containing antibiotic discs were incubated for 24 h at 37°C. Then, the A. baumannii’s diameter of the growth inhibition zones surrounding the discs was measured and compared with the CLSI instructions [30]. A. baumannii ATCC 19606 and Escherichia coli (E. coli) ATCC 25922 were used as controls.

2.4. PCR-Based Detection of Antibiotic Resistance Genes

At first, all A. baumannii isolates were prepared for DNA extraction. For this purpose, A. baumannii were subcultured on tryptic soy broth (TSB) media and incubated for 48 h at 37°C. Then, the DNA was extracted from colonies using the kit of DNA extraction (Thermo Fisher Scientific, St. Leon-Rot, Germany). Then, the quality (by electrophoresis on a 2% agarose gel) and quantity (by the spectrophotometer (A260/A280)) of extracted DNA were checked [31, 32].

Table 1 shows the conditions used for the PCR-based detection of antibiotic resistance genes in the A. baumannii isolates [33–36]. A programmable DNA thermocycler (Eppendorf Mastercycler 5330, Eppendorf-Netheler-Hinz GmbH, Hamburg, Germany) was used in all PCR reactions. All ingredients were purchased (Thermo Fisher Scientific, St. Leon-Rot, Germany). In addition, amplified samples were analyzed by electrophoresis (120 V/208 mA) in a 2.5% agarose gel stained with 0.1% ethidium bromide (0.4 μg/mL) [36]. Besides, UVI doc gel documentation systems (Grade GB004, Jencons PLC, London, UK) were used to analyze images [37–39].

2.5. Data Analysis

SPSS software was applied to assess any statistical analysis of extracted data. For this aim, chi-square and Fisher’s tests were used. Statistical differences between sample types and A. baumannii prevalence and antibiotic resistance were examined. value < 0.05 was considered as significant level.

3. Results

3.1. Prevalence of A. baumannii

Figure 1 shows a sample of gel electrophoresis of PCR products for A. baumannii detection. Table 2 shows the A. baumannii’s prevalence amongst the seafood samples. Twenty out of 450 (4.44%) seafood samples were contaminated with A. baumannii. Amongst the examined samples, fish harbored the highest (7.85%) contamination rate with the A. baumannii, while lobster harbored the lowest (1.66%).

3.2. Phenotypic Pattern of Antibiotic Resistance

Table 3 shows the A. baumannii’s phenotypic pattern of antibiotic resistance. A. baumannii isolates harbored the maximum resistance rate against tetracycline (; 85%), ampicillin (; 85%), gentamicin (; 70%), and erythromycin (; 60%). Resistance rates toward trimethoprim-sulfamethoxazole, ciprofloxacin, ceftazidime, and azithromycin were 55% (), 45% (), 35% (), and 30% (), respectively. The minimum rates of resistance were obtained against imipenem (; 10%) and chloramphenicol (; 15%).

3.3. Genotypic Pattern of Antibiotic Resistance

Figure 2 shows the samples of gel electrophoresis of PCR products for antibiotic resistance gene detection. Table 4 shows the A. baumannii’s genotypic pattern of antibiotic resistance. Amongst the examined antibiotic resistance genes, bla_CITM (75%), bla_SHV (70%), tetA (70%), qnr (55%), blaVIM (50%), and aac(3)-IV (50%) had the highest distribution rate. The aadA1, sul1, dfrA1, qnrA, bla_VIM, bla_SIM, bla_OXA-51, bla_OXA-23, and bla_OXA-58 were detected in 40%, 30%, 45%, 50%, 35%, 25%, 30%, and 20% of strains, respectively. The lowest rates were observed for cmlA (5%), cat1 (10%), bla_IMP (10%), tetB (15%), and bla_OXA-24 (15%) genes.

4. Discussion

Cumulative consumption of fresh, raw, and undercooked food is not only measured to be the most significant food-borne disease leading cause [40], but also related to frequent bacterial pathogens eruptions. In this regard, A. baumannii is considered an important risk of foodborne diseases in contaminated food samples in rare studies [18]. In this survey, A. baumannii prevalence amongst the lobster, fish, and shrimp samples was 1.66%, 7.85%, and 4.61%, respectively. The higher catch rate of fish compared to shrimp and lobster and the transfer of contamination between caught fishes can be a possible reason for the higher prevalence rate of A. baumannii in fish samples. Filter-feeding nature of shrimp and lobster which accumulate the pathogens may face them in a higher risk of contamination. Additionally, the role of hand manipulation of seafoods in ports may increase the risk of contamination. Scarce studies have been aimed at assessing the A. baumannii prevalence in seafood samples. In our previous survey [27], A. baumannii prevalence amongst the fish, shrimp, and lobster samples was 10%, 5.30%, and 2.50%, respectively. Hasiri et al. found A. baumannii in 5.6% seafood in Iran. This low prevalence in Iran indicates that A. baumannii contamination of seafood is emerging. In this study, samples were collected only from seafood markets in central Shiraz, so this low prevalence is not representative of the whole province, and different results could be found in other seafood markets [27]. In the United States [41], Acinetobacter was detected in 9.54% of retail seafood samples. In India, a virulent A. baumannii associated with mortality of farmed Indian major carp Labeo rohita was found in 2017 [42]. Another study performed in India reported multi-drug-resistant Acinetobacter baumannii associated with snakehead Channa striatus eye infection [43]. Antibiotic-resistant Acinetobacter johnsonii and Acinetobacter lwoffii were isolated from fish cultured in Poland [44]. Other food-based research focused on other food samples. Askari et al. [45] reported that the A. baumannii prevalence amongst the raw meat samples collected from Iran was 20.10%. According to the findings of Askari et al. [21], A. baumannii prevalence amongst the retail camel, sheep, and goat meat samples was 2.26%, 41.12%, and 11.72%, respectively. In Egypt [19], A. baumannii prevalence amongst the camel, cow, sheep, and goat meat samples was 9.68%, 15%, 46.55%, and 32.50%, respectively. In another Iranian survey, Tavakol et al. [46] reported that the A. baumannii prevalence amongst the raw chicken, bovine, camel, and ovine meat samples was 45.45%, 18.18%, 13.64%, and 9.10%, respectively. Such a large variation across countries in A. baumannii prevalence rate from food samples may show real regional differences or may be affected by the use of various detection techniques. Additional developments in the A. baumannii detection techniques in foods are desirable.

Acinetobacter baumannii strains isolated from seafood samples harbored a high resistance rate toward some of the basic therapeutic options mainly used in veterinary and medicine, particularly tetracycline, ampicillin, gentamicin, and erythromycin. Unauthorized and improper antibiotic administration, antibiotic and disinfectant overuse, and self-medication with antibiotics can be conceivable reasons for the high prevalence of antibiotic resistance. Contact of the seafood surface with the port environment, equipment used for their sorting, and contaminated staff can cause the transfer of antibiotic-resistant strains to them. Kim et al. [47] stated the high A. baumannii prevalence (27.80%) amongst the raw milk samples which is supported by the high antibiotic resistance of isolates against ceftriaxone (4.4%), tetracycline (30.8%), gentamicin (2.9%), and cefotaxime (12.5%). Similarly, in surveys conducted on Iran [48], Brazil [49], Jordan [50], United States [51], Korea [52], and Africa [53], high A. baumannii resistance rates against tetracycline, ampicillin, gentamicin, trimethoprim, ciprofloxacin, and erythromycin were reported. Askari et al. [21] stated that the A. baumannii strains isolated from raw meat of animal species harbored the highest resistance rate against tetracycline (82.35%), gentamycin (74.50%), streptomycin (54.90%), cotrimoxazole (70.58%), and trimethoprim (62.74%). In another study, Askari et al. [45] mentioned that the resistance rate of A. baumannii strains isolated from raw meat samples toward gentamicin, tetracycline, erythromycin, azithromycin, ciprofloxacin, trimethoprim-sulfamethoxazole, and rifampin was 87.17%, 79.48%, 74.35%, 66.66%, 58.97%, 56.41%, and 51.28%, respectively. Ahmad et al. [54] reported that the prevalence of resistance of A. baumannii isolated from meat samples against ampicillin, ceftriaxone, imipenem, gentamicin, kanamycin, tetracycline, chloramphenicol, trimethoprim, sulfamethoxazole, and norfloxacin was 100%, 20.80%, 33.30%, 16.60%, 54.10%, 79.10%, 66.60%, 100%, 8.30%, and 16.60%, respectively. An Egyptian survey [19] showed the highest resistance rate of A. baumannii strains against amoxicillin/clavulanic acid (89.10%), gentamicin (74.55%), tetracycline (72.73%), ampicillin (65.45%), and tobramycin (52.73%). The differences reported in the A. baumannii phenotypic pattern of antibiotic resistance in various studies are probably due to the availability or nonavailability of antibiotics, the level of strict rules in prescribing antibiotics, and the opinion of physicians and veterinarians on prescribing antibiotics. The prevalence of resistance to imipenem (10%) and chloramphenicol (15%) was lower than that of other antibiotics. Imipenem, a human-prescribed antibiotic in the hospital, is not used in veterinary medicine and also for the treatment of marine animals (in fish, shrimp, and lobster cultures). Thus, it is not surprising that A. baumannii strains harbored a low resistance rate against imipenem. Chloramphenicol is also an illicit drug with a limited prescription. The use of this antibiotic illegally is done only in poultry farms in Iran. Thus, it should have a low resistance rate. The final part of the study is aimed at assessing the genotypic pattern of antibiotic resistance amongst the A. baumannii strains. Findings showed that bla_CITM (encodes resistance against beta-lactams), bla_SHV (encodes resistance against beta-lactams), tetA (encodes resistance against tetracyclines), qnrA (encodes resistance against quinolones), bla_VIM (encodes resistance against carbenicillin), and aac(3)-IV (encodes resistance against gentamicin) were the most commonly detected antibiotic resistance genes. The high distribution of the genes that encode resistance against diverse classes of antibiotics in the A. baumannii strains in this survey revealed the critical role of seafood samples as a possible vehicle for the community-wide dissemination of antibiotic-resistant A. baumannii strains. Similarly, Ghazaei [55] reported that the distribution of bla_SHV, bla_TEM, and bla_PER antibiotic resistance genes amongst the A. baumannii isolates of foodstuffs was 29.62%, 18.51%, and 14.81%, respectively. Tavakol et al. [46] also identified aadA1, aac(3)-IV, bla_SHV, bla_CITM, cat1, cmlA, tetA, tetB, sul1, dfrA1, bla_IMP, bla_SIM, bla_VIM, and qnrA antibiotic resistance genes amongst the A. baumannii strains of raw meat. In a German study [56], OXA-23, OXA-51, and OXA-58 oxacillinase genes were detected in A. baumannii strains isolated from milk powder.

5. Conclusion

In conclusion, A. baumannii strains were detected in 4.44% of seafood samples, with the higher prevalence of bacteria amongst the fish samples (7.85%). The considerable prevalence of A. baumannii strains was accompanied by the high rate of bacterial resistance toward commonly used antibiotic agents, particularly tetracycline, ampicillin, gentamicin, and erythromycin. The findings may show the high antibiotic resistance of A. baumannii and the potential role of seafood samples in its transmission to the human population. Some strains harbored different antibiotic resistance genes, particularly bla_CITM, bla_SHV, tetA, qnrA, bla_VIM, and aac(3)-IV. These findings may show the role of seafood samples as a source of antibiotic resistance genes. It seems that the consumption of contaminated seafood with the resistant A. baumannii may cause severe food-borne diseases that resist antibiotic therapy. However, the role of contaminated seafood as a hazard of foodborne infection has not been determined yet. Thus, several studies should perform to assess the role of seafood samples in the transmission of virulent and resistant A. baumannii foodborne diseases.

Data Availability

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

Conflicts of Interest

The authors declare no potential conflict of interest.

Authors’ Contributions

All authors read and approved the final manuscript.

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Copyright © 2023 Zahra Hasiri et al. This is an open access article distributed under the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.

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