VIBRIO PARAHAEMOLYTICUS IN SEAFOOD
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Occurrence of antimicrobial resistant or pathogenic Vibrio parahaemolyticus in seafood. A mini review O. A. ODEYEMI1*, D. STRATEV2 1 2
Ecology and Biodiversity, Institute of Marine and Antarctic Studies, University of Tasmania, Australia Department of Food Hygiene and Control, Veterinary Legislation and Management, Faculty of Veterinary Medicine, Trakia University, 6000 Stara Zagora, Bulgaria
*Corresponding author:
[email protected]
ABSTRACT
RÉSUMÉ
Vibrio parahaemolyticus is a Gram-negative, non-sucrose fermenting marine halophilic bacterium. It is widely prevalent in the aquatic environment and is frequently isolated from seafood. Moreover, some V. parahaemolyticus strains isolated from seafood are pathogenic. V. parahaemolyticus is a human pathogen causing gastroenteritis after consumption of raw or undercooked seafood. Microbiological safety of seafood is of global concern in recent years due to outbreaks of seafood-borne pathogens such as V. parahaemolyticus. There has been recent increase of reports on antibiotic resistance among V. parahaemolyticus isolated from seafood. The emergence of antimicrobial resistant seafood-borne pathogens poses threat to human health. With regard to the increasing reports of V. parahaemolyticus food borne infections, we aimed to review occurrence of antibiotic resistant V. parahaemolyticus in selected seafood and its importance to consumers’ health.
Occurrence de Vibrio parahaemolyticus résistant aux antimicrobiens ou pathogenes chez les fruits de mer: une mini-revue
Keywords: V. parahaemolyticus, antimicrobial resistance, food safety
occurrence,
Vibrio parahaemolyticus est une bactérie marine halophile qui est Gramnégative et ne fermente pas le saccharose. Elle est largement répandue dans l’environnement aquatique et est souvent isolée de fruits de mer. En outre, certaines souches de V. parahaemolyticus isolées à partir de fruits de mer sont pathogènes. V. parahaemolyticus est un agent pathogène humain provoquant des gastro-entérites après la consommation de fruits de mer crus ou insuffisamment cuits. Au cours des dernières années, les risques microbiologiques liés aux fruits de mer représentent une préoccupation mondiale en raison de cas humains dus à des agents pathogènes tels que V. parahaemolyticus suite à la consommation de fruits de mer. Récemment, les rapports sur la résistance aux antibiotiques chez les V. parahaemolyticus isolés à partir de fruits de mer sont plus en plus fréquents. L’émergence d’agents pathogènes résistants aux agents antimicrobiens et isolés de fruits de mer constitue une menace pour la santé humaine. En ce qui concerne les nombreux rapports d’infections alimentaires causés par V. parahaemolyticus, nous avons cherché à examiner l’apparition de résistance aux antibiotiques chez V. parahaemolyticus isolés de certains fruits de mer et son importance pour la santé des consommateurs.
Mots-clés : V. parahaemolyticus, occurrence, résistance antimicrobienne, sécurité alimentaire
Introduction Seafood has been described as one of the fastest growing sources of food in the world and serves as a major source of income to many developing and developed countries [55]. Various health benefits such as reduction of heart diseases risk [29, 41] and neural development during gestation and infancy [10, 16, 23] have been attributed to consumption of seafood. Despite the high benefits of seafood consumption, health risks related to seafood consumption cannot be overemphasized [23]. According to Wang et al. [59] and Iwamoto et al. [23], seafood (mollusks, finfish, marine mammals, fish eggs and crustaceans) constitute an important route of transmission of pathogenic microorganisms to human. Outbreaks of epidemic diarrhoea linked with consumption of contaminated raw seafood have been reported in different parts of the world. Feldhusen [14] investigated major bacterial pathogens that have been associated with seafoodborne diseases. Subsequent contamination may occur in various stages like processing, storage and distribution of seafood. Sources of contamination include water, facilities, Revue Méd. Vét., 2016, 167, 3-4, 93-98
equipment and handlers. The processing stage is particularly important due to the high microbial load on the surface of processing facilities. According to Hernandez-Macedo et al. [22], fecal materials containing spoilage microorganisms and pathogens can serve as source of microbial contamination of seafood. Antimicrobial agents are commonly used in aquaculture either as preventive or curative treatments [12]. Antibiotic resistant V. parahaemolyticus has been reported recently [3, 5, 12, 47]. The emergence and re-emergence of antimicrobial resistant seafood-borne pathogens in recent years pose threat to human health [28]. This has been attributed to factors such as indiscriminate use of antibiotics in aquaculture. With regard to the increasing reports of V. parahaemolyticus food-borne infections, we aimed to reviewing occurrence and prevalence of antibiotics resistant V. parahaemolyticus in seafood and its importance to consumers’ health.
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Characteristics of V. parahaemolyticus V. parahaemolyticus belongs to the family Vibrionaceae. It is a non-sucrose fermenting halophilic bacterium that can grow between 10 °C and 44 °C (optimum 35-37 °C), pH ranges from 5 to 11 and with 3-8% NaCl tolerance. V. parahaemolyticus possesses somatic (O) and capsular (K) antigens, and on this basis 12 O and 65 K groups have been determined [21, 58, 63]. It has been isolated from aquatic environment such as seawater, sediment and diverse vertebrate and invertebrate seafood [53]. V. parahaemolyticus is a human pathogen that causes gastroenteritis due to the presence of thermo-stable direct hemolysin (TDH) or TDHrelated hemolysin (TRH) toxins, encoded by tdh and trh genes [2].
V. parahaemolyticus gastroenteritis in humans The survival of V. parahaemolyticus in seafood subjected to chilling, freezing, heating, drying and smoking has been reported. This organism is being completely destroyed in cooked foods [43]. However, some seafood such as oysters is consumed raw. The consumption of raw or undercooked seafood contaminated with V. parahaemolyticus may cause acute gastroenteritis. This bacterium is recognized as the leading cause of human gastroenteritis associated with seafood consumption in the United States and an important seafood-borne pathogen throughout the world [49]. V. parahaemolyticus was firstly reported as seafood-borne pathogen in Japan in 1950 [21, 35]. Since then, various outbreaks due to consumption of either contaminated raw or undercooked seafood have been reported in countries such as the United States [13, 23, 39], China [36], Taiwan [6], Spain [37], Italy [46], Chile [17], Peru [18] and Brazil [31]. The number of outbreaks of V. parahaemolyticus infections in the aforementioned countries varies. For example, in the United States, 40 outbreaks of V. parahaemolyticus infection were registered during the period between 1973 and 1998 that included more than 1000 illnesses [11]. More than 300 gastroenteritis outbreaks due to V. parahaemolyticus were reported in China between 2003 to 2008, which resulted into over 9000 illnesses and 3940 hospitalizations [60]. According to Letchumanan et al. [33], V. parahaemolyticus causes 2030% of food borne diseases in Japan and many cases in Asian countries. Martinez-Urtaza et al. [38] summarized data regarding several V. parahaemolyticus outbreaks in Spain. V. parahaemolyticus infection is characterized with acute abdominal pain, vomiting, watery or bloody diarrhea and gastroenteritis [2, 58] with an incubation period of 4 to 96 hours [35]. According to Zamora-Pantoja et al. [63], infective dose varies between 105 and 107 cfu, and the infection is selflimiting over a period of a week. Three serotypes, namely O3:K6, O4:K68, and O1:K untypeable (KUT), cause a pandemic of V. parahaemolyticus infecton [7]. Non-toxic V. parahaemolyticus strains do not cause any infection [25].
ODEYEMI (O. A.) AND STRATEV (D.)
Occurrence of V. parahaemolyticus in seafood V. parahaemolyticus is widely prevalent in the aquatic environment and is frequently isolated from seafood. The bacterium was found out to be prevalent among oysters (48.8100%), mussels (34-68,1%), clamps (63.9-100%), cockles (7.5-62%), scallops (55-60%), shrimps (7.1-57.8%), crabs (20%), fish (2.9-45.1%). Moreover, some V. parahaemolyticus strains isolated from seafood are pathogenic [1, 27, 30, 48, 50, 61, 64, 65]. The number of V. parahaemolyticus in seafood varies (Table I). Enumeration of this organism from seafood is important because Food and Drug Administration (FDA) stipulate less than 103 cfu/g in seafood. However, despite this permissible limit, there are still outbreaks in the United States. Seafood has been described as vehicle of transmission of food borne bacteria that cause human illness worldwide [34]. The prevalence of V. parahaemolyticus depends on several factors including water temperature, salt and oxygen concentrations, interaction with plankton, presence of sediment, organic matter and marine organisms [34]. The presence of V. parahaemolyticus in seawater is influenced by season of the year with highest occurrence in the warmer months [43]. V. parahaemolyticus usually concentrates, multiplies and coheres in the gut of filter feeding shellfish such as clams, oysters and mussels [56]. The presence of V. parahaemolyticus in seafood can be hazardous to human health especially when postharvest temperatures are not properly controlled in the supply chain [15].
Prevalence of antimicrobial resistant V. parahaemolyticus in seafood Microbial drug resistance has increased in recent years and therefore becomes public health issue [52]. Centre for Disease Control and Prevention (CDC) recommended antibiotics such as fluoroquinolones (levofloxacin), cephalosporin (cefotaxime and ceftazidime), aminoglycosides (amikacin and gentamicin), and folate pathway inhibitors (trimethoprim-sulfamethoxazole) for treatment of Vibrio spp. infections [34]. However, variation in antibiotic resistance pattern among V. parahaemolyticus isolated from seafood in different countries has been observed. In a recent study regarding antibiotic resistance of V. parahaemolyticus isolated from seafood [45], it was observed that 20% of the isolates were resistant to all tested antibiotics. In another study, Shaw et al. [52] observed that 68% of isolates of V. parahaemolyticus were resistant to penicillin. The result of this study was similar to resistance pattern of V. parahaemolyticus isolated from Gulf Coast raw oysters in Louisiana [19]. Resistance to ampicillin and oxytetracycline was also reported recently among V. parahaemolyticus isolated from shrimps in Thailand [62]. The use of tetracycline which ranks among mostly used antibiotics in aquaculture is attributed to efficiency and reduced cost [42]. Lesley et al. [32] determined antibiotics resistance of V. parahaemolyticus isolated from cockles (Anadara granosa) in Malaysia. Results showed Revue Méd. Vét., 2016, 167, 3-4, 93-98
VIBRIO PARAHAEMOLYTICUS IN SEAFOOD that all 62 tested strains were resistant to streptomycin, tobramycin, carbenicillin, teicoplanin, cephalothin, clindamycin, rifampicin, sulfamethoxazole and oflaxacin. A similar study in Malaysia revealed that out of 44 strains of V. parahaemolyticus isolated from cockle (Anadara granosa), 37 were confirmed to harbour toxR gene. Out of these toxRpositive strains, 34 were highly resistant to bacitracin (92%), 33 resistant to penicillin (89%), 25 resistant to ampicillin (68%), 14 resistant to cefuroxime (38%), 5 ceftazidime (14%) and 2 were resistant to amikacin (6%) [51]. In the study of Letchumanan et al. [34], 82% of 185 V. parahaemolyticus strains isolated from Malaysian banana prawn (Penaeus indicus) and red prawn (Solenocera subnuda) were resistant to ampicillin. The prevalence of multiple antibiotic resistance was attributed to abuse of antibiotics in treatment of bacterial infections in aquaculture. This was similar to a study in Korea. Jun et al. [26] observed high prevalence of antibiotic resistance to cefotaxime and ceftazidime (70-80%) among V. parahaemolyticus isolated from seafood obtained from several fish markets in Korea. Melo et al. [40] reported that 5 out of 10 V. parahaemolyticus strains isolated from shrimp (Litopenaeus vannamei) in Brazil showed multiple antibiotic resistance toward ampicillin (90%) and amikacin (60%). Ottaviani et al. [47] established resistance of 107 strains of V. parahaemolyticus isolated from wild shrimps
95 in Italy to amoxicillin and ampicillin (100%), cefalexin (59%), colistin (47%), erythromycin (24%), cefalothin (18%) and streptomycin (6%). According to Costa et al. [8], V. parahaemolyticus strains isolated from shrimps (Litopenaeus vannamei) were resistant to penicillin (100%), tetracycline (90%), ampicillin (30%) and cephalothin (10%). Han et al. [20] reported that V. parahaemolyticus strains isolated from shrimps in Mexico were resistant to ampicillin, oxytetracycline and tetracycline. Factors attributed to antimicrobial resistance in bacteria isolated from seafood include presence of plasmid, indiscriminate use of antibiotics in aquaculture and horizontal gene transfer. Indiscriminate use of antimicrobials such as tetracycline and quinolone either for therapeutic or prophylactic purposes has been described in intensive shrimp farming [62]. Although some V. parahaemolyticus strains were isolated from wild shrimps they showed high level of antibiotic resistance [47]. In the belief of Han et al. [19], this phenomenon due to environmental contamination by agricultural run-off or wastewater treatment plants which contain antimicrobial agents acting as selective pressure for the development of resistant aquatic bacteria. According to Shaw et al. [52], the patterns of antibiotic resistance among Vibrio species isolated from aquatic environments may have
Source
Percentage of positive samples
Density (MPN/g)
Reference
Clams
80
-
[57]
Clams
100
1.07
[24]
Clams
63.9
4.2 x 10
[65]
Cockles
40
-
[57]
Cockles
62
>1100
[4]
Cockles
7.5
-
[1]
Crabs
20
-
[1]
Fish
45.1
-
[55]
Fish
2.9
-
[64]
Mussels
55
-
[57]
Mussels
34
-
Mussels
68.1
3.9 x 10
[65]
Oysters
50
11000
[44]
Oysters
100
1.88
[24]
Oysters
94.8
99.3
[27]
Oysters
48.8
3 x 102
[65]
Oysters
81
-
[9]
Oysters
100
[54]
Scallops
55
1.78 - 6.04 log10
Scallops
60
4 x 10
[65]
Shrimps
7.1
-
[64]
Shrimps
57.8
-
[34]
Shrimps
22.5
-
[1]
Shrimps
37.7
3-100
[61]
Table I: Occurrence of V. parahaemolyticus in selected seafood Revue Méd. Vét., 2016, 167, 3-4, 93-98
2
[9] 2
-
2
[57]
96 impact on seafood, seafood consumers and human marine related activities such as recreation. Lesley et al. [32] stated that the specific role of antibiotics in management of human infections associated with Vibrio species is still unknown.
Recommendation and future study on V. parahaemolyticus in seafood The occurrence and prevalence of antimicrobial resistant V. parahaemolyticus in seafood require urgent and formidable effort to prevent outbreaks of seafood-borne Vibrio infections. There is need for guided policy on use of antibiotics in aquaculture farming. Eating of raw seafood like oyster should be with caution. Continuous monitoring of seafood and aquaculture environment for presence of this pathogen is recommended. Additionally, there is need for meta-analysis and systematic study of global prevalence of antimicrobial resistant V. parahaemolyticus in seafood to provide knowledge regarding the most prevalence pattern of resistance to antibiotics in seafood globally.
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