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Histamine-Producing Bacteria and Histamine Induction in Retail Sardine and Mackerel from Fish Markets in Egypt

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Histamine-Producing Bacteria and Histamine Induction in Retail Sardine and Mackerel from Fish Markets in Egypt FOODBORNE PATHOGENS AND DISEASE Volume 16, Number 9, 2019 ORIGINAL ARTICLES ª Mary Ann Liebert, Inc. DOI: 10.1089/fpd.2018.2616 Histamine-Producing Bacteria and Histamine Induction in Retail Sardine and Mackerel from Fish Markets in Egypt Maha Ahmed Sabry,1 Hayam Abd-El Aal Mansour,2 Radwa Mohamed Ashour,1 and Eman Hamza1 Abstract This study examined the occurrence of histamine-producing bacteria (HPB) and histamine induction in retail sardine and mackerel in Egypt; and whether the fish vendors play a role in the transmission of HPB. Fish were collected from the fish markets, additionally; hand swab samples were taken from the fish vendors. All samples were cultured on modified Niven’s medium (MNM); the positive colonies were subcultured on Violet Red Bile Glucose (VRBG) agar, followed by biochemical identification and histidine decarboxylase (hdc)-gene-PCR of the VRBG-positive isolates. The hdc-gene-positive fish and human isolates were subjected to partial hdc-gene- sequencing and phylogenetic analysis. Production of histamine in the fish muscles was measured by high- performance liquid chromatography. A higher percentage of sardine showed the presence of MNM-positive bacteria (84%) than mackerel (53%). Enterobacteriaceae was the dominant family; the most frequent species were Enterobacter cloacae, Raoultella planticola, Citrobacter freundii, and Enterobacter aerogenes. Higher proportion of the R. planticola isolates were hdc positive as compared with the other species. Only 32% sardine and 17% mackerel of the MNM-positive isolates carried the hdc gene. Fish muscles that contain hdc-positive bacteria exhibit higher levels of histamine (median 86; IQR 80–1112 mg/kg) than those with hdc-negative bacteria (48; 75–223 mg/kg). The level of histamine was significantly higher in sardine (109; 104–1094 mg/kg) than in mackerel (40; 49–106 mg/kg). The 20 fish vendor samples were MNM positive, 2 of them were hdc- gene positive. The close genetic relatedness between the human and fish strains isolated from the same markets suggests a possible bidirectional transmission of the HPB. This warns for the presence of HPB carrying hdc gene in retail sardine and mackerel, which is associated with a relatively high level of histamine. Regular inspection of the fish markets is required, including accurate determination of HPB by using a combination of the MNM culture, hdc-gene PCR, and measurement of histamine level. Keywords: histamine fish poisoning, histamine-producing bacteria, Enterobacteriaceae, Raoultella planticola, retail market fish, sardine, mackerel, hdc gene, Egypt Downloaded by 188.154.164.186 from www.liebertpub.com at 09/12/19. For personal use only. Introduction (Lerke et al., 1978; Ferrario et al., 2012; Wongsariya et al., 2016). ish is a low-calorie high-protein food; its consumption This process can start as soon as the fish dies and kept at Fmight result in some foodborne illnesses and outbreaks temperature above 4°C for an extended period (FAO/WHO, (Iwamoto et al., 2010). Of particular interest is histamine fish 2012). Once the HDC enzyme is synthesized, it continues to poisoning (HFP), which is caused by eating spoiled fish that produce histamine even if the bacteria get inactivated (EFSA, contain high levels of histamine (Taylor et al., 1989; Vis- 2011; FDA, 2011). Cooking can inhibit the HPB and the ciano et al., 2012; Feng et al., 2016). HDC, while histamine cannot be degraded by cooking, Scombroid and other dark muscle fish such as tuna, bo- smoking, or canning of fish, indicating that both raw and nito, mackerel, blue fish, dolphin, sardine, carangids, her- cooked fish might cause HFP (Hungerfood, 2010). Accord- ring, and anchovies are prone to form histamine, as their ingly, the legal level of histamine should not exceed muscles are histdine-rich. (Choudhury et al., 2008; Feng 200 mg/kg in marketed fish species rich in histidine (EFSA, et al., 2016). Histamine formation results from histdine 2011; FAO/WHO, 2012, 2018). The major HPB reported in decarboxylation through histamine-producing bacteria fish are the family Enterobacteriaceae (Kim et al., 2003; (HPB) containing histidine decarboxylase (HDC) enzyme. Klanian et al., 2018). Of these, Morganella morganii, 1Department of Zoonoses and 2Meat Hygiene and Control Department, Faculty of Veterinary Medicine, Cairo University, Cairo, Egypt. 597 598 SABRY ET AL. Enterobacter aerogenes, Enterobacter cloacae, Raoultella Isolation of histamine-producing Enterobacteriaceae. planticola, Raoultella ornithinolytica, and Photobacterium The presumptive MNM-positive isolates (mackerel, n = 58; damselae are particularly high histamine producers. How- sardine, n = 44; humans, n = 20) were streaked onto plates of ever, other species including Citrobacter freundi, Vibrio al- Violet Red Bile Glucose (VRBG; LAB M, Heywood, United ginolyticus, and Escherichia coli are weak histamine Kingdom) agar, a selective medium for isolation of En- producers (Takahashi et al., 2003). terobacteriaceae, and were incubated at 37°C for 24 h So far, little information is available about HPB in Egypt. (Mossel, 1985). The suspected colonies were purified Therefore, the objectives of this study were to investigate the through subculture on Tryptic Soya Agar (LAB M) plates, presence of HPB and histamine production in retail sardine and were examined for morphological and phenotypic traits. and mackerel, two types of commonly consumed histidine- Typical colonies of Enterobacteriaceae are Gram negative, rich fish in Egypt; and to examine whether the fish vendors round, purple-pink surrounded by purple halo. play a role in the transmission of the HPB. Accordingly, we collected muscle samples from the fish at the markets, as well c. Biochemical identification. The VRBG colonies sub- as hand swab samples from the fish vendors. All samples cultured on Tryptic Soya Agar were subjected to the tra- were subjected to bacterial isolation and identification of HP- ditional oxidase biochemical test according to Shore and Enterobacteriaceae, followed by molecular detection of hdc Isenberg (2007), and confirmed with API 20E kit (Bio- gene among the isolates. The level of histamine in the fish Me´rieux, Marcy-l’E´ toile, France). API 20NE kit was used muscles was measured by high-performance liquid chroma- to confirm the identity of the non-Enterobacteriaceae tography (HPLC). The genetic relatedness of the fish and strains that grew on the VRBG. The accuracy of the kit human isolates collected from the same markets was deter- resultswas100%asdeterminedbyAPIwebsoftware mined by partial sequencing of the hdc gene. (BioMe´rieux). Materials and Methods III. Molecular detection of histidine decarboxylase (hdc) gene Samples All the MNM-VRBG-positive isolates (mackerel, n = 58; The study included apparently healthy frozen imported sardine, n = 44; humans, n = 20) were examined for the mackerel (n = 100) and fresh local sardine (n = 57); whole fish presence of the hdc gene. Genomic DNA was extracted using were taken and placed in sterile polyethylene bags. Hand swab the rapid boiling method (Reischl et al., 1994) and subjected samples were collected from the fish vendors (n = 20); none of to conventional PCR using specific oligonucleotide primers: them had allergic symptoms. One swab per individual was forward 5¢-TGGGGTTATGTSACCAATGG-3¢, reverse 5¢- used, rubbed in the interdigital spaces, nails, palms, and on the GTRTGGCCGTTACGY GARCC-3¢ with an amplicon size back of the hands, then inoculated into sterile tubes containing of 571 bp (Wongsariya et al., 2016). PCR mixtures for a total 9 mL of 0.1% peptone water solution. Both fish and human volume of 25 lL consisted of 3 lL of template DNA from samples were transported to the laboratory on ice. All samples each isolate, 12.5 lL of GT-PCR master mix (Takara Bio, were collected from randomly selected fish markets located in Inc., Shiga, Japan), 1 lL of 10 pmol of each primer, and EL-Giza and Alexandria Governorates, during the period from 8.5 lL nuclease-free water. All PCR mixtures were per- March 2016 to April 2017. Protocols for collection of samples formed in duplicates and subjected to 35 cycles of 94°C for as well as all methods were performed in accordance with the 1 min, 54°C for 1 min, and 72°C for 4 min. The PCR products guidelines and regulations of Cairo University Council, Fa- were electrophoresed on 1.5% agarose gel, a DNA marker culty of Veterinary Medicine, Egypt. Written consent to use (Gene RulerÔ 100 bp DNA Ladder, Vivantis Technologies samples was obtained from each person. Sdn. Bhd., Selangor Darul Ehsan, Malaysia) was run simul- taneously. Downloaded by 188.154.164.186 from www.liebertpub.com at 09/12/19. For personal use only. Bacterial isolation and identification Sequencing of the PCR-amplified hdc-gene fragment Ten gram muscles were taken from the dorsal, abdominal, and tail parts of each fish. The muscles were inoculated into The amplified hdc-gene PCR product obtained from the 9 mL of 0.1% peptone water, and homogenized using Sto- fish (n = 6) and human (n = 2) samples collected from the macherÒ 400 blender (Seward lab, Worthing, United King- same markets was purified using Qiaquick PCR Product ex- dom) (Fletcher et al., 1998). traction kit (Qiagen, Hombrechtikon, Switzerland). The purified PCR products were sequenced using BigDye Ter- minator V3.1 sequencing kit (Applied Biosystems, Waltham, Isolation of HPB. The modified Niven’s medium (MNM) MA; the obtained nucleotide sequences were deposited in the was used for initial selection of HPB. One milliliter from GenBank. each of the fish homogenates (mackerel, n = 100; sardine, n = 57) as well as the human hand swab suspensions (n = 20) Phylogenetic analysis. The obtained nucleotide se- were streaked separately into the MNM prepared according quences were compared with those available in public do- to Niven et al. (1981); Joosten and Northolt (1989); and mains using the NCBI-BLAST server, and were imported Mavromatis and Quantick (2002). The plates were incubated into the BioEdit program version 7.0.1.4 for multiple align- at 37°C for 48–72 h and were examined every 24 h.
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