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Distribution of new Staphylococcal Enterotoxin Genes (seg, seh, sei, sej, and sel) in Staphylococcus aureus Isolated from Retail Ready-to-Eat Foods in the Northeast Thailand

การแพร่กระจายของยีนเอ็นเทโรทอกซินชนิดใหม่ (seg, seh, sei, sej, and sel) ในเชื้อสแตฟฟิโลคอคคัส ออเรียส ที่แยกได้จากอาหารสำเร็จรูปในภาคตะวันออกเฉียงเหนือของประเทศไทย

Bongkot Khaenda (บงกช แคนดา) 1, Wises Namwat (วิเศษ นามวาท) 2, Daroon Kotimanusvanij (ดรุณ โกฏิมนัสวนิชย์) 3, Chariya Chomvarin (จริยา ชมวารินทร์) 4

หลักการและวัตถุประสงค์:  เชื้อ Staphylococcus aureus เป็นสาเหตุสำคัญที่ทำให้เกิดโรคอาหารเป็นพิษ อาหารสำเร็จรูปเป็นที่นิยมรับประทานกันในประเทศไทย การวิจัยนี้ทำการศึกษาการแพร่กระจายของยีนสร้างสารพิษเอ็นเทโรทอกซินชนิดใหม่ที่สำคัญ 5 ชนิดในเชื้อ S. aureus ที่แยกได้จากอาหารสำเร็จรูปที่ขายในจังหวัดขอนแก่น

วิธีการศึกษา:  ใช้วิธีปฏิกิริยาลูกโซ่พอลิเมอเรส (PCR) ตรวจหายีนสร้างสารพิษเอ็นเทโรทอกซินชนิดใหม่ 5 ยีน (seg, seh, sei, sej และ sel) ในเชื้อ S. aureus 57 สายพันธุ์ที่แยกได้จากอาหารสำเร็จรูปที่สุ่มตรวจจำนวน 151 ตัวอย่าง ที่วางขายในอำเภอเมือง จังหวัดขอนแก่น โดยวิเคราะห์ข้อมูลร่วมกับยีนของสารพิษเอ็นเทโรทอกซินชนิดดั้งเดิม ที่ศึกษาก่อนหน้านี้แล้ว (sea-sed and tsst-1).

ผลการศึกษา:  ตรวจพบยีนสร้างสารพิษเอ็นเทโรทอกซินชนิดใหม่ร้อยละ 29.8 (17 สายพันธุ์) โดยพบ ยีน sea ร่วมกับ seg จำนวนมากที่สุด (ร้อยละ 12.3) ตามด้วยยีน seg+sei (ร้อยละ 8.8) และยีน sec+seg (ร้อยละ 1.7) นอกจากนี้ยังพบยีน seg แบบเดี่ยวๆ จำนวน 4 สายพันธุ์ (ร้อยละ 7.0) แต่ไม่พบยีน seh, sej และ sel

สรุป:  การตรวจพบยีนสร้างสารพิษเอ็นเทโรทอกซินชนิดใหม่ในเชื้อ S. aureus ที่แยกจากอาหารสำเร็จรูป ในอำเภอเมือง ขอนแก่น พบว่ายีน seg และ sei พบได้จำนวนมาก และมักพบร่วมกับยีนสร้างสารพิษเอ็นเทโรทอกซินชนิดดั้งเดิม ชี้ให้เห็นว่าสารพิษเอ็นเทโรทอกซินชนิดใหม่ อาจมีส่วนทำให้เกิดโรคอาหารเป็นพิษในอาหารสำเร็จรูปได้


Background and Objective:  Staphylococcus aureus is a common cause of food poisoning.   Various ready-to-eat (RTE) foods have become increasingly popular in Thailand. The aim of this study was to investigate the distribution of enterotoxigenic S. aureus strains carring the newly important enterotoxin-encoding genes isolated from retail RTE foods in Khon Kaen municipality, Thailand.

Methods:  In this study, polymerase chain reaction (PCR) primers specific for the detection of newly staphylococcal enterotoxin (se); encoding genes including seg, seh, sei, sej and sel were used for the assay of 57 S. aureus isolates from 151 RTE food samples randomly collected from food vendors and food shops in Khon Kaen municipality that have been previously investigated for the five classical enterotoxin genes (sea-sed and tsst-1).

Results:  The result showed that the new enterotoxins could be found in 29.8% (17 of 57 isolates). The sea coexisted with seg was the most frequently found (12.3%), following by seg+sei (8.8%) and sec+seg (1.7%). Four isolates (7.0%) had single seg and none of S. aureus isolates had seh, sej and sel.

Conclusion:  These findings indicated that some new enterotoxin genes such as seg, and sei were the most frequently found and frequently coexists with other classical enterotoxin genes.  Therefore, these new enterotoxins may play a role to cause food poisoning in RTE foods in Khon Kaen, Thailand.



          Staphylococcus aureus is an important pathogen associated with Staphylococcal food poisoning worldwide including Thailand 1,2. According to the case outbreak in Thailand between January and December, 2014, the Bureau of Epidemiology, Ministry of public health reported a morbidity rate of food poisonings were  191.70  per 100,000 population and higher rate in North and Northeast Thailand 3.

          S. aureus can produce more than 30 different extracellular enzymes and toxins 4.  Staphylococcal toxins can be categorized into many groups such as Staphylococcal enterotoxins (SEs), exfoliative toxins, toxic shock syndrome toxin-1, leucocidin and other toxins 5-7. Generally, the classical staphylococcal enterotoxins  i.e., SEA, SEB, SEC, SED, and SEE  encoded by sea, seb, sec, sed and see, respectively, are recognized as the major cause of food poisoning 8-12.  Another enterotoxin, SEF, is biochemically identical to TSST-1 13,14.  The TSST-1 is also found to be associated with enterotoxins 15. Some S. aureus can secrete SEs in contaminated food and they can apply to cooked food due to the thermostable character 16,17. Moreover, the SEs and TSST-1 are known as bacterial super-antigens that can induce emetic activity, stimulating T cells and macrophages to release massive amounts of pro-inflammatory cytokines such as tumor necrosis factor-α (TNF-α),interleukin (IL)-1, IL-6 and interferon-γ (IFN-γ) leading to capillary leakage, fever, hypotension and shock 18.

            Recently, the new SEs are designated as SE-like (SEl) toxins because they lack the emetic properties 7,19. Many new enterotoxins including SEG, SEH, SEI, SElJ, SElK, SElL, SElM, SElN, SElO, SElP, SElQ, SER SES, SET, SElU, SElV and SElW have been reported in other countries20-26.  It has been known that approximately 95% of staphylococcal food poisoning outbreaks are caused by SEA to SEE 27 and the remaining 5% of outbreaks may be associated with other newly identified as SEs.

Various RTE foods have become increasingly popular in Thailand.  Various microorganisms including S. aureus can be easily contaminated in RTE foods resulting in food poisoning 28,29. Thai traditional foods especially green papaya salad (“somtum”) and fermented pork mixed with rice (“nam krug”) are popular local RTE foods. In addition, seafood and fresh fruit juice are also popular around the world 30.

          In Thailand, our previous study has been reported the classical enterotoxin genes (sea-sed and tsst-1 and protein productions (SEA-SED and TSST-1) in RTE foods in Khon Kaen, Thailand 2, however, the new SEs genes have not been investigated.

          Normally, many immunoassay kits such as the reverse passive latex agglutination and staphylococcal enterotoxin ELISA kits have been used for detection of classical enterotoxins (SEA-SED) and TSST-1 2.  Molecular methods such as DNA probes and polymerase chain reaction (PCR) assays, have been developed and used for the detection of these classical enterotoxins 31-34.  However, the detection of new SEs is not available because of lacking of commercial immunoassay kit in Thailand 24. Therefore, the molecular assay PCR was used for detection these new enterotoxins in this study.  As, the new enterotoxin genes, the seg, seh, sei, sej and sel genes were more frequently found in several types of foods 21,23-25,35-37.  Therefore, we choose to detect those enterotoxin genes in this study.

          The aim of this study was to investigate the distribution of seg, seh, sei, sej, and sel  combined with the classical staphylococcal enterotoxin genes (sea-sed and tsst-1 genes) that were isolated from RTE foods and patients in the Northeast Thailand.  This study will be useful for understanding the prevalence of some staphylococcal new enterotoxins in food samples and clinical isolates.


Material and Methods

7.1 Bacterial strain

          S. aureus strains used as reference strains or positive controls in this study were S. aureus ATCC 13565 (sea), ATCC 14458 (seb), ATCC 23235 (sed), ATCC 33586 (tsst-1), ATCC 19095 (sec, seg, seh, sei and sel) and S. aureus ATCC 23235 (sej). Fifty seven of S. aureus were isolated from 151 RTE food samples in Khon Kaen, Thailand.


7.2  Food sample collection and processing

          The food samples collection and processing were performed as described previously 2. In brief, 151 food samples were randomly collected from food vendors and food shops in Khon Kaen municipality, Thailand (20 food shops in Khon Kaen University and 60 food vendors and food shops outside Khon Kaen University).  Food samples were grouped into three categories: 1) 50 samples of local foods (27 samples of green papaya salad, “somtum” and 23 samples of fermented pork mixed with rice, “nam krug”); 2) 50 samples of spicy seafood salad; and 3) 51 samples of fresh fruit juices and beverages. The food samples were aseptically collected and kept in sterile containers at 4 ºC prior to transfer to the laboratory.

A 25 g of each food sample (solid sample) was cut into small pieces and then, added to 225 ml of sterile Trypticase soy broth (TSB, Oxoid).   The food sample mixture was incubated at 37 ºC for 18-24 hours, and then streaked on Baird-Parker plate containing egg yolk tellurite emulsion (Biomark, India) and incubated at 37 ºC for a further 48 hours 38. Colonies typical of S. aureus (gray to jet-black surrounding opaque zone) were identified using biochemical tests 39.


7.3 DNA extraction

          Genomic DNA of S. aureus was prepared by boiling method according to Perez-Roth et al 40. In brief, S. aureus was grown overnight in brain heart infusion (BHI) with shaking at 37oC following with sedimentation at 13,000 g for 30 seconds. The bacterial pellet was re-suspended in sterile distilled water, boiled for 10 minutes, cooled on ice and sedimentation at 5,000 g for 1 minute. The supernatant was used as a template for PCR assay.  A 5 μl of bacterial lysate was used directly as PCR template.


7.4 PCR assay

          7.4.1 PCR Primer

                   The published primers were selected for detection of Staphylococcal new enterotoxin genes including seh, sej and sel. The new primers specific for seg and sei were designed and assessed in specificity. The primer sequences, amplification sizes and PCR condition are shown in Table 1. All primer pairs were checked for melting temperature, self-dimer, hetero dimer by using integrated DNA technology and test specificity of primer base on in siligo by BLAST software from the NCBI nucleotide public database (http:/ blast.ncbi.nlm.nih.gov/Blast.cgi) and then test specificity of primer using S. aureus reference strains as shown above with uniplex conventional PCR.


Table 1 The primer sequence and PCR condition.

Target gene

Primer sequence

PCR condition


sea (135 bp)




94oC ; 7 min

35 cycles of

94 oC ; 30 sec/ 58 oC ; 30 sec/ 72 oC ; 45 sec

72 oC ; 7 min

Wongboot et al., 2013 41


seb (592 bp)


Wongboot et al., 2013 41


sec (454 bp)


Wongboot et al., 2013 41


sed (263 bp)


Wongboot et al., 2013 41


tsst-1 (371 bp)


Wongboot et al., 2013 41


seg (200 bp)


94oC ; 5 min

35 cycles of

94oC ; 1 min/ 58oC ; 1 min/ 68oC ; 1 min

72oC ; 5 min

This study


sei  (374 bp)


This study


seh (463 bp)



94oC ; 5 min

35 cycles of

94oC ; 1 min/ 56oC ; 1 min/ 68oC ; 1 min

72oC ; 5 min

Cremonesi et al., 2005 25




sej (306 bp)


94oC , 5 min (35 cycle)

35 cycles of

94oC ; 1 min/ 53oC ; 1 min/ 72oC ; 1 min

 72oC ; 5 min

Cremonesi et al., 2005 25


sel (240 bp)


Cremonesi et al., 2005 25



          7.4.2 PCR mixture and PCR amplification

                   The oligonucleotide primers used in this study are listed in Table 1. For uniplex PCR, the amplification reaction was conducted in total volume of 30 μl contained 1X PCR buffer (contain 1.5 mM MgCl2, 10 mM Tris-HCl (pH 8.3), 50 mM KCl), 0.2 mM of deoxynucleotide triphosphate (dNTPs), concentration of primer including 0.5 μM for seg, seh, sei and sej or 0.6 μM for sel of each primer, 0.5 U of Taq DNA polymerase and 300 ng DNA template. After determined using the uniplex PCR with positive results, the duplex PCR of sec and seg, and seg and sei genes were also done.The amplification reaction was conducted in total volume of 30 μl containing 1X PCR buffer,  0.2 mM of dNTPs, concentration of primer including 0.5 μM for sec and seg, and seg and sei , 1 U of Taq DNA polymerase and 300 ng DNA template.  PCR thermocyclings were performed using thermocycler (Bio-Rad C1000 thermal cycler).


7.4.3 Analysis of PCR products

          The amplified products were analyzed by 1.5% agarose gel electrophoresis and stained with ethidium bromide before visualized by UV-transiluminator (Bio-Rad GelTM Doc XR+ Imageer).


          7.4.4 Statistic analysis

          The distribution of newly staphylococcal enterotoxin genes was determined in percentage.







          The enterotoxigenic types of S. aureus strains isolated from food samples obtained from Khon Kaen province in Thailand were investigated.  The results are shown in Table 2 and Figure 1. Fifty seven S. aureus were isolated form 151 RTE foods.  The finding of new enterotoxins showed that sea combined with seg was the most commonly found (12.3%), following with seg combined with sei (8.8%).  The sec coexisted with seg was also found (1.7%).  There were only four of these 57 isolates (7.0%) harbored seg and none of which harbored the seh, sej and sel.  Local food showed the most harboring the new enterotoxin genes. We also determined those new enterotoxin genes in S. aureus strains isolated from diarrheal patients.  Although, the number of isolates was small (4 isolates), 25% (1 isolate) harbored seg and sei together (data not shown).


Table 2 Information of staphylococcal enterotoxin genes detected by PCR assay.



of sample

Number of

S.aureus isolates

Number of toxin-positive and type of toxin (%)






Food (n=151)

Local food



2 (8.3)

3 (12.5)


3 (12.5)

8 (33.3)

Sea food



2 (11.8)

1 (5.9)

1 (5.9)

1 (5.9)

5 (29.4)

Fruit juice and beverage




3 (18.7)


1 (6.3)

4 (25.0)




4 (7.0)

7 (12.3)

1 (1.7)

5 (8.8)

17 (29.8)

Figure1 Gel electrophoresis for PCR products of Staphylococcal enterotoxin (se) genes. Lane M: 1 kb DNA ladder. Lane 1-7: sea (135 bp), sec (454 bp), seg (200 bp), seh (463 bp), sei (374 bp), sej (306 bp) and sel (240 bp) positive control. Lane 8-11: sea, seg, sec+seg and seg+sei of food samples. Lane 12: negative control.



          Previous study, the classical enterotoxin genes (sea-sed and tsst-1) were determined in RTE foods obtained from Khon Kaen province, Thailand 2. The result showed that 60% was positive for presence of those classical enterotoxin genes and sea (46%) was the most common classical enterotoxigenic type to be found 2. The precent study, we further determined some of new S. aureus enterotoxin genes (seg, seh, sei, sej and sel) in S. aureus strains isolated from the same RTE food samples in order to understand the emergence and distribution of new se in the RTE foods in Khon Kaen for indication of the risk of RTE foods in this province.   

          The local foods, “namkrug” and green papaya salad, gently heated foods may promote S. aureus contamination from unhygienic hand contact and/or raw materials2,30. Our previous study showed that the local foods were the highest of carring the classical enterotoxin genes which are similar with these new enterotoxin genes in the present study2. Our result indicated that the new enterotoxin genes were found in 29.8%.  Although, most S. aureus strains harbored the classical enterotoxins, especially sea 2, the combination with other new enterotoxin genes was also found in RTE foods similar to other previous studies 22,23,26,37. Other country studies showed that some of new S. aureus enterotoxin genes that the most recently described were seg, seh, sei, sej and sel 25,42. Coexistence of sea, seb, sec, sed with other new enterotoxins -seg, seh and sei has been reported by other investigators 26,43,44.  These findings showed that the variation of new Staphylococcal enterotoxin gene types was found in foods and can be explained with the epidemiology in each region and the type of foods that detected 21-24,35,36,45 such as Mashouf and colleagues reported that 35.7% of seg had more frequently found than classical se(s) in S. aureus isolated from milk, dairy product and raw meats 37, Omoe and colleagues reported that 38.9% of seg and sei was the most frequently found in S. aureus isolated from raw milk 26. 

          In this study, we also determined those new enterotoxins in S. aureus strains isolated from diarrheal patients.  Although, the number of S. aureus isolated from diarrheal patients was small (4 isolates), 25% harbored seg and sei together (data not shown).  Overall result of staphylococcal enterotoxin genes in S. aureus strains isolated from RTE foods and diarrheal patients in Khon Kaen, it can indicate that the major enterotoxins caused food poisoning were the classical enterotoxins 2, whereas the new enterotoxins may involve to cause food poisoning in Khon Kaen, Thailand.  The result is in agreement with a previous report in Taiwan that showed that S. aureus strains isolated from fecal specimens of patients who were sick from food poisoning outbreaks in Taiwan were mostly positive for classical enterotoxins (67.8%), such as sea or see and some carried seg, seh, sei and seg + sei 23. For the new enterotoxin, the seg was suggested to be detected in association with sei 46,47. In this study, some strains were found to carry seg alone similar to McLauchlin et al. (2000)46 reported.  As, most S. aureus strains harbored the classical enterotoxins (60%) in previous study 2 and when combined with this report, over 90% of S. aureus strains isolated from RTE foods in Khon Kaen harbored the enterotoxin genes, indicated that RTE foods carried a risk for staphylococcal food poisoning.



            This study indicates that some S. aureus strains isolated from RTE foods in Khon Kaen harbored the new enterotoxins alone (seg) and in combination together (sei and seg) or combination with the classical enterotoxins (sea and sec). Therefore, the new enterotoxins may involve causing food poisoning in RTE foods in Khon Kaen, Thailand.  However, it should be aware that the quantitative assessment of these enterotoxin levels should be more elucidated for indicating food-poisoning.





          This study was supported by a Postgraduate Study Support Grant of Faculty of Medicine, Khon Kaen University and an invitation research grant (IN59227) from the Faculty of Medicine, Khon Kaen University, Thailand.



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