Food Sci. Technol. Res.

, 18 (6), 843 848, 2012

Bacterial Contamination of Soybean Curd (Tofu) Sold in Thailand

Chiraporn Ananchaipattana1,2,4, Yukie Hosotani1, Susumu Kawasaki1, Sirikhae Pongswat4, Bari Md. Latiful3,
Seiichiro Isobe1,2 and Yasuhiro Inatsu1*
1

National Food Research Institute, National Agriculture and Food Research Organization, 2-1-12 Kannondai, Tsukuba, Ibaraki, 305-8642,
Japan

Graduate School of Life and Environmental Science, University of Tsukuba, 1-1-1 Tennodai, Tsukuba, Ibaraki, 305-8577, Japan

Center for Advanced Research in Sciences, University of Dhaka, Dhaka-1000, Bangladesh

Department of Biology, Faculty of Science and Technology, Rajamangala University of Technology Thanyaburi, 39 Muh1, Thanyaburi
Pathum Thani, 12110, Thailand

Received April 16, 2012; Accepted July 25, 2012

Soybean curd (Tofu) is a popular food for many people, especially those with health concerns. The objective of this study, therefore, was to evaluate the contamination rate and types of foodborne pathogens
and food spoilage bacteria in packaged and unpackaged tofu sold in Thai markets. A total of 133 tofu
samples (59 packaged tofu samples and 74 unpackaged tofu samples) were collected from open markets
and supermarkets in Thailand. The predominantly identified Gram-negative bacteria were coliforms (67%
in tested samples), Pseudomonas spp. (56%) and Escherichia coli (28%) and the predominantly identified
Gram-positive bacteria were Enterococcus spp. (77%), lactic acid bacteria (68%), Bacillus cereus (41%)
and Staphylococcus spp. (26%). No Listeria spp. were found in any of the tofu samples. The contamination rates of E. coli, Salmonella spp. and Enterococcus spp. in unpackaged tofu were significantly higher
than those in packaged tofu (P < 0.05). Three kinds of Gram-negative pathogenic bacteria, Cronobacter
sakazakii, Salmonella spp. and Yersinia enterocolitica (serotype 0:5), were found only in unpackaged tofu
samples. Of 54 B. cereus isolates, four isolates from three unpackaged tofu samples and one packaged tofu
sample were found to produce diarrheal enterotoxin. The most common Enterococcus spp. isolates were
Enterococcus faecium and Enterococcus faecalis. These results suggested that the improvement of hygienic
practices might be required for reducing the risk of food poisoning and food spoilage of tofu in Thailand.
Keywords: tofu, bacterial contamination, Thailand

Introduction
Tofu (soybean curd) is considered a healthy part of a
well-balanced diet, as it is low in calories and rich in protein, iron, calcium, magnesium, and B-vitamins (Pontecorvo
and Bourne, 1978; Prestamo and Fontecha, 2007). The low
cost of soybean products makes them a suitable alternative
for reducing malnutrition problems in poor people living on
grain-centered diets (Shurtleff and Aoyagi, 1983). Tofu has
been produced for centuries using the same basic methods.
Soybeans are soaked until completely hydrated, rinsed and
ground. The liquid and solid portions are then separated.
The soymilk is heated to the boiling point, filtered and then
*To whom correspondence should be addressed.
E-mail: inatu@affrc.go.jp

precipitated with coagulants such as calcium or magnesium

sulfate, calcium or magnesium chloride. The resultant curd
is formed and pressed into cakes of tofu (Kovats et al., 1984;
Shurtleff and Aoyagi, 1983). Tofu is available in several
types: soft tofu is approximately 84- 89% water, firm tofu is
approximately 79 87% water and has a firm texture, and
dried tofu is the firmest variety, with a moisture content of
60 82%. In Thailand, two categories of tofu (packaged tofu
and unpackaged tofu) are commonly sold in open markets
and supermarkets. Usually, packaged tofu is sold in supermarkets, where it is normally found refrigerated (4 10).
Unpackaged tofu is sold only in open markets, typically by
independent vendors who display the product unwrapped or
covered by banana leaf, laid on a tray or soaked in a large
bucket filled with water at ambient temperature, and where

844

hands can directly touch it. Tofu is easily spoiled in warm

environments by microbial growth due to its characteristics:
high protein, high water content, and neutral pH (Asharaf et
al., 1999; Tuitemwong and Fung, 1991; van Kooij and de
Boer, 1985). Thus, its shelf life is short and storage / distribution is limited.
Spoilage of tofu is characterized by a sour taste and
is associated with bacterial growth (Dotson et al., 1977);
however, limited information has been available on the major bacteria responsible for its spoilage. Joo et al. (1998)
reported that Acinetobacter calcoaceticus, Bacillus cereus,
Klebsiella pneumoniae and Xenorhabdus luminescens were
major causes of tofu spoilage. Dotson et al. (1977) developed criteria for measuring spoilage and attributed lactic acid
bacteria to the phenomenon. In addition, several outbreaks
of yersiniosis have been implicated in tofu; a case in Seattle
(Aulisio et al., 1983) and one in Washington State between
December 1981 and February 1982 (Tacket et al., 1985)
were reported. Several incidents of tofu recalled due to Listeria monocytogenes contamination were also reported (Associated Press, 1992). The lack of good sanitary practices in
tofu manufacturing processes may result in the purchase and
consumption of unacceptable tofu products. The evaluation
of contamination rates and types of contaminating bacteria
in tofu could provide important information for tracing the
source of bacterial contamination, as well as in the development of suitable food hygiene measures for tofu production.
The objective of this study was to evaluate the contamination rates and types of foodborne pathogens / spoilage bacteria, including coliform bacteria, E. coli, Salmonella spp.,
Yersinia spp., C. sakazakii, Pseudomonas spp., Listeria spp.,
B. cereus, Staphylococcus spp., Enterococcus spp., and lactic
acid bacteria (LAB), in packaged and unpackaged tofu sold
in Thai markets.
Materials and Methods
Collection of Thai tofu samples A total of 133 tofu samples, including 74 unpackaged tofu samples from open markets and 59 packaged tofu samples from supermarkets, were
purchased randomly from 12 different open markets and 7
supermarkets in Bangkok (Pathum Thani and Chiang Rai
areas) from September 2010 to February 2012. All samples
were transported to the laboratory of Rajamangala University of Technology Thanyaburi in an insulated box with ice
to maintain the temperature at 4 6. Tofu samples were
homogenized with distilled water (1:2, wt/v) and pH values
were measured using an electric pH meter (F-55 pH meter,
Horiba, Japan).
Isolation of foodborne pathogens and spoilage bacteria
Each 25 g tofu sample (cake and immersion solution) was

C. Ananchaipattana et al.

homogenized in 225 mL of enrichment buffer corresponding

to each kind of bacteria: EEM enrichment broth (Nissui Co.,
Ltd., Tokyo, Japan) for Salmonella spp.; phosphate-buffered
saline (PBS, pH 7.0) for Yersinia spp.; Mossel-Bouillon
enrichment medium (Merck, Darmstadt, Germany) for C.
sakazakii, coliform bacteria and E. coli; Listeria enrichment
broth (Oxoid Ltd., Basingstoke, England) for Listeria spp.;
buffered peptone water (Merck) for Bacillus spp., Staphylococcus spp., Pseudomonas spp. and Enterococcus spp.; and
de Man, Rogosa and Sharpe (MRS) broth (Difco, NH, USA)
for LAB. Enrichment cultivation of Listeria and Yersinia
was performed at 30 for 48 h and 10 for 7 days, respectively. The other enrichment cultivations were performed at
30 35 for 24 h. A loopful of each enrichment culture was
streaked onto the corresponding selective media [PBS (pH
7.0) cultures for Yersinia spp. were streaked onto Yersinia selective agar (Oxoid Ltd) with Yersinia selective supplement
SR0109 (Oxoid Ltd), Mossel-Bouillon enrichment cultures
were streaked onto Chromocult Enterobacter Sakazakii agar
(Merck) and MacConkey Sorbitol agar (Nissui Co., Ltd., Tokyo, Japan), Listeria enrichment was streaked onto Listeria
selective agar (Oxoid Ltd) supplemented with SR0140E (Oxoid Ltd), buffered peptone water was streaked onto NGKG
agar (Nissui Co., Ltd) with 20% egg yolk, mannitol salt agar
(Nissui Co.) with 20% egg yolk and NAC agar (Nissui Co.)
and MRS broth was streaked on MRS agar], and the plates
were incubated at 30 35 for 24 48 h. Portions (0.5 and
1.0 mL) of the EEM-enriched samples were transferred to
10 mL of Rappaport-Vassiliadis (RV) broth (Eiken Co., Ltd.,
Tokyo, Japan) (incubated at 42 for 20 h) and 10 mL Hajna
tetrathionate (TT) broth (Eiken Co.) (incubated at 35 for
20 h), respectively. To isolate Salmonella strains, the cultures
were streaked onto DHL agar (Nissui Co.), Bismuth sulfide
agar (Difco) and MLCB agar (Nissui Co.) and incubated
at 35 for 20 h. Ten milliliters of buffered peptone water
culture was added to 10 mL of two times concentration (2x)
of AC medium (Nissui Co.) and incubated at 35 for 20 h.
After incubation, one loopful of culture was inoculated into
a 10 mL of standard concentration (1x) of AC medium and
incubated at 42 for 20 h. To isolate Enterococcus strains, a
loopful of 1x AC culture was streaked onto EF agar (Nissui
Co.). Aliquots (10 mL) of the Mossel-Bouillon enrichment
cultures were transferred to 10 mL of two times concentration (2x) of EC medium (Nissui Co.) and incubated at 35
for 20 h. One loopful of culture was inoculated into a 10 mL
of standard concentration (1x) of EC medium with Durham
fermentation tubes and incubated at 42 for 20 h. To isolate
E. coli strains, a loopful of 1x EC culture broth from a gas
producing tube was streaked onto EMB agar (Nissui Co.).
After incubation, strains were isolated by visual observation

Bacteria in Thai Tofu

845

of colony shape and color, and stored at 4 until further

studies.
Identification of bacterial isolates Characterization of
the isolates was based on colony morphology, shape of microscopic features after Gram straining, biochemical characteristics in the TSI/LIM test (Nissui Co.) and API diagnostic
system (BioMrieux, Marcy lEtoile, France). Suspected
strains of Salmonella spp. and Listeria spp. were picked and
subjected to further immunological tests using a Salmonella
LA Seiken latex-agglutination test kit (Denka Seiken Co.,
Ltd., Tokyo, Japan) and a NH Immunochromato Listeria kit
(Cosmo Bio Co., Ltd., CA, USA), respectively. Identification of Yersinia spp., C. sakazakii, Listeria spp. and S. aureus was performed using 16S ribosomal DNA sequencing.
Production of diarrheal enterotoxin and the existence of the
cereulide synthetic enzyme (CRS) gene of B. cereus were
determined with a commercially available CRET-RPLA Kit
(Denka Seiken Co., Ltd) and a PCR detection kit (Takara Bio
Inc., Tokyo, Japan), respectively. The antiserum type of isolated Y. enterocolitica strains was fixed by a Yersinia enterocolitica O-Antisera SEIKEN set (Denka Seiken Co., Ltd).
Suspected colonies of E. coli serotype O26, O157 or O111
were picked from XM-EHEC agar (Nissui Co., Ltd) and CTMacConkey Sorbitol agar (Nissui Co., Ltd) and confirmed
by biochemical characteristics in TSI/LIM tubes (Nissui Co.,
Ltd). The O26, O157 or O111 antisera (Denka Seiken Co.,
Ltd) were used for serotype confirmation. The possible production of Shiga-like toxin (stx) 1 and Shiga-like toxin (stx)
2 was assayed by NH Immunochromato VT1/2 (Cosmo Bio
Co., Ltd., CA, USA) and O-157 VT1/2 PCR Typing Set Plus
(Takara Biotechnology Co., Ltd).
Statistical analysis Differences between the two categories of tofu were evaluated using the Students t-test. Mi-

crosoft EXCEL 2007 was used for the data analysis.

Results and Discussion
Tofu is recognized as a very good source of protein and
numerous other nutrients necessary for good health. However, there are few published reports about the contamination
rate or prevalence of foodborne pathogens / spoilage bacteria
in tofu products. In this study, 11 kinds of bacteria (coliform
bacteria, E. coli, Salmonella spp., Yersinia spp., C. sakazakii,
Pseudomonas spp., Listeria spp., B. cereus, Staphylococcus
spp., Enterococcus spp., and LAB) were isolated and identified from 133 Thai tofu samples, including 74 unpackaged
samples from 38 vendors and 59 packaged samples manufactured by 17 commercial brands, purchased from September 2010 to February 2012. The pH range of collected tofu
samples was recorded as 4 6 in both tofu categories. A low
pH level in tofu is reported to be associated with the growth
of Gram-positive organisms, primarily Streptococcus sp. and
Pediococcus sp. (Tuitemwong and Fung, 1991).
The contamination rate of bacteria in the collected 133
tofu samples is summarized in Table 1. The contamination
rate of Gram-negative bacteria was 67% for coliform bacteria, 56% for Pseudomonas spp., 28% for E. coli, 4% for Salmonella spp., 2% for Yersinia spp. and 1% for C. sakazakii.
Nine E. coli O26, O157 and O111 suspected isolates did not
harbor stx1/2 genes or produce Shiga-like toxins. The identified bacteria isolated from each category of tofu sample are
shown in Table 2. In the 32 types of Gram-negative isolates,
12 kinds of them were found in both tofu sample categories
(Citrobacter braakii, Citrobacter freundii, Enterobacter aerogenes, Enterobacter cancerogenus, Enterobacter cloacae, E.
coli, Klebsiella oxytoca, Pantoea spp., Rahnella aquatilis,
Serratia marcescens, Serratia odorifera and Pseudomonas

Table 1. Contamination rate of bacteria in Thai tofu.

Pathogens
Coliform bacteria*
Escherichia coli*
Salmonella spp.*
Yersinia spp.
Cronobacter sakazakii
Pseudomonas spp.
Listeria spp.
Bacillus spp.
Staphylococcus spp.
Enterococcus spp.*
Lactic acid bacteria

Tofu samples
packaged tofu

(%)

unpackage tofu

(%)

total tofu

(%)

26/59
1/59
0/59
1/59
0/59
35/59
0/59
24/59
14/59
37/59
40/59

44
2
0
2
0
59
0
41
24
63
68

63/74
36/74
5/74
1/74
1/74
40/74
0/74
30/74
21/74
65/74
51/74

85
49
7
1
1
54
0
40
28
88
69

89/133
37/133
5/133
2/133
1/133
75/133
0/133
54/133
35/133
102/133
91/133

67
28
4
2
1
56
0
41
26
77
68

The * indicates a significant difference (P<0.05) in the contamination rate of each bacterium between the two categories
of tofu.

C. Ananchaipattana et al.

846
Table 2. Identified Gram-negative and Gram-positive bacteria in Thai tofu.
Categories of tofu

packaged tofu

Gram-negative bacteria

Gram-positive bacteria

Acinetobacter baumannii
Aeromonas hydrophila
Citrobacter braakii
Citrobacter freundii
Enterobacter aerogenes
Enterobacter amnigenus
Enterobacter cancerogenus
Enterobacter cloacae
Escherichia coli
Klebsiella oxytoca
Pantoea spp.
Rahnella aquatilis
Serratia marcescens
Serratia odorifera
Yersinia intermedia

Aneurinibacillus aneurinilyticus
Bacillus cereus
Brevibacillus laterosporus
Bacillus mycoides

Pseudomonas spp.

Categories of tofu

unpackaged tofu

Staphylococcus hominis
Staphylococcus lentus
Staphylococcus sciuri
Staphylococcus xylosus
Aerococcus viridans
Enterococcus faecalis
Enterococcus faecium
Enterococcus durans
Lactobacillus acidophilus
Lactobacillus brevis
Lactobacillus collonoides
Lactobacillus fermentum
Lactobacillus plantarum
Leuconostoc lactis
Leuconostoc mesenteroides ssp. mesenteroides/dextranicum
Pediococcus pentosaceus
Weissella confusa

Gram-negative bacteria

Gram-positive bacteria

Buttiauxella agrestis
Citrobacter braakii
Citrobacter freundii
Citrobacter koseri
Citrobacter youngae
Cronobacter sakazakii
Enterobacter aerogenes
Enterobacter asburiae
Enterobacter cancerogenus
Enterobacter cloacae
Enterobacter hormaechei
Escherichia coli
Klebsiella oxytoca
Klebsiella pneumoniae ssp. pneumoniae
Kluyvera spp.
Pantoea spp.
Pasturella pneumotropica
Proteus mirabilis
Proteus penneri
Proteus vulgaris
Rahnella aquatilis
Salmonella spp.
Serratia fonticola
Serratia liquefaciens
Serratia marcescens
Serratia odorifera
Yersinia enterocolitica (serotype 0:5)

Bacillus cereus
Bacillus mycoides

Pseudomonas spp.

Staphylococcus capitis
Staphylococcus lentus
Staphylococcus sciuri
Staphyloccous xylosus
Micrococcus spp.
Microbacterium spp.
Enterococcus avium
Enterococcus faecalis
Enterococcus faecium
Lactobacillus acidophilus
Lactobacillus brevis
Lactobacillus collinoides
Lactobacillus delbrueckii ssp. delbrueckii
Lactobacillus fermentum
Lactobacillus plantarum
Leuconostoc lactis
Leuconostoc lactis ssp. lactis
Leuconostoc mesenteroides ssp. mesenteroides/dextranicum
Pediococcus pentosaceus
Weissella confusa

Bacteria in Thai Tofu

847

spp). Four kinds of Gram-negative bacteria were found only

in packaged tofu (Acinetobacter baumannii, Aeromonas hydrophila, Enterobacter amnigenus and Yersinia intermedia).
Sixteen kinds of Gram-negative bacteria were found in only
unpackaged tofu (Buttiauxella agrestis, Citrobacter koseri,
Citrobacter youngae, Cronobacter sakazakii, Enterobacter
asburiae, Enterobacter hormaechei, Klebsiella pneumoniae
ssp. pneumoniae, Kluyvera spp., Pasteurella pneumotropica,
Proteus mirabilis, Proteus penneri, Proteus vulgaris, Salmonella spp., Serratia fonticola, Serratia liquefaciens and Y.
enterocolitica).
A high coliform bacteria contamination rate (67%) in
Thai tofu was found in this study. Rehberger (1984) reported
that coliform bacteria were found often in fresh tofu. On
the other hand, a substantially higher E. coli contamination
rate was observed in unpackaged tofu (49%) than in packaged tofu (2%) in this study. E. coli contamination of commercial foods is typically of human or animal origin, and
grows under inappropriate temperature control. Differences
in hygienic conditions of these markets relates to the rate of
E. coli contamination. A previous outbreak of yersiniosis in
Seattle was thought to be associated with the water used in
the manufacturing processes (Aulisio et al., 1983). The other
case of yersiniosis in Washington State was associated with
contaminated tofu (Tacket et al., 1985). Moreover, Y. enterocolitica was detected in 11% of 154 collected tofu samples
sold in the Netherlands (van Kooij and Boer, 1983). In this
study, out of two Yersinia spp. isolates (2% contamination
rate in tested samples), one was Y. intermedia from packaged
tofu and the other one was Y. enterocolitica (serotype 0:5)
from unpackaged tofu. According to Kovats et al. (1984), Y.
enterocolitica can increase to 4.0 to 6.0 log cycles within 14
days at 5, but sufficient heat treatment of tofu after packaging can inactivate this bacterium.
This is the first report that shows the contamination of
Salmonella spp. into commercially distributed tofu. Salmonella spp. were found only in unpackaged tofu (7%)
purchased from open markets. All of these contaminated unpackaged tofu samples were sold in close proximity to meat,
suggesting that the display of unwrapped tofu products in
these areas and/or the direct touching of tofu after touching
meat may increase the risk of contamination with pathogenic
bacteria. C. sakazakii contamination was also found only in

unpackaged tofu. The source of C. sakazakii contamination

is probably similar to that of Salmonella spp.
The contamination rate of Gram-positive bacteria in collected tofu samples was 77% for Enterococcus spp., 68% for
LAB, 41% for B. cereus and 26% for Staphylococcus spp.,
while no Listeria spp. were found in any of the collected
samples. Fouad and Hegeman (1993) observed that major
LAB species were found in all aged tofu samples and major
Enterococcus spp. were found in all aged tofu samples except for 1 day-old lot of tofu. Sixteen of 26 kinds of Grampositive bacteria isolated from the 133 tofu samples were
found in both categories of tofu samples (B. cereus, Bacillus
mycoides, Staphylococcus lentus, Staphylococcus sciuri,
Staphylococcus xylosus, Enterococcus faecalis, Enterococcus faecium, Lactobacillus acidophilus, Lactobacillus brevis, Lactobacillus collonoides, Lactobacillus fermentum,
Lactobacillus plantarum, Leuconostoc lactis, Leuconostoc
mesenteroides ssp. mesenteroides, Pediococcus pentosaceus
and Weissella confuse). Five kinds of Gram-positive bacteria were found only in packaged tofu (Aneurinibacillus
aneurinilyticus, Brevibacillus laterosporus, Staphylococcus
hominis, Aerococcus viridans and Enterococcus durans).
Five kinds of Gram-positive bacteria were found in only
unpackaged tofu (Staphylococcus capitis, Micrococcus spp.,
Microbacterium spp., Enterococcus avium and Lactobacillus
delbrueckii ssp. delbrueckii).
Of 54 B. cereus isolates, 4 isolates from 3 unpackaged
and 1 isolate from packaged tofu samples produced diarrheal
enterotoxin. No isolated B. cereus strains harbored the CRS
gene (Table 3). No statistically significant differences in the
contamination rate of B. cereus in packaged tofu (36%) and
that in unpackaged tofu (36%) were observed. The source of
contamination might be the presence of B. cereus spores on
soybean seeds, which survived the heat treatment step of soy
milk production.
In this study, S. aureus strains were not found in any of
the tested tofu samples. However, 26% of tested tofu samples
were contaminated with Staphylococcus spp. This might be
due to inadequate sanitary practices during production and
inappropriate storage conditions.
The contamination rates of coliform bacteria, E. coli,
Salmonella spp. and Enterococcus spp. in unpackaged tofu
samples were significantly higher than those in packed tofu

Table 3. Production of B. cereus diarrheal enterotoxins in Thai tofu.

Categories of tofu

Number of tested samples

Number of isolated B. cereus

Number of positive enterotoxin production

Packaged tofu
Unpackaged tofu
Total

59
74
133

24
30
54

1
3
4

C. Ananchaipattana et al.

848

samples (P < 0.05) (Table1). This study confirmed the concerns regarding the safety of unpackaged tofu sold in openmarkets.
Results of this microbiological survey of two categories
of tofu highlight the inadequacy of sanitary practices during
tofu production and the exposure of tofu to inappropriate
open-market storage conditions, leading to contamination.
The presence of Y. enterocolitica, Salmonella spp., C. sakazakii or the higher contamination rate of E. coli and B. cereus
in foods constitutes or indicates a potential health hazard.
Thus, good manufacturing practices (GMP) during the production process, hygienic distribution practices and proper
storage conditions are necessary for producing high quality
tofu. Moreover, increasing public awareness of the proper
manufacturing, storage and hygienic handling of tofu is recommended.

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Dontson, C.R., Frank, HA. and Cavaletto, C.G. (1977). Indirect
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Fouad, H.K. and Hegeman, G.D. (1993). Microbial spoilage of tofu
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Joo, G.J., Hur, S.S., Choi, Y.H. and Rhee, I.K. (1998). Characterization and identification of bacteria from putrefying soybean curd.
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Acknowledgements

This work was supported by a grant from the

Rehberger, T.G., Wilson, L. A. and Glatz, B.A. (1984). Microbio-

Ministry of Agriculture, the Forestry and Fisheries of Japan (research

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