JMID/ 2017; 7 (1): 13-20
Jou nal o Mic obiology and In ec ious Diseases doi: 10.5799/ahinjs.02.2017.01.0247
Co espondence: D . Thuan Huu Vo, Uni e si y o Tampe e, School o Heal h Sciences, Depa men o Epidemiology, Tampe e,
Finland, E-mail: [email p o ec ed]
Recei ed: 14 June 2016, Accep ed: 26 Oc obe , 2016
Copy igh © JMID / Jou nal o Mic obiology and In ec ious Diseases 2017, All igh s ese ed
RESEARCH ARTICLE
Epidemiologic Cha ac e is ics o Foodbo ne Ou b eaks in Sou he n
Vie nam, 2009–2013
Thuan Huu Vo1,2, Nguyen Nhu T an Minh3, Vinh Le2, Ninh Hoang Le2, Huy Quang Nguyen2, Tuan Van
Le4, J. Pekka Nuo i1
1Uni e si y o Tampe e, School o Heal h Sciences, Depa men o Epidemiology, Tampe e, Finland
2Ins i u e o Public Heal h, Depa men o Planning and Technical Suppo , Ho Chi Minh Ci y, Vie nam
3Vie nam Field Epidemiology T aining P og am, Gene al Dep. o P e en i e Medicine, Minis y o Heal h, Hanoi,
Vie nam
4Wo ld Heal h O ganiza ion Technical O ice, Ho Chi Minh Ci y, Vie nam
ABSTRACT
In oduc ion: Accu a e da a on he bu den o oodbo ne diseases (FBD) a e impo an o in o m p e en ion and
con ol measu es. We desc ibed epidemiologic cha ac e is ics and assessed ends in oodbo ne ou b eaks in
Sou he n Vie nam.
Me hodology: We analyzed su eillance da a o ou b eaks epo ed in Sou he n Vie nam du ing 2009–2013. A FBD
ou b eak is de ined as “ wo o mo e people who go gas oin es inal diso de a e ea ing he same meal o one a al
case a e ea ing a meal”. Annual a es o ou b eaks/100,000 popula ion we e calcula ed; ends in ou b eaks we e
assessed in ime-se ies analysis.
Resul s: Du ing 2009-2013, he e we e 261 epo ed ou b eaks, 10,263 cases, and 50 dea hs; a e, 0.16
ou b eaks/100,000 popula ion/yea . O all ou b eaks, 77% occu ed in nine p o inces (popula ion 19.4 million) whe e
expo manu ac u ing zones a e loca ed (2–8 ou b eaks/p o ince/yea ). O 212 ou b eaks in which epo e s had
suspec ed an e iology, bac e ia accoun ed o 41%, na u al oxins o 20%, and unknown causes o 28%. Se en y-
wo pe cen o all cases we e associa ed wi h meals ea en in can eens; 94% o cases li ed in he nine p o inces.
Fou pe cen o all cases we e linked o amily meals; 85% o hese cases li ed in he u al Mekong Del a egion. All
50 a al cases we e a ibu ed o oxic chemicals o na u al oxins, 48 we e amily meals. Mos ou b eaks occu ed in
wa me mon hs, bu no empo al end was seen in epo ed ou b eaks.
Conclusions: The a e o epo ed ou b eaks and o al epo ed cases o FBD we e low, sugges ing unde de ec ion
and unde epo ing. Mos iden i ied ou b eaks we e associa ed wi h meals ea en in can eens; a al cases we e linked
o amily meals. J Mic obiol In ec Dis 2017; 7(1): 13-20
Keywo ds: Foodbo ne diseases, epidemiology, ou b eaks, su eillance, Vie nam
INTRODUCTION
In de eloping coun ies, oodbo ne diseases
(FBD) su eillance sys ems a e o en
subop imal; epidemiologic cha ac e is ics o FBD
a e insu icien ly desc ibed, and mo bidi y and
mo ali y due o FBD is p obably unde es ima ed
[1]. In Vie nam, a ailable da a on FBD come
p ima ily om oodbo ne ou b eak epo s [2].
The Vie nam Food Adminis a ion (VFA) and
Food Sa e y Agencies (FSAs) gene ally ecei e
epo s o ood poisonings o gas oen e i is
ou b eaks when local epo e s suspec
ansmission h ough ood. Mos ou b eaks a e
de ec ed when se e e cases a e admi ed o
heal h acili ies o when dea hs ha e occu ed. A
ew e en s ha e been epo ed by dis ic
hospi als, heal h wo ke s, o local esiden s
while some e en s ha e been de ec ed om
daily newspape epo s.
Pee - e iewed publica ions ela ed o
epidemiology o FBD in Vie nam a e sca ce. We
desc ibed he epidemiologic cha ac e is ics and
assessed ends o oodbo ne ou b eaks in
Sou he n Vie nam om 2009 o 2013.
14 Vo TH, e al. Foodbo ne Ou b eaks in Sou he n Vie nam
J Mic obiol In ec Dis www.jmidonline.o g Vol 7, No 1, Ma ch 2017
METHODS
In Vie nam, na ional su eillance schemes
ela ed o ood sa e y a e passi e. The
su eillance sys ems o FBD a e unde he
au ho i y o he VFA in Minis y o Heal h (MOH).
In 2009, a FSA was es ablished in each o 63
p o inces o be esponsible o su eillance and
con ol o FBD. Acco ding o cu en egula ions,
all heal h o icials, public and p i a e heal h
se ices a e esponsible o no i y FSAs a dis ic
o p o incial le els when a suspec ed oodbo ne
ou b eak occu s in hei se ing. When cases o
FBD a e admi ed o a heal h acili y, he acili y
has o epo o a highe -le el acili y and
ul ima ely o he VFA. In se e e ou b eaks o
hose associa ed wi h dea hs, p e en i e
medicine se ices, heal h acili ies, o dis ic
FSAs a e allowed o sha e da a/ epo s ou side
hei ju isdic ion [3,4].
In 2013, he popula ion o 19 Sou he n p o inces
o Vie nam was 33 million (37% o he o al
popula ion o Vie nam) [5]. We analyzed ou ine
su eillance da a o no i ied oodbo ne ou b eaks
om hese p o inces du ing 2009–2013. A FBD
ou b eak is de ined as “ wo o mo e people who
go gas oin es inal diso de a e ea ing he
same meal o one a al case a e ea ing a meal”
[4]. The FSAs in Sou he n p o inces o Vie nam
use a s anda d epo ing o m which includes he
ollowing i ems: loca ion o ou b eak, implica ed
meal and ood, pa ien ’s clinical signs and
symp oms, causa i e agen s, numbe o
exposed, cases, dea hs and hospi aliza ion by
age g oups, samples aken om cases and
oods o labo a o y analysis, en i onmen al
inspec ions, as well as conclusions and
ecommenda ions ela ed o he ou b eak.
In es iga ed ou b eaks a e epo ed o he
Ins i u e o Public Heal h in Ho Chi Minh Ci y [3].
Ca ego ized a iables we e desc ibed in
equencies and p opo ions. Ra es we e
calcula ed by using he o al annual ou b eaks
du ing 2009-2013 di ided by mean popula ion o
he egion/p o ince du ing he s udy pe iod.
Time-se ies analysis was used o assess ends
and seasonal ac o s in ou b eaks. Da a we e
analyzed by using R so wa e ( se ies and
o ecas packages).
RESULTS
Du ing 2009–2013, 261 oodbo ne ou b eaks
we e epo ed in he 19 p o inces in Sou he n
Vie nam. Annually, abou 2–8 oodbo ne
ou b eaks we e epo ed in Ho Chi Minh Ci y
(HCMC) and eigh p o inces a ound HCMC
(Figu e 1A), accoun ing o 77% o all ou b eaks.
The popula ion o HCMC and he eigh
p o inces we e abou 7.5 and 11.9 million,
espec i ely. The a e o gene al oodbo ne
ou b eaks in Sou he n Vie nam was es ima ed a
0.16 pe 100,000-popula ion pe yea . Ra es o
ou b eaks in p o inces a ound HCMC we e
highe han hose in p o inces in Mekong Del a
egion (Figu e 1B).
O he 261 epo ed ou b eaks, 38% we e
associa ed wi h can eens, 31% wi h amily
meals and 18% wi h es au an s. Abou 7% o
he ou b eaks occu ed in schools and 6% we e
associa ed wi h s ee endo s. On a e age,
app oxima ely 20 ou b eaks we e associa ed
wi h can eens and 16 wi h amily meals annually
in he egion (Figu e 2).
O he 212 (81%) ou b eaks in which e iology
was suspec ed, bac e ia we e pos ula ed in 87
(41%), na u al oxins in 42 (20%), and
unknown/unde ined causes in 59 (28%) o he
ou b eaks (Table 1). O he 49 (19%) ou b eaks
in which e iology was con i med by labo a o y
es s (labo a o y me hods we e based on he
Vie nam Food Sa e y S anda d – app o ed by
ISO/IEC 17025 – and he Associa ion o O icial
Analy ical Chemis s in e na ional s anda ds o
ood i ems), bac e ia (E. coli, S. au eus,
Salmonella spp., B. ce eus, C. pe ingens, and
Shigella spp.) accoun ed o 23 (47%), his amine
o 17 (35%), chemicals (me hanol,
ino ganochlo ine, o ganophospho us, ni a es,
and oden icides) o 7 (14%), and e odo oxin
o 2 (4%). In 181 (69%) ou b eaks links o
speci ic oods we e sugges ed, bu hese we e
no con i med by epidemiologic o labo a o y
in es iga ion. The mos common suspec ed ood
i ems we e po k (15%), una ish (13%), mul i-
ing edien oods (12%), jelly ish (8%), alcohol
con aining me hanol (7%), oad (6%), and pu e
ish (6%).
In each speci ic loca ion whe e oodbo ne
ou b eaks occu ed, bac e ia we e suspec ed
accoun o mos (33% in amily meals, 49% in
la ge can eens, 65% in schools, 77% in
15 Vo TH, e al. Foodbo ne Ou b eaks in Sou he n Vie nam
J Mic obiol In ec Dis www.jmidonline.o g Vol 7, No 1, Ma ch 2017
es au an s, and 84% in s ee endo s). The
pe cen ages o unknown/unde ined causes we e
12% in s ee endo s, 16% in es au an s, 18%
in amily meals, 25% in la ge can eens, and 35%
in schools. Fo ou b eaks which occu ed in
p i a e homes, na u al oxins accoun ed o 31%
o ou b eaks (Figu e 3). Among 44 ou b eaks
caused by na u al oxins, 91% we e associa ed
wi h amily meals. O ou b eaks associa ed wi h
chemicals, 61% (11) we e linked o amily meals.
A o al o 10,263 cases we e pa o he epo ed
ou b eaks. Abou 72% o cases had ea en hei
meals a can eens in indus ial zones and 14%
in es au an s, while only 5%, 4%, and 4% o
cases we e associa ed wi h ou b eaks in o he
loca ions (schools, s ee endo s, and amily
meals, espec i ely) (Figu e 4). O he cases
linked wi h can eens, 94% (6927) li ed in HCMC
and he eigh su ounding p o inces al eady
men ioned be o e. O he 428 cases associa ed
wi h 82 ou b eaks occu ing a p i a e
esidences, 85% (363) o cases we e in he u al
Mekong Del a egion. The numbe o po en ially
exposed pe sons (de ined as hose who a e he
same meal as cases) was abou 78,000 du ing
2011–2013 (Table 1).
O he 50 a al cases, 48 we e associa ed wi h
amily meals, while one case was associa ed
wi h s ee endo and one wi h a wedding pa y
(Table 1). The implica ed oods in a al cases
we e alcohol con aining me hanol (28), jelly ish
(07), oad (07), pu e ish (06), and sea-c abs
(02).
In Figu e 5, he obse ed da a on ou b eak
no i ica ions we e decomposed in o h ee
componen s: end, seasonal, and
andom/ esidual componen s. A e emo ing
seasonal e ec s, no end was seen in epo ed
ou b eaks du ing 2009–2013. The e we e mo e
ou b eaks in 2010 han in he o he yea s. The
numbe o ou b eaks pe mon h a ied by
season and was highe du ing summe (highes
in May) and lowe du ing win e (lowes in
Decembe ). The mon hs wi h ewes ou b eaks
we e Feb ua y–Ma ch and Augus -Decembe .
Table 1. Baseline cha ac e is ics o he s udy popula ion.
Ou b eak Yea s
2009
2010
2011
2012
2013
To al
Numbe o epo ed ou b eaks
42
80
48
48
43
261
Numbe exposed
NA
NA
20,555
20,675
36,639
77,869
Numbe o cases
1,903
3,076
1,233
2,032
2,019
10,263
Numbe o dea hs
11
12
12
12
3
50
Numbe o suspec ed oods
35
62
32
26
26
181
Numbe o ou b eaks wi h suspec ed e iology
17
67
37
48
43
212
Bac e ia
3
30
19
15
20
87
Na u al oxins
3
9
11
9
10
42
Ro en ood
1
9
1
0
2
13
Chemicals
1
4
1
5
0
11
Unknown
9
15
5
19
11
59
Numbe o ou b eaks wi h con i med e iology
25
13
11
-
-
49
Bac e ia
7
7
9
-
-
23
Na u al oxins
0
2
0
-
-
2
Ro en ood
16
1
0
-
-
17
Chemicals
2
3
2
-
-
7
16 Vo TH, e al. Foodbo ne Ou b eaks in Sou he n Vie nam
J Mic obiol In ec Dis www.jmidonline.o g Vol 7, No 1, Ma ch 2017
Figu e 1. Annual numbe (A) and a e o oodbo ne ou b eaks pe 100,000 (B), Sou he n Vie nam, 2009–2013
Figu e 2. Annual numbe o ou b eaks by implica ed loca ion, Sou he n Vie nam, 2009–2013
Figu e 3. E iology o oodbo ne ou b eaks by place o occu ence, Sou he n Vie nam, 2009–2013
17 Vo TH, e al. Foodbo ne Ou b eaks in Sou he n Vie nam
J Mic obiol In ec Dis www.jmidonline.o g Vol 7, No 1, Ma ch 2017
Figu e 4. Loca ion o oodbo ne ou b eaks and numbe o cases by yea , Sou he n Vie nam, 2009–2013
Figu e 5. Decomposi ion o addi i e ime-se ies o epo ed ou b eaks by yea , Sou he n Vie nam, 2009–2013
DISCUSSION
Mos de ec ed ou b eaks and cases we e
associa ed wi h can eens in HCMC and
neighbo ing p o inces, whe e many expo
manu ac u ing zones a e loca ed. In abou a hal
o hese ou b eaks he suspec ed e iology was
bac e ia and mo e han a qua e o suspec ed
ood i ems con ained po k o we e mul i-

18 Vo TH, e al. Foodbo ne Ou b eaks in Sou he n Vie nam
J Mic obiol In ec Dis www.jmidonline.o g Vol 7, No 1, Ma ch 2017
ing edien oods. This inding is consis en wi h
ea lie epo s o ood poisonings o acu e
gas oen e i is ou b eaks in he expo
manu ac u ing zone can eens being associa ed
wi h poo pe sonal hygiene and ime-
empe a u e abuse du ing ood p epa a ion and
se ing [6,7]. Tuna ish accoun ed o a
conside able p opo ion o suspec ed oods.
P ope handling and empe a u e con ol o una
ish a e impo an o p e en simila ou b eaks,
pa icula ly in he yea - ound ho wea he in
Sou he n p o inces o Vie nam [8].
Ou b eaks associa ed wi h amily meals mainly
occu ed in he Mekong Del a egion. Al hough
he e we e ew cases, hese accoun ed o 96%
o all epo ed a al cases. The a al cases we e
caused by consump ion o coun e ei alcohol
con aining me hanol o na u al oxins. I is clea
ha alcohol sales should be con olled and
heal h educa ion should be s eng hened o
a oid consump ion o coun e ei alcohol and he
common animals con aining na u al oxins.
O e all, he e we e mo e ou b eaks in wa me
mon hs (Figu e 5). The wa m and humid clima e
in Sou he n Vie nam ( om 28°C o 35°C)
enables mic oo ganisms o g ow and p oli e a e
as e in con amina ed oods [9,10]. The highe
numbe o ou b eaks du ing summe in 2010
could be ela ed o he highe empe a u e
du ing he summe han o he yea s [11].
Au ho i ies o ood sa e y egula ly conduc wo
in ensi ied inspec ions annually abou one mon h
be o e mid-au umn es i al and luna New Yea
ac oss Vie nam e e y yea . Fewe epo ed
ou b eaks du ing Augus –Decembe and
Feb ua y–Ma ch could be a esul o he
inspec ions.
Ou b eak no i ica ions only p o ide a c ude
es ima e o he bu den o oodbo ne illness. The
ou ine su eillance da abase in Sou he n
Vie nam only included oodbo ne ou b eak
epo s, p obably om se e e e en s. No
demog aphic o epidemiologic in o ma ion was
collec ed o indi idual cases. In addi ion, sel -
medica ion wi h speci ic d ugs which can be
ob ained wi hou p esc ip ion, could a ec
de ec ion o ou b eaks. Because o hese
easons, many mild ou b eaks may no ha e
been no i ied o we e unde no i ied. I is likely
ha he a e o ou b eaks and numbe o cases
es ima ed om he su eillance da a a e likely
an unde es ima ion. F om 2000 o 2010, a o al
o 2,147 oodbo ne ou b eaks, 60,602 cases and
583 dea hs we e epo ed h oughou Vie nam;
he incidence o cases was 6.9 pe 100,000
people pe yea . This was qui e low compa ed
wi h o he coun ies in he egion, e.g., 47.8 pe
100,000 people in Malaysia and 67.8 pe
100,000 people in Thailand, and e en
de eloped coun ies e.g., 290 pe 1000 people
in Ne he land [12-15].
Mos iden i ied ou b eaks we e associa ed wi h
can eens in expo manu ac u ing zones.
Ou b eaks in his kind o se ings whe e he
a ec ed coho is well de ined a e mo e likely o
be de ec ed and in es iga ed han ou b eaks in
which cases a e widely dispe sed in he
communi y because o con amina ed
comme cial p oduc s [16,17]. The e o e,
de ec ion bias should be conside ed when
in e p e ing he indings ela ed o he se ing o
no i ied ou b eaks.
Beside unde es ima ion and de ec ion bias, ou
s udy has some limi a ions. Fi s , he da abase
did no include in o ma ion o indi iduals and
epo ing ime, so cha ac e is ics o cases and
delays in epo could no be desc ibed. Second,
incuba ion ime was no collec ed and mos
implica ed oods we e pos ula ed, no con i med
by epidemiologic in es iga ion. Thi d, mos
causa i e agen s o he ou b eaks we e
suspec ed on he basis o subjec i e
assessmen s, no labo a o y e idence was
p esen ed, and con ibu ing ac o s we e no
documen ed. These indica e lack o applica ion
o s anda d epidemiologic me hods in ou b eak
in es iga ions making i di icul o assess which
ac o s uly con ibu ed o he epo ed
ou b eaks. Finally, he cu en su eillance
sys em o oodbo ne diseases has low
sensi i i y and capaci y o ea ly de ec ion o
oodbo ne ou b eaks. To enable ea ly de ec ion,
su eillance sys ems o FBD ha a e capable o
eco ding/ e iewing no i ica ions and complain s
om he public (no i ica ion/complain sys ems)
and o collec ing in o ma ion on FBD symp oms
(synd omic su eillance) should be conside ed.
In addi ion, labo a o y capaci y should be
s eng hened. Da a agg ega ion om he new
and exis ing su eillance sys ems o FBD would
enable be e es ima ion o FBD bu den and
in o m e idence-based p e en ion and con ol
measu es.
19 Vo TH, e al. Foodbo ne Ou b eaks in Sou he n Vie nam
J Mic obiol In ec Dis www.jmidonline.o g Vol 7, No 1, Ma ch 2017
Conclusion
The a e o epo ed ou b eaks and o al
epo ed cases o FBD in Sou he n Vie nam
we e low, sugges ing unde -de ec ion and
unde epo ing. Mos iden i ied ou b eaks we e
associa ed wi h can eens in expo
manu ac u ing zones and could be linked o poo
pe sonal hygiene and ime- empe a u e abuse
[7]. Homemade ood ou b eaks mainly occu ed
in u al a eas and associa ed wi h mos a al
cases. P ope ood handling should be
implemen ed in expo manu ac u ing zones and
heal h educa ion on common poisonous animals
should be s eng hened in u al a eas. Food
sa e y inspec ions should be implemen ed
egula ly h oughou he yea . App op ia e
su eillance sys ems e.g., no i ica ion/complain
sys ems and synd omic su eillance o FBD
should be es ablished.
Acknowledgemen s: We hank he Food Sa e y
Agencies o 19 Sou he n P o inces o Vie nam
which submi ed he ou b eak in es iga ion
epo s.
Funding: Uni e si y o Tampe e, School o
Heal h Sciences suppo ed conduc ing his
s udy.
Decla a ion o con lic ing in e es s: The
au ho s decla ed no con lic s o in e es wi h
espec o he au ho ship and/o au ho ship o
his a icle.
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