7/23/2019 Yersinia enterocolitica.pdf

http://slidepdf.com/reader/full/yersinia-enterocoliticapdf 1/6

Yersinia enterocolitica   infection among children aged less than 12 years:a case–control study

Iyad A. El Qouqa a, Mahmoud A. El Jarou b, Ahmed S. Abu Samaha c, Ahmed S. Al Afifi d,Abdel Moati Kh. Al Jarousha e,*a Medical Technology Department, Hejazi Medical Center, Medical Services, Gaza, Palestineb Medical Microbiology Department, Al-Shifa Hospital, Ministry of Health, Gaza, Palestinec Biology Department, Al Aqsa University, Gaza, Palestined Medical Microbiology Department, Al-Nasser Pediatric Hospital, Ministry of Health, Gaza, Palestinee Laboratory Medicine Department, Al Azhar University, Gaza, Palestine

1. Introduction

Yersiniosis due to infection with the bacterium   Yersinia

enterocolitica   is a zoonotic gastrointestinal disease in humans.

The species   Y. enterocolitica   has been isolated from a variety of domestic and wild animals, including pigs, cattle, sheep, goats,

dogs, cats, wild boars, and small rodents.1 The transmission of 

infection to humans is thought to occur primarily through the

ingestion of food, in particular raw or undercooked pork and pork

products.1,2 However, other risk factors, such as the consumption

of contaminateddrinking water and contact withpet animals, have

also been reported.3–5 Y. enterocolitica   infections are usually

sporadic, although outbreaks do occur.6–8

Y. enterocolitica  is responsible for a wide spectrum of clinical

manifestations, including acute gastroenteritis,9 mesenteric

lymphadenitis, and endocarditis,10 and predominantly affectsyoung children.

There are numerous serotypes of Y. enterocolitica. Eleven of these

serotypes have frequently been associated with infections in

humans, with serogroups O:3, O:8, O:9 and O:5.27 predominat-

ing.1,11 However, only a few case–control and epidemiological

studies have beenreportedworldwide investigating symptoms, risk

factors, and potential sources of  Y. enterocolitica infections.3–5,12

Very little information is available in the literature regarding this

organism in Palestine. This study was undertaken to identify risk

factors for infection with Y. enterocolitica and to identify presenting

signs and symptoms specifically associated with developing infec-

International Journal of Infectious Diseases 15 (2011) e48–e53

A R T I C L E I N F O

 Article history:

Received 18 March 2010

Received in revised form 1 August 2010

Accepted 1 September 2010

Corresponding Editor:  William Cameron,

Ottawa, Canada

Keywords:

Yersinia enterocolitica

Risk factor

Diarrhea

Serotype

S U M M A R Y  

Objectives:   A case–control study was conducted to identify risk factors, signs, and symptoms that may be

associated with, Yersinia enterocolitica  among children aged less than 12 years.

Methods:   From February 2006 to January 2007, stool samples from diarrhea cases with a clinical

diagnosis of gastroenteritis and those of matched uninfected and infected controls, were examined for

the presence of  Y. enterocolitica.

Results:   Sixteen sporadic cases of Y. enterocolitica were identified. Of these, eight were detectedin winter

(December through February),while theremainingcases occurred in the spring,summer, andautumn. Of 

the 16 isolates, 10 belonged to serotype O:3, five belonged to serotype O:9, and one to serotype O:8.

Compared to matched uninfected controls, multivariate analysis revealed that malnutrition (adjusted

odds ratio (aOR) 6.23; p  = 0.002) and water supply (aOR 3.05; p = 0.049) were independently associated

with infection. Compared to infected controls, multivariate analysis showed malnutrition (aOR 3.53;

 p = 0.027) to be an independent risk factor for the acquisition of yersiniosis. The antibiotic susceptibility

profile showed that Y. enterocolitica was generally susceptible to meropenem (100%), ceftriaxone (94%),and ciprofloxacin (94%), followed by ceftazidime (88%) and amikacin (81%). Almost all  Y. enterocolitica

was resistant to ampicillin.

Conclusions:   This study demonstrated that   Y. enterocolitica   occurs sporadically in children, with a

predominance of serotypes O:3 and O:9. Furthermore malnutrition was identified as the main risk factor

for yersiniosis.

 2010 International Society for Infectious Diseases. Published by Elsevier Ltd. All rights reserved.

* Corresponding author. Laboratory Medicine Department, Al Azhar University,

Gaza, P.O. Box 1277, Gaza Strip, Palestine. Tel.: +970(2) 8 2867510.

E-mail address:  Amoati2007@yahoo.com (A.M.K. Al Jarousha).

Contents lists available at  ScienceDirect

International Journal of Infectious Diseases

j o u r n a l h o m e p a g e : w w w . e l s e v i e r . c o m / l o c a t e / i j i d

1201-9712/$36.00 – see front matter    2010 International Society for Infectious Diseases. Published by Elsevier Ltd. All rights reserved.

doi:10.1016/j.ijid.2010.09.010

7/23/2019 Yersinia enterocolitica.pdf

http://slidepdf.com/reader/full/yersinia-enterocoliticapdf 2/6

tion. We alsosought to determine theserotypes of Y. enterocolitica in

our community.

2. Materials and methods

 2.1. Clinical setting 

The study population comprised children aged less than 12

years whowere admittedto the pediatric departments of Al Dorra

Hospital (100 beds), Al Nasser Hospital (250 beds), and Shohada

Al Aqsa Hospital (80 beds) or who presented to the outpatient

clinics of these hospitals, seeking treatment for a gastroenteritis

infection. Six hundred stool samples were collected from these

children.

 2.2. Case selection

A matched case–control study was performed by comparing

each case of   Y. enterocolitica   to uninfected as well as infected

controls. The selection of cases was carried out according to

symptoms and signs of gastroenteritis. Suspected gastroenteritis

was defined as a case of acute diarrhea (three or more stools a

day).13 Outpatients were first examined by a physician and those

requiring further care were admitted to the hospital wards. Aphysician performed a physical examination and assessed the

patient’s level of dehydration according to clinical signs and

symptoms. The study was conducted with the official approval of 

the Helsinki Committee and the Palestinian Ministry of Health. In

compliance with the Helsinki Declaration, a consent form for

study participation was signed by parents of the children

following an explanation of the importance and objectives of 

the study.

 2.3. Case definition

Yersiniosis cases were those with acute diarrhea (three or more

stools a day), from which   Y. enterocolitica   were identified by

laboratory techniques.

 2.4. Controls

One hundredsixty-five non-diarrhea cases were selected from

the same age group; these children had a diagnosis other than

gastroenteritis, such as chest infection, skin, or orthopedic

problems, or were present at the clinic for vaccination. These

uninfected controls were non-diarrhea controls with no isolation

of   Y. enterocolitica   or other enteropathogens. In addition, 152

infected controls were enrolled in the study. These controls had

enteropathogens other then   Y. enterocolitica   isolated and were

included from the entire collection of diarrhea cases (N  = 600).

Controls were matched with cases of  Y. enterocolitica by age, sex,

and geography (same municipality). Furthermore, for eachdiarrhea and control case, a complete blood count was done in

the hematology laboratories; a low hemoglobin level (anemia)

was taken as an indicator of malnutrition status.14–16

For each   Y. enterocolitica  case, uninfected as well as infected

controls were investigated in an attempt to determine the specific

potential risk factors and presenting signs and symptoms

associated with the acquisition of  Y. enterocolitica.

 2.5. Demographic characteristics

The cases were initially seen by a physician. Demographic data

were subsequently collected through a well-prepared question-

naire: the guardians of the cases were questioned about house

crowdedness (crowdedness index, per room), maternal education,

family income, and other relevant information including disposal of 

sewage and water supply. The poverty rate is based on a monthly

household income of NIS 2000 (US$ 500) for households of two

adults and four children; low income is therefore defined as an

income between US$ 500 and US$ 750 was considered as moderate

and above US$ 750 considered as a high income. Moderate income

was included in the high incomecategory.17 For maternal education

level, low level of education was defined as primary or preparatory

school and high level of education was defined as secondary school

or university.

 2.6. Bacteriological studies

Stools were processed and analyzed for enteric bacteria on the

day of sample collection. Standard culture and identification

methods were used to identify enteric pathogens.18 In brief, stool

samples were inoculated on blood, Salmonella–Shigella, Mac-

Conkey, and cefsulodin–irgasan–novobiocin (CIN) agars, and

incubated at 37   8C for 24–48 h. For Salmonella enrichment, feces

were inoculated in selenite-F broth, incubated at 37   8C for 18 h,

and sub-cultured on Salmonella–Shigella agar. All plates were

examined, and the colonies suspected of corresponding to

enteropathogenic bacteria were identified by standard microbio-

logical methods and commercial antisera. The Campylobacterblood-free medium was used to isolate Campylobacter species;

incubationwas carriedout for48 h at 42   8C undermicroaerophilic

conditions. Stools were screened for enterohemorrhagic Escher-

ichia coliby platingon sorbitol-MacConkey agar. Allnon-sorbitol-

fermenting colonies were tested in an agglutinating assay with

O157 and H7 antisera.

 2.7. Isolation and identification of Y. enterocolitica

For isolation of Y. enterocolitica, the enrichment method

(phosphate-buffered saline, pH 7.0) with incubation at 4   8C was

used (cold enrichment). After inoculation, the enrichment medium

was incubated at 4   8C for 2 weeks, and then a loop of this was

inoculated in CIN medium with supplement19,20 and incubated fortwo further days at 25   8C. In addition, citrate, triple sugar iron (TSI)

agar and biochemical tests (API 20E, bioMerieux, France) were

used for the bacterial identification.

 2.8. Serotyping of Y. enterocolitica

The isolates of   Y. enterocolitica   were serotyped by slide

agglutination test using specific typing sera O:1, O:2, O:3, O:5,

O:8, and O:9 for  Y. enterocolitica  (Denka Seiken, Japan).

 2.9. Antimicrobial susceptibility testing 

The antibiotic susceptibilities of enteropathogen isolates were

determined by the disk diffusion method on Mueller–Hinton agarplates (SanofiDiagnostics, Sanofi Pasteur,France) using calibrated

inoculums of the isolates based on McFarland standard with the

following antibiotics: ampicillin (AM), amoxicillin (AC), chlor-

amphenicol (C), tetracycline (T), cephalexin (CN), trimethoprim–

sulfamethoxazole (SXT), ceftazidime (CAZ), ceftriaxone (CRO),

gentamicin (GN), amikacin (AK), cefuroxime (CXM), ciprofloxacin

(CIP), and meropenem (MER).21,22 The antibiotic disks used were

those produced by BD Diagnostic Systems (BD BBL Sensi-Disc;

Becton Dickinson, Sparks, MD, USA).

 2.10. Statistical analysis

Statistical analysis was carried out using SPSS version 15 for

Windows (SPSS Inc., Chicago, IL, USA). For continuous data, the

I.A. El Qouqa et al./ International Journal of Infectious Diseases 15 (2011) e48–e53   e49

7/23/2019 Yersinia enterocolitica.pdf

http://slidepdf.com/reader/full/yersinia-enterocoliticapdf 3/6

mean, standard deviation, and median with interquartile range

(IQR) were calculated. The Chi-square test was applied to assess

differences in proportions. Odds ratios (OR) and their respective

95% confidence intervals (CI) were calculated to assess the

magnitude of association between correlates. Variables found to

be significant by univariate analysis at   p-values of < 0.1 were

selected for inclusion in multivariate modeling. Backward

stepwise logistic regression was used to model the association

between   Y. enterocolitica   positivity and selected correlates

adjusted for confounding factors identified in univariate

analysis. A   p-value of    <0.05 was considered statistically

significant.

3. Results

This study was a case–control study focusing on the detection

of Y. enterocolitica. BetweenFebruary2006 andJanuary 2007, 24 Y.

enterocolitica   isolates were identified from diarrhea cases

(N  = 600). Of these, eight were excludedbecause another microbe

was reported from the same patient: Salmonella (n = 2),   E. coli

(n = 4), Shigella (n  = 1), and Campylobacter (n = 1). Thus, 16   Y.

enterocolitica isolates were subjected to serotyping analysis and

constituted the study cases. A higher rate of   Y. enterocolitica

infection was encountered in the winter months (n = 8; 50%);18.8% were encountered in the spring, 18.8% in the autumn, and

12.5% in the summer (Figure 1).

Diarrhea cases (N  = 600) had a mean (   standard deviation

(SD)) age of 5.01 3.06 years, with median of 4 (IQR 3–8) years.

The mean SD age of yersiniosis cases (n = 16) was 4.69 2.57

years, with a median of 4 (IQR 3–7 years). Originally there were

165 non-diarrhea controls, with a mean SD age of 5.01 3.15

years and median of 5 (IQR 2–8) years. However, 37 cases were

excluded from the analysis: 13 cases showed one or more

enteropathogens other than   Y. enterocolitica   and the rest had

missing data. Consequently the uninfected control group (free from

infection) constituted 128 cases. Of the original 152 infected

control cases (mean SD age of 5.76 2.59 years, median 5.0 (IQR 

4.0–7.75) years), eight were excluded from the analysis as theywere co-infected with   Y. enterocolitica. Thus there were 144

infected controls.

Measurement of hemoglobin levels revealed that 11 (68.8%)

yersiniosis cases were anemic, while 33 (25.8%) uninfected

controls were anemic. Similarly 56 (38.9%) infected controls

suffered from anemia.

 3.1. Serotypes

Of the 16 isolates, 10 belonged to serotype O:3, five belonged to

serotype O:9, andone to serotype O:8. Y. enterocolitica serotype O:3

infection was highest among those aged 1–6 years (43.7%),

followed by those aged 7–12 years (18.75%). Serotype O:9 was

more frequently found in those aged 1–6 years (25%) than in thoseaged 7–12 years (6.2%). Serotype O:8 was only found within the

age group 1–6 years (6.25%).

 3.2. Seasonal variation

Theresults of the present study showedseasonalvariation forY.

enterocolitica cases, with the highest frequency in the cool rainy

months of winter (50%), and the lowest frequency detected in the

summer months (12.5%) (Figure 1).

The distribution of   Y. enterocolitica  by age group and season,

with reference to the total cases, is shown in  Table 1.

 3.3. Demographic characteristics and risk factors

The univariate analysis of risk factors for infection in relation to

thematched uninfectedcontrols is shown in Table 2. Y. enterocolitica

cases were significantly more likely to suffer from malnutrition (OR 

6.08; p < 0.001) and have a non-chlorinated water supply (OR 2.93; p = 0.039). Several variables showed a tendency to be more

associated with developing an infection but did not reach statistical

significance. In multivariate logistic regression, the same factors

remained associated with infection: malnutrition (OR 6.23;

 p = 0.002) and non-chlorinated water supply (OR 3.05; p = 0.049).

Univariate analysis of the risk factors for infection in relation to

the matched infected controls is displayed in   Table 3. Both

malnutrition (OR 3.46;   p = 0.022) and non-chlorinated water

supply (OR 2.83;   p = 0.045) were found to be significantly

associated with yersiniosis. On multivariate logistic regression

analysis, malnutrition was the only independent risk factor (OR 

3.53; p  = 0.027) demonstrated to be associated with the develop-

ment of yersiniosis.

The clinical signs and symptoms accompanying yersiniosiscases were abdominal pain (56.3%), fever (25%), vomiting (12.5%),

and dehydration (6.3%).

[

Figure 1.  Seasonal distribution of  Yersinia enterocolitica  cases.

 Table 1

Distribution of  Yersinia enterocolitica  and total diarrhea cases by age and season

Season Age 1–6 yearsa Age 7–12 years

Total cases (N = 280) Yersinia (n = 12) Total cases (N = 320) Yersinia (n = 4)

Autumn 52 (18.6) 2 (16.7) 68 (21.3) 1 (25)

Winter 80 (28.6) 6 (50) 100 (31.3) 2 (50)

Spring 73 (26.1) 2 (16.7) 87 (27.2) 1 (25)

Summer 75 (26.8) 2 (16.7) 65 (20.3) 0 (0)

Results are n  (%).a

Children aged less than 1 year were included in this category.

I.A. El Qouqa et al./ International Journal of Infectious Diseases 15 (2011) e48–e53e50

7/23/2019 Yersinia enterocolitica.pdf

http://slidepdf.com/reader/full/yersinia-enterocoliticapdf 4/6

 3.4. Organism characteristics

In the current study, the pathogens other than  Y. enterocolitica

isolated among diarrhea cases were diarrheagenic  E. coli (50/144;

34.7%), Shigella spp (40/144; 27.8%), Salmonellaspp (24/144; 16.7%),

and Campylobacter spp  (30/144; 20.8%).

 3.5. Antibiotic susceptibility profile

The antibiotic susceptibility profile of the   Y. enterocolitica

isolates revealed that 100% were susceptible to meropenem, 94%to

ceftriaxone, 94% to ciprofloxacin, 88% to ceftazidime, 81% to

amikacin, 75% to cefuroxime, 69% to gentamicin, 63% to

 Table 2

Univariate analysis of risk factors associated with  Yersinia enterocolitica  vs. uninfected controls

Variable Cases (N = 16) Uninfected controls (N = 128) OR (95% CI)   p-Value

Malnutrition (Hb  <9 g/dl) 11 (68.8) 33 (25.8) 6.08 (1.97–18.78)   <0.001

Family income

Low 9 (56.3) 62 (48.4) 1.37 (0.48–3.90) 0.56

High 7 (43.8) 66 (51.6)

Mother’s education

Low 10 (62.5) 55 (43.0) 2.21 (0.76–6.45) 0.14High 6 (37.5) 73 (57.0)

Crowdedness

>3 12 (75) 91 (71.1) 1.22 (0.37–4.03) 0.74

1–2 4 (25) 37 (28.9)

Residence

Rural 11 (68.8) 60 (46.9) 2.49 (0.82–7.59) 0.099

Urban 5 (31.3) 68 (53.1)

Gender

Male 9 (56.3) 59 (46.1) 1.5 (0.53–4.28) 0.44

Female 7 (43.8) 69 (53.9)

Age group (years)

1–6 12 (75) 85 (66.4) 1.52 (0.46–4.99) 0.49

7–12 4 (25) 43 (33.6)

Water supplyChlorinated 7 (43.8) 89 (69.5)

Non-chlorinated 9 (56.3) 39 (30.5) 2.93 (1.02–8.44) 0.039

Sewage

Reticulated 6 (37.5) 77 (60.2)

Not reticulated 10 (62.5) 51 (39.8) 2.52 (0.86–7.35) 0.084

OR, odds ratio; CI, confidence interval; Hb, hemoglobin;  p  <   0.05 is statistically significant.

 Table 3Univariate analysis of risk factors associated with  Yersinia enterocolitica   vs. infected controls

Variables Cases (N = 16) Infected control (N = 144) OR (95% CI)   p-Value

Malnutrition (Hb  <9 g/dl) 11 (68.8) 56 (38.9) 3.46 (1.14–10.48) 0.022

Family income

Low 9 (56.3) 75 (52.1) 1.18 (0.42–3.35) 0.75

High 7 (43.8) 69 (47.9)

Mother education

Low 10 (62.5) 84 (58.3) 1.19 (0.41–3.45) 0.75

High 6 (37.5) 60 (41.7)

Crowdedness

>3 12 (75) 98 (68.1) 1.41 (0.43–4.6) 0.57

1–2 4 (25) 46 (31.9)

Residence

Rural 11 (68.8) 86 (59.7) 1.48 (0.49–4.49) 0.48Urban 5 (31.3) 58 (40.3)

Gender

Male 9 (56.3) 58 (40.3) 1.6 (0.74–3.49) 0.22

Female 7 (43.8) 86 (59.7)

Age group (years)

1–6 12 (75) 89 (61.8) 1.85 (0.57–6.04) 0.30

7–12 4 (25) 55 (38.2)

Water supply

Chlorinated 7 (43.8) 99 (68.8)

Non-chlorinated 9 (56.3) 45 (31.3) 2.83 (0.99–8.07) 0.045

Sewage

Reticulated 6 (37.5) 85 (59.0)

Not reticulated 10 (62.5) 59 (41.0) 2.40 (0.83–6.97) 0.099

OR, odds ratio; CI, confidence interval; Hb, hemoglobin;  p<

0.05 is statistically significant.

I.A. El Qouqa et al./ International Journal of Infectious Diseases 15 (2011) e48–e53   e51

7/23/2019 Yersinia enterocolitica.pdf

http://slidepdf.com/reader/full/yersinia-enterocoliticapdf 5/6

chloramphenicol, and 50% to tetracycline. Almost all strains were

resistant to ampicillin.

4. Discussion

For a long time   Y. enterocolitica   was considered a rare

microorganism, however during the last two decades it has been

isolated all over the world from animals, raw food materials, the

environment, water, and human beings.23 Data on Y. enterocolitica

isolated from humans in Palestine are limited, despite frequent

descriptions of human infections with Y. enterocolitica from Europe,

North America, Brazil, and some African countries. Our findings

show Y. enterocolitica  to be a significant pathogen associated with

diarrhea in this part of the world.

From the total of 600 diarrheal cases, 16 were infected with  Y.

enterocolitica, giving a prevalence rate of 2.7%. The distribution of 

cases was higher inthe age group 1–6 years (4.3%) than inthe age

group 7–12 years (1.3%). This is similar to other findings, which

indicate a prevalence rate of 1.4%   Y. enterocolitica   strains from

fecal samples of children aged from 1 to 12 years.24 However, our

findings are much lower compared with a similar study that

documented a prevalence rate of 32.8% among children with

diarrhea.25 The highest prevalence of  Y. enterocolitica  was seen

amongst children aged 1–6 years. Factors that may contribute tothe high prevalence rate in this age group include an increased

rate of exposure  to enteric pathogens as a result of fecal–oral

contamination,24 in addition to an immature and unchallenged

immune system,26 and the higher frequency of physician

consultation among parents of children in this age group.27

Seasonal differences in   Y. enterocolitica   isolation rates were

noted. A higher prevalence in winter (December, January, and

February) was recorded than in other seasons. This is in agreement

with other studies.28 These result could be explained by the fact

that these enteropathogens essentially prefer psychrophilic

conditions. In addition, the CIN selective medium and the cold

enrichment method used in this study probably enhanced the

isolation of  Y. enterocolitica, as documented in other studies.29,30

The serotypes identified in the current study were O:3, O:9, andO:8. These results are consistent with other studies f rom the

Mediterranean area, and other European countries,28,31 demon-

strating that O:3 and O:9 are the predominant strains.

It is well-known that swine are the primary source of 

pathogenic   Y. enterocolitica   strains throughout the world;

however this is not the case in our area, which is free from pig

farming. We believe that other sources of yersiniosis may be

involved in the transmission of infection, such a wild or domestic

dogs, sheep, cows, etc. Previous studies conducted in China and

elsewhere have shown that dogs belonging to farmers may be a

source of pathogenic infectious Y. enterocolitica strains.32 A recent

case–control study conducted in Sweden among children   <7

years of age identified contact with domestic animals, in

particular dogs and cats, as the source of infection, in additionto pork consumption.5

Statistical analyses were performed separately for children aged

1–6and 7–12years.Despite thehigherprevalence rate among those

aged1–6 years, there was nodifferencein infection rate betweenthe

two age groups. Demographic characteristics of the Yersinia-

infected cases showed that 56.3% belonged to households with a

low family income, 75% were living in houses with a crowdedness

index of over three persons per room, 68.8% lived in rural areas,

56.3% had a non-chlorinated water supply, and 62.5% households

were not connected to a reticulated sewage system. These values

indicate the low socio-economic status of the study population in

theGaza Strip,in whichpoverty is dominant (65%).17 Itisalsoofnote

that 62.5%of the patients’ mothers had a low levelof education; this

has a negative impact on child personal hygiene.

Logistic regression analysis matching with uninfected controls

revealed both malnutrition and a non-chlorinated water supply as

independent risk factors significantly associated with yersiniosis.

In the comparison with infected controls, multivariate analysis

showed malnutrition as the only independent risk factor for

contracting   Y. enterocolitica  infection. Although our study identi-

fied malnutrition (anemia) as a major risk factor by multivariate

logistic regression, some of the anemia may have been caused by

iron deficiency. Other causes of anemia are folate deficiency,

vitamin B complex deficiency, protein deficiency, and hematologi-

cal disorders, either acquired or congenital. Our study shows that

anemia is a predisposing factor for  Y. enterocolitica  infection.

The most commonly recorded symptoms in  Y. enterocolitica

cases were abdominal pain followed by fever, vomiting, and

dehydration. This agrees with the typical clinical picture of 

yersiniosis as recorded in various studies.33

The present study demonstrated a high susceptibility of 

isolated strains of Y. enterocolitica to most of the tested antibiotics;

meropenem, third-generation cephalosporins ceftriaxone and

ceftazidime, and the aminoglycoside amikacin, as well as

fluoroquinolone ciprofloxacin, were the most active antimicrobial

agents tested. However, almost all strains were resistant to

ampicillin. This is consistent with other studies.34,35

To theauthors’ knowledge, this is thefirst case–control study of Y. enterocolitica infection in children in the Gaza Strip. The present

study identified risk factors for sporadic yersiniosis caused by  Y.

enterocolitica. However, the limitations of the study reside in the

low number of yersiniosis cases in comparison to the controls,

which may have introduced a statistical bias. In addition, most of 

the patients were outpatients and there was difficulty in

performing follow-up.

In conclusion, Y. enterocolitica   is one of the causative agents

of childhood diarrhea in our area. More attention should be

given to the alleviation of malnutrition. Furthermore there

should be increased supervision of the water supply by the local

health departments, and these should be regularly investigated

and controlled. Further studies are needed to investigate more

risk factors and the main sources of   Yersinia enterocoliticapathogens.

 Acknowledgements

We acknowledge the support and assistance of all the

laboratory personnel at both Al Nasser and Al Dorra pediatric

hospitals, as well as Shohada El Aqsa Hospital for their cooperation

and assistance in the stool samplecollections. We are also thankful

for the pediatricians and nurses for their cooperation.

Conflict of interest:  No conflict of interest to declare.

References

1. Bottone EJ.   Yersinia enterocolitica: overview and epidemiologic correlates.Microbes Infect  1999;1:323–33.

2. Tauxe RV, Wauters G, Goossens V, Van Noyen R, Vandepitte J, Martin SM, et al.Yersinia enterocolitica   infections and pork: the missing link.   Lancet 1987;1:1129–32.

3. Ostroff SM, Kapperud G, Hutwagner LC, Nesbakken T, Bean NH, Lassen J, et al.Sources of sporadic  Yersinia enterocolitica   infections in Norway: a prospectivecase–control study.  Epidemiol Infect   1994;112:133–41.

4. Satterthwaite P, Pritchard K, Floyd D, Law B. A case–control study of  Yersiniaenterocolitica  infections in Auckland.  Austr N Z J Public Health  1999;23:482–5.

5. Boqvist S, Pettersson H, Svensson A , Andersson Y. Sources of sporadic Yersiniaenterocolitica infection in children in Sweden, 2004: a case–control study.Epidemiol Infect  2008;137:897–905.

6. Ackers ML, Schoenfeld S, Markman J, Smith MG, Nicholson MA, DeWitt W, et al.An outbreak of Yersinia enterocolitica O:8 infectionsassociatedwith pasteurizedmilk.  J Infect Dis  2000;181:1834–7.

7. Babic-Erceg A, Klismanic Z, Erceg M, Tandara D, Smoljanovic M. An outbreak of Yersinia enterocolitica   O:3 infections on an oil tanker.   Eur J Epidemiol

2003;18:1159–61.

I.A. El Qouqa et al./ International Journal of Infectious Diseases 15 (2011) e48–e53e52

7/23/2019 Yersinia enterocolitica.pdf

http://slidepdf.com/reader/full/yersinia-enterocoliticapdf 6/6

8. Grahek-Ogden D, Schimmer B, Cudjoe KS, Nygard K, Kapperud G. Outbreak of Yersinia enterocolitica  serogroup O:9 infection and processed pork, Norway.Emerg Infect Dis  2007;13:754–6.

9. Karachalios G, Bablekos G, Karachaliou G, Charalabopoulos AK, Charalabopou-los K. Infectious endocarditis due to   Yersinia enterocolitica.   Chemotherapy2002;48:158–9.

10. Ray SM, Ahuja SD, Blake PA, Farley MM, Samuel M, Fiorentino T, et al. Popula-tion-based surveillance for Yersinia enterocolitica   infections in Food Net sites,1996–1999: higher risk of disease in infants and minority populations.  ClinInfect Dis  2004;38:S181–9.

11. Wannet WJ, Reessink M, Brunings HA, Maas HM. Detection of pathogenic

Yersinia enterocolitica by a rapid and sensitive duplex PCR assay. J Clin Microbiol2001;39:4483–6.12. Rosner BM, Stark K, Werber D. Epidemiology of reported Yersinia enterocolitica

infections in Germany, 2001–2008. BMC Public Health  2010;10:337.13. Perry S, de la Luz Sanchez M, Hurst PK, Parsonnet J. Household transmission of 

gastroenteritis. Emerg Infect Dis  2005;11:1093–6.14. Mitrache C, Passweg JR, Libura J, Petrikkos L, Seiler WO, Gratwohl A, et al.

Anemia: an indicator for malnutrition in the elderly.   Ann Hematol2001;80:295–8.

15. Awasthi S, Das R, Verma T, Vir S. Anemia and undernutrition among preschoolchildren in Uttar Pradesh, India.   Indian Pediatr  2003;40:985–90.

16. Liu J, Raine A, Venables PH, Mednick SA. Malnutrition at age 3 years andexternalizing behavior problems at ages 8, 11, and 17 years.   Am J Psychiatry2004;161:2005–13.

17. United Nations Development Programme (UNDP). Inside Gaza—attitudes andperceptions of the Gaza Strip residents in the aftermath of the Israeli militaryoperations. UNDP Programme of Assistance to the Palestinian People; 2009.Available at:   http://www.papp.undp.org/en/focusareas/crisis/surveyerf.pdf (accessed July 27, 2010).

18. WorldHealth Organization, Diarrhoeal Disease Control Programme.Manual forlaboratoryinvestigationsof acute enteric infections. Geneva; WHO; 1987, p. 1–113.

19. World Health Organization, International Organization for Standardization.Microbiology—general guidance for the detection of presumptive pathogenicYersinia enterocolitica. ISO 10273. Geneva: WHO; 1994.

20. US Food andDrugAdministration, Centerfor Food Safetyand AppliedNutrition.Bacteriological analytical manual. Chapter 8: Yersinia enterocolitica and Yersinia

 pseudotuberculosis. FDA/CFSAN/BAM; 2001. Available at: http://www.fda.gov/Food/ScienceResearch/LaboratoryMethods/BacteriologicalAnalyticalManual-BAM/UCM072633  (accessed September 2010).

21. Isenberg HD. Essential procedures for clinical microbiology. Washington DC:ASM press; 1998.

22. World Health Organization. Guidelines on standard operating procedures formicrobiology, 2005. SEA/HLM/324. Geneva: World health Organization; 2005.

23. OkworiAE, Agada GO,Olabode AO,AginaSE, Okpe ES,OkopiJ. Theprevalenceof pathogenic Yersinia enterocolitica among diarrhea patients in Jos, Nigeria.  Afr J Biotechnol 2007;6:1031–4.

24. Onyemelukwe NF. Yersinia enterocolitica   as an aetiological agent of childhooddiarrhea in Enugu Nigeria.  Cent Afr J Med 1993;39:192–5.

25. Omoigberale AI, Abiodun PO. Prevalence of  Yersinia enterocolitica  among diar-rheal patients attending University of Benin Teaching Hospital Benin-City

Nigeria.  Sahel Med J  2002;445:182–5.26. Cohen MB. Etiology and mechanisms of acute infectious diarrhea in infants inthe United States.   J Pediatr  1991;118:S34–9.

27. Scallan E, Jones TF, Cronquist A, Thomas S, Frenzen P, Hoefer D, et al. Factorsassociated with seeking medical care and submitting a stool sample in esti-mating the burden of foodborne illness.  Foodborne Pathog Dis  2006;3:432–8.

28. Galanakis E, Perdikogianni C, Maraki S, Giannoussi E, Kalmanti M, Tselentis Y.Childhood Yersinia enterocolitica infection in Crete.  Eur J Clin Microbiol Infect Dis2006;25:65–6.

29. Wesley IV, Bhaduri S, Bush E. Prevalence of   Yersinia enterocolitica   in marketweight hogs in the United States.  J Food Prot  2008;71:1162–8.

30. Hussein HM, Fenwick SG, Lumsden JS. A rapid and sensitive method for thedetection of   Yersinia enterocolitica   strains from clinical samples.   Lett ApplMicrobiol 2001;33:445–9.

31. Hoogkamp-Korstanje JA, Stolk-Engelaar VM. Yersinia enterocolitica infection inchildren. Pediatr Infect Dis J  1995;14:771–5.

32. Wang X, Cui Z, Wang H, Tang L, Yang J, Gu L, et al. Pathogenic strains of  Yersiniaenterocolitica isolated from domestic dogs (Canis familiaris) belonging to farm-ers are of the same subtype as pathogenic Y. enterocolitica strains isolated from

humans and may be a source of human infection in Jiangsu Province, China.  J Clin Microbiol  2010;48:1604–10.

33. Huovinen E, Sihvonen LM, Virtanen MJ, Haukka K, Siitonen A, Kuusi M.Symptomsand sources of Yersinia enterocolitica-infection: a case–control study.BMC Infect Dis  2010;10:122.

34. Abdel-Haq NM, Papadopol R, Asmar BI, Brown WJ. Antibiotic susceptibilities of Yersinia enterocolitica   recovered from children over a 12-year period.   Int J 

 Antimicrob Agents  2006;27:449–52.35. Andualem B, Geyid A. Antimicrobial responses of  Yersinia enterocolitica isolates

in comparison to other commonly encountered bacteria that causes diarrhoea.East Afr Med J  2005;82:241–6.

I.A. El Qouqa et al./ International Journal of Infectious Diseases 15 (2011) e48–e53   e53