EPIDEMIOLOGICAL STUDY ON YERSINIOSIS IN PEDIATRIC ACUTE DIARRHEA

Assiut Vet. Med. J. Vol. 52 No. 111 October 2006

Dept. of Animal Hygiene and Zoonoses Fac. of Vet. Med., Assiut University.

EPIDEMIOLOGICAL STUDY ON YERSINIOSIS IN

PEDIATRIC ACUTE DIARRHEA

(With 5 Tables and 5 Figures)

By AMAL S.M. SAYED (Received at 19/9/2006)

دراسة وبائية على اليارسينيوسيس في حالات الإسهال الحاد في الأطفال

أمل سيد محمد سيد تزايدت في الآونة الأخيرة حالات الإصابة بالنزلات المعوية الناتجة عن الإصابة بميکروب الدارسينيا انتيروکولیتیکا والدارسينيا سيدوتیوبرکلوسيس، ولذلک أجريت هذه الدراسة لتحديد نسبة الإصابة بميکروب اليارسينيا أنتيروکولیتیکا واليارسينيا سيدو تیوبرکیلوسيس لدي مجموعة من الأطفال تعاني من حالات الإسهال المدمم والإسهال الغير المدمم. لذلک فقد تم جمع عدد ۱۰۰ عينة عشوائية من براز الأطفال بواقع ۱۰۰ عينة من حالات الإسهال الغير المدمم، ۵۰ عينة من حالات الإسهال المدمم من وحدة الجهاز الهضمي في مستشفى الأطفال بجامعة أسيوط في الفترة من يناير إلى ديسمبر ۲۰۰۵. وقد تم عزل میکروب اليارسينيا انتيروکولیتیکا واليارسينيا سيدوتیوبرکیلوسیس بنسبة

۱۷,۳۳

% و ۱۳٫۳۳ % من براز الأطفال على التوالي. وقد ارتفعت نسبة الإصابة بين الأطفال في الريف (5۲٫۹%) عن الأطفال في المدينة ( ۱۱,۲۰ %). وقد أثبتت الدراسة أن غالبية المرضى من الأطفال کانت

تتراوح أعمارهم بين (4 ۲- ۰ اشهر) وکانت نسبة الإصابة (۸۷,۰

%) بينما کانت نسبة الإصابة (۱۸٫۳۳ %) بين الأطفال التي تتراوح أعمارهم بين (۷-۲۶ شهر). کما أظهرت النتائج أن الإصابة کانت أعلى بين الإناث (۳۳٫۳۳%) عن الذکور (

۲۹,۵۲

%). وقد تمت

دراسة نسبة الإصابة على مدار العام. وقد تمت مناقشة الأهمية الصحية والوبائية ومصادر التلوث المختلفة لميکروب اليارسينيا انتيروکولیتیکا واليارسينيا سينوتیوبرکیلوسیس، هذا بالإضافة إلى مناقشة التوصيات لکيفية الحد من انتشار هذا الميکروب وکيفية الوقاية منه.

SUMMARY

Yersiniosis is considered one of the most important bacterial foodborne infections as their incidence among humans had increased dramatically. A total of one hundred and fifty random samples were collected from children with acute diarrhea. 50 of them had blood in stools and 100 had

the

from

collected stools. Samples were their

in no blood gastroenterology unit of Assiut University Children Hospital during the period from January to December 2005. The present study was designed

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to estimate the incidence of Yersinia enterocolitica and Yersinia pseudotuberculosis among diarrheal children with and without blood in stools. Moreover, demographic and clinical characteristics of the Yersinia infected children were investigated. Yersinia enterocolitica and Yersinia pseudotuberculosis could be detected in 17.33% and 13.33 % of the examined children, respectively.Ecological distribution of the examined children revealed that the rate of infection was higher in rural areas (52.9%) than in urban areas (11.25%). The majority of cases in the present study were in the age group of (> 24-60months ) with a rate of (87.5%), followed by those in age group of (7-24 months) with a rate of 18.33%. It has been determined that incidence of Yersinia species was higher among females (33.33%) than males (29.52%). Seasonal incidence of the infection by Yersinia enterocolitica and Yersinia pseudotuberculosis was studied. Public health hazard and preventive measures to control infection were discussed.

Key words: Yersinia enterocolitica, Yersinia pseudotuberculosis,

pediatric acute diarrhea

INTRODUCTION Foodborne diseases caused by microbial pathogens remains a significant international public health problem in the 21st century, so that governments are intensifying their efforts to improve food safety (WHO, 2000). Yersiniosis is considered one of the most important bacterial foodborne infections as their incidence among humans had increased dramatically.

Yersiniosis is an infection associated with either Yersinia enterocolitica or Yersinia pseudotuberculosis. Epidemiological studies has been implicated animals including pigs, rodents, rabbits, sheep, goats, cattle, horses, dogs and cats as reservoirs of pathogenic Yersinia speices (Butler, 1998). Transmission of infection to human occurs by ingestion of contaminated food or water and less commonly by direct contact with infected animals and patients (Butler, 1998). It was been reported that milk, dairy products, powdered milk, cheese, meat and vegetables are considered as the major sources of infection in different reported outbreaks (Toora et al., 1994).

Yersinia enterocolitica infection can assume many different forms depending on the strain and dose of the organism as well as the age and physical condition of the person infected (Gray, 1995). Several outbreaks of Yersinia enterocolitica food poisoning were reported by different authors (Barret, 1989; Greenwood and Hooper, 1990 & Ackers,

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King, M.E., Kirakofe, S.D.; Stevenson, J.S. and Schalles, R.R. (1982):

Effect of stage of the estrous cycle on interval to estrus after

PGF2a in beef cattle. Theriogenology. 18: 191. Larson, L.L. and Ball, P.J.H. (1992): Regulation of estrous cycles in

dairy cattle: a review. Theriogenology. 38:255. Lucy, M.C., Stevenson, J.S. and Call. E.P (1986): Controlling first

service and calving interval by prostaglandin F2a gonadotrophin-releasing hormone and timed insemination. J.

Dairy Sci. 69: 2186. Mee, O.M.: Stevenson, J.S.: Alexander. B.M. and Sasser. R.G. (1993):

Administration of GnRH at estrus influences pregnancy rates, serum concentration of LH, FSH, estradiol-17B, pregnancy, specific protein b, and progesterone, proportion of luteal cell types, and in vitro production of progesterone in dairy cows. J.

Anim. Sci.71,185-198. Momcilovic, D.; Archbald, L.F.; Walters, A.; Tran, T.; Kelbert, D. and

Risco, C. (1998): Reproductive performance of lactating dairy cows treated with gonadotrophin-releasing hormone (GnRH) and\or prostaglandin F2a (PGF2a) for synchronization of estrus

and ovulation. Theriogenology, 50: 1131-1139. Momont, H.W. and Seguin, B.E. (1983): Treatment of unobserved estrus

in lactating dairy cows with prostaglandin F2a products. Page 28 in The Compendium on Continuing Education for the Practicing Veterinarian on Reproductive Management in Food

Animals. Univ. Minnesota, St. Paul. Nebel, R.L. and Jobst, S.M. (1998): Evaluation of systematic breeding

program for lactating dairy cows: a review. J. Dairy Sci. 81:

1169- 1174. Paul, V. and Prakash, B.S. (2005): Efficacy of the Ovsynch protocol for

synchronization of ovulation and fixed-time artificial insemination in Murrah buffaloes (Bubalus bubalis).

Theriogenology, 64: 1049-1060. Pietro S.B.; Ed Hoffman M.; Valquiria H.B.; Renato C.B. and Rodolfo

C.B. (2003): Evaluation of synchronization of ovulation for fixed timed insemination in buffalo (Bubalus bubalis). Brazilin J. Vet. Res. Anim. Sci. 40: 6: Sao Paulo. Aproved para

puplication: 17/09/2003. Pursley, J.R., Kosorok, MR. and Wiltbank, M.C. (1997a): Reproductive

management of lactating dairy cows using synchronization of ovulation. J. Dairy Sci .80: 301 -306.

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Pursley, J.R.; Mee, M.O. and Wiltbank, M.C. (1995): Synchronization of

ovulation in dairy cows using PGFza and GnRH.

Theriogenology, 44: 915 - 923. Pursley, J.R.; Wiltbank, M.C.; Stevenson, J.S.; Ottobre, J.S.; Garverick,

H.A. and Anderson, L.L. (1997b): Pregnancy rates per artificial insemination for cows and heifers inseminated at a synchronized ovulation or synchronized estrus. J. Dairy Sci.

80: 295-300. Roy, G.L. and Twargiramungu, H.A. Fixed -time AI program using the

GnRH- PGF2a -GnRH method for beef females. J. Anim. Sci.

74 (suppl.): 222 (Abstr). Silcox, RW., Powell, K.L. and Kiser, T.E. (1993): Ability of dominant

follicles (DF) to respond to exogenous GnRH administration is depended on their stage of development. J. Anim. Sci. 71

(Suppl 1): 513 Abstr. Snedecor, G.W. and Cochran, W.G. (1980): Statistical methods 7th ed.

J.B.H publishing Comp. Oxford. Stevenson, J.S.; Kobayashi, Y. and Thompson, K.E. (1999):

Reproductive performance of dairy cows in various programmed breeding systems including Ovsynch and combination of gonadotrophin-releasing hormone and

prostaglandin F2a. J. Dairy Sci. 82: 506-515. Stevenson, J.S.; Lucy, M.C. and Call, E.P. (1987): Failure of timed

inseminations and associated luteal function in dairy cattle after

two injections of prostaglandin F2a. Theriogenology. 28: 937. Stevenson, J.S.; Mee, M.O. and Stewart, R.E. (1989): Conception rates

and calving intervals after prostaglandin F2a or rebreeding

progesterone in dairy cows. J. Dairy Sci. 72: 208. Stevenson, J.S.; Smith, J.F. and Hawkins, D.E. (2000): Reproductive

outcomes of dairy heifers treated with combination of prostaglandin F20, norgestomet, and gonadotrophin-releasing hormone. J. Dairy Sci. 83: 1-8.

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1995). The most frequent manifestation is gastroenteritis, which primarily affects children especially infants are considered highly susceptible to infection in the first year of life. Exudative pharyngitis and septicemia may also occur. Although Y. enterocolitica causes a syndrome which mimics appendicitis oftenly in older children and young adults (Naktin and Beaves, 1999 & Lamps et al., 2001). Y. enterocolitica is implicated as a major bacterial cause of appendicitis (Shorter et al., 1998; Lamps et al., 2001; Sakellaris et al., 2004 and Sayed and Hassan, 2005). Serious cases of infection may occur with rectal bleeding and perforation of the ileum.

It is interesting to note that, secondary immunological mediated complications may develop after complete recovery of infection such as arthritis, erythema nodosum and to a lesser extent Reiter's syndrome, glomerulonephritis and myocarditis, (Bottone, 1997; and Strobel et al., 2000).

Yersinia pseudotuberculosis mainly affects children, adolescents and young adults (Butler, 1998). The most clinical forms are mesenteric adenitis, pseudoappendicitis, fever, vomiting and diarrhea in 20% of the infected patients (Acha and Szyfer, 1991). Moreover, Y.pseudotuberculosis has been isolated from cases of appendicitis (Puylaert et al., 1989 & Sayed and Hassan, 2005).

The present investigation was designed to estimate the prevalence of Yersinia enterocolitica and Yersinia pseudotuberculosis among children with diarrhea and to study the possible risk factors in acquiring the infection.

MATERIALS and METHODS Sample Collection:

One hundred and fifty random stool samples were collected from children with acute diarrhea (100 had no blood in stools and 50 had blood in stools). Samples were collected from gastroenterology unit of Assiut University Children Hospital during the period from January to December 2005. Precoded questionnaires were completed at the time of recruitment to record demographic details and clinical history. Isolation and identification of Yersinia species: Cold enrichment technique: swabs of stool specimens were enriched in phosphate buffer saline pH 7.6 (PBS) supplemented with 2% peptone and incubated at 4°C for 14 days (Varnam and Evans, 1991). Isolation on Yersinia selective agar:

Loopfuls from the enriched broth were streaked onto Yersinia selective agar plates supplemented with Cefsulodin-Irgasan-Novobiocin

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(CIN) and incubated at 28°C for 24 hours. Dark red, bull eye-like colonies were screened by biochemical reactions according to the technique described by Varnam and Evans (1991). Determination of Virulence markers: Autoagglutination and congo red uptake were used to identify virulent strains of Y. enterocolitica (Varnam and Evans, 1991).

RESULTS

Table 1: Prevalence of Yersinia species among the examined children

Type of diarrhea No.of

Yersinia species

samples Y. enterocolitica Ypseudotuberculosis Non bloody diarrhea

*16 (16 %)

7 (7%) Bloody diarrhea

50

*10 (20%)

13 (26 %) Total

150

26 (17.33%)

20 (13.33%) * All of the isolated Yersinia enterocolitica strains were virulent

100

Table 2: Ecological distribution of Yersinia infection among the

examined children

Yersinia species Residence No.of Y. enterocolitica Y.pseudotuberculosis Total

samples Rural

20 (28.6%)

17 (24.3%) 37 (52.9%) Urban

80

6 (7.5%)

3 (3.75%) 9 (11.25 %)

70

Percent

PR

Y. enterocolitica

Y. pseudotuberculosis

Fig. 1: Prevalence of Yersinia species

among the examined children

Fig. 2: Ecological distribution of Yersinia

infection in the examined children

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Table 3: Age-wise prevalence of Yersinia infection among the examined

children Age-wise No.of

Yersinia species (months) samples Y. enterocolitica y pseudotuberculosis Total

50

7-24 > 24-60

1

60

6 (10%) 20 (50%)

5(8.33 %) 15 (37.5%)

11( 18.33%) 35( 87.5%)

40

Table 4: Occurrence of Yersinia infection in male and female children

Yersinia species Y. enterocolitica Y.pseudotuberculosis

Sex

Total

No.of samples

105

Male Female

18 (17.14%)

8 (17.8%

13 (12.38%) 7(15.56%)

31 (29.52 %) 15 (33.33%)

45

DY.eniero

BY. ಸರಳtubeಂಬಂti

O Male

Female

Pancen

lli

Yanmeca

-restauர்க

ள்

Fig. 3: Age-wise prevalence of Yersinia infection

among the examined children

Fig. 4: Occurrence of Yersinia infection

in male and female children

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Table 5: Incidence of Yersinia species in relation to the months of the

year Month No.of Y. enterocolitica Y. pseudotuberculosis

samples

No. %

No.

% January

10 February

10 March

10 April

25

8.33 May

26.67

13.33 June

20

26.67 July

15

26.67

33.33 August

12

33.33

33.33 September

15

26.67

13.33 October

15

26.67

13.33 November December

10 - -

12

15 15

Percent

January

February

March

April

May

July

August

September

October

November

December

June

Months

Fig. 5: Incidence of Yersinia species in relation to the months of the year

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DISCUSSION

Foodborne bacterial gastrointestinal infections are important causes of morbidity and mortality worldwide, and despite successful control programs in some developed countries, these infections continue to have a major impact on public health and economy (Varnam and Evans, 1991). Yersinia species are one of the most reported pathogens incriminated in gastrointestinal illness (Kapperud, 1991).

Results of this study revealed that the prevalence of Yersinia enterocolitica among the examined children was 17.33% however, the prevalence of Yersinia pseudotuberculosis was 13.33% in the examined samples (Table and Figure 1).

Clinical and laboratory investigation revealed that Y enterocolitica was isolated from 16% and 20% of the examined children with nonbloody diarrhea and bloody diarrhea, respectively (Table and Figure 1).

It has been confirmed that all of the isolated strains of Y.enterocolitica were virulent (Table 1). It has been noted that the virulence of Y. enterocolitica results from a complex interplay between a series of temperature-controlled plasmid borne and chromosomal genes (Robins-Browne, 1997). Moreover, Y. pseudotuberculosis was isolated from 7% and 26% of the examined children with nonbloody diarrhea and bloody diarrhea, respectively (Table and Figure 1). Several investigators reported variable prevalence rates in different geographical areas. Higher prevalence rates were detected with rates of 53% and 77.6% reported by Greenwood and Hooper, (1986) and Metchock et al. (1991), respectively. However, lower prevalence rates were detected with rates of 0.9%, 0.64%, 2%, 2.7% ,0.54% and 7.1% reported by Ogunsanya et al. (1994 ); Essers et al. (2000); Kafetzis et al. (2001); Soltan-Dallal and Moezardalan, (2004); Klein et al. (2006) and Koehler et al. (2006), respectively.

The higher prevalence rate detected in this study may be due to the high prevalence rate of Yersinia species among animals in the studied areas as reported previously by El-Prince and Sayed, (2002).

Ecological distribution of the infected children in the present study (Table and Figure 2) revealed that the prevalence of Yersinia species were higher in rural areas (52.9%) than in urban areas (11.25%). The high prevalence rate reported in rural areas may be attributed to the high risk of infection from animal as well as high contamination rates of food and water in these area.

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Data illustrated in (Table and Figure 3) reveals that the majority of infected children were in the age group (>24-60 months) with a rate of 87.5% followed by children in the age group (7-24 months) with a rate of 18.33%, however Yersinia species were not isolated from children with age group younger than (7 months). It has been reported that the peak age related incidence of Yersinia species was in young children especially younger than 5 years Metchock et al., 1991 and Olesen et al., 2005).

Results in (Table and Figure 4) declared that Yersinia species were slightly higher among females with a percent of 33.33% than males with a rate of 29.52%. Y. enterocolitica was isolated from male and female children with a rate of 17.14% and 17.8%, respectively while, Y. pseudotuberculosis were detected in 12.38% and 15.56% of the examined males and females children, respectively. It seems from the obtained results that gender does not play a major role in acquiring infection whereas, the prevalence rate in both sexes was nearly the same.

Studying the seasonal distribution of Yersinia infection as illustrated in (Table and Figure 5) revealed that Yersinia infection were most common in warm months with incidence rate varied from 20% - 26.67% in case of Y. enterocolitica. However, the incidence of Y. pseudotuberculosis varied from 8.33% to 33.33%. Results obtained in this study agrees with that reported by Hayashidani et al., (1995). However, several investigators had reported that Yersinia infection occurs throughout the year [Fukushima et al. (1987); Prentice et al. (1991)] and Wormser et al. (1996).

In conclusion, results obtained in this study reflect the public health hazard of Y. enterocolitica and Y. pseudotuberculosis which obligate applying control measures to reduce the risk of human infection by collaboration of governments, food industry and consumers.

AKNOWLEDGEMENTS

Sincere thanks to staff members at gastroenterology unit of Assiut University Children Hospital for their great help to obtain the samples.

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enterocolitica: clinical observation, p. 83-94. In E.J. Bottone (ed), Yersinia enterocolitica, CRC press, Inc., Boca Raton, Fla.

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طفيليات: بعض الدراسات الوبائية والطفيلية على مدى انتشار طفيليات الجهاز الهضمي في الابل وحيدة السنم بمنطقة شلاتين ، محافظة البحر الأحمر ، مصر ومحاولة علاجها. عثمان محمد مهران

أمراض دواجن: . بعض الدراسات عن عدوى الميکروب المکور العنقودي في الدجاج بمحافظة أسيوط هبة الله عبد الحليم محمد،منال حسن ثابت،نيفين عبد الغي التسر.

دراسات اشعاعية على کسور والتهاب العظام السمسانية العلوية في الحمير. نبيل أحمد معک،أمل جل أبو العلا،بهاء اللبن على عبد اللاه حسين.

التطبيق الحقلی لبعض تقنيات تخفيف الشد التقويمية لاعادة بناء الجلد. أمل جلال أبو العلاء إعادة هيکلة الجهاز البولي بعد قطع جزئي للمثانة. لک. عماره،ح. عقاد،أ. بوکر،م. ميليزي.

ولادة وتناسليات: علاج خمول المبايض بعد الولادة في الجاموس وتقييمه الاقتصادي. کمال کمال متولی علاقة عدم توازن الأکسدة ومضادات الأکسدة الخصوبة في فترة ما بعد الولادة في الأبقار. جابر أحمد مجاهد،صلاح القدور،رشاد عثمان،فوزي الزهیری. تقييم معدل الحمل في الجاموس المصري في فترة ما بعد الولادة باستخدام الحقن المزدوج للبروستاجلاندين أو نظام تزامن التبويض. فوزي الزهیری،عبد الخالق نصرة،صلاح القدوره

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أمراض مشترکة: دراسة وبائية على اليارسینیوسيس أمل سعيد محمد مد.

في حالات الإسهال الحاد في الأطفال.

لجنة الطباعة: قام بإعداد وکتابة وتصوير وطبع هذا العدد کل من:

السيدة/ کوکب أحمد على مسک السيد محمد محمود حسین عاشور السيده/ منى عبده عبدالحافظ السيده / منال ابراهيم ناجي العقاد