M. N. H. CHOWDHURY ET AL.

Campylobacter Gastroenteritis in Children in Riyadh, Saudi Arabia by M. N. H. Chowdhury,* MBBS, D Bact, MSc, PhD and Youssef A. Al-Eissa,** MBBS, FAAP, FRCP(C) Departments of * Microbiology and ** Paediatrics, King Khalid University Hospital, College of Medicine, King Saud University, PO Box 2925, Riyadh 11461, Saudi Arabia

Introduction Campylobacter species has been suspected of being a human intestinal pathogen in 1957 by King who called the organism a 'related vibrio'.1 Later it was called Campylobacter fetus subsp.jejuni.2 In spite of King's earlier report this condition was not recognized for a long time. Although in a few cases of gastroenteritis due to Campylobacter blood cultures were positive, stools were negative because appropriate culture media were not used and the gaseous environment was inappropriate. 3 " 5 However, the importance of C. jejuni/coli (CJC) as a major cause of gastroenteritis was appreciated after the introduction of selective faecal culture techniques by Butzler et al. in 1973 in Belgium.6 Since then several workers from different countries including Britain,7 Sweden,8 United States, 9 Belgium, 10 Central Africa,11 South Africa,12 Canada, 1 3 Saudi Arabia, 1 4 1 5 Bangladesh, 16 and India 17 have confirmed Butzler's findings. As far as we know, there is no comprehensive published data on the incidence of CJC gastroenteritis in children in Saudi Arabia. This paper reviews the CJC associated gastroenteritis in children in Riyadh with special reference to some of the clinical and epidemiological characteristics of this infection. Subjects and Methods A total of 7369 children having gastrointestinal symptoms (4130 males and 3239 females) presented to the out-patient clinics and emergency room at King Khalid University Hospital in Riyadh, Saudi Arabia during the 2-year period from January, 1989, to December, 1990. Stool specimens were collected from 158

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each patient for bacterial examination. Stool specimens from 1130 control children free from gastrointestinal symptoms were also examined during the period of the study. For isolation of CJC a modified Skirrow's selective medium which consisted of 10 per cent sheep blood agar (Brucella agar base) with polymixin B (2.5 i.u/ml), vancomycin (10 ^g/ml) and trimethoprim (5 /Jg/ml) was used. The plates were incubated at 42°C under microaerophilic condition for 48 hours. 14 A plate with the control strain was also included with each set of inoculated plates to ensure that conditions for the adequate recovery of Campylobacter samples were met. Suggestive Campylobacterlike colonies were Gram-stained employing 0.2 per cent carbolfuchsin as counterstain. All isolates having a curved or spiral morphology were further identified at species level by oxidase and catalase production, growth at 25°C, 37°C, and 42°C, nalidixic acid and cephalothin sensitivity, and hippurate hydrolysis. Sensitivity tests were carried out on all isolates by agar diffusion using disc technique on Muller Hinton agar. In addition, the stool specimens were also cultured for the presence of other enteric pathogens by conventional procedures. Clinical history and physical examination of all patients included in this study were documented in a standard proforma. Results Campylobacter species was isolated from 82 (1 per cent) of 7369 patients. These isolates included 70 C. jejuni, 11 C. coli, and one C. laridis. Mixed infections with Salmonella species occurred in 3 of the 82 patients. The overall isolation rate of other pathogenic bacteria from the 7369 patients was 4 per cent. Of the Journal of Tropical Pediatrics

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Summary Campylobacter jejunijcoli (CJC) was isolated from the stools of 82 (1 per cent) of 7369 children with gastrointestinal symptoms during a 2-year period. Among 1130 control children, CJ was isolated from the stool of one (0.09 per cent). The peak incidence of CJC associated gastroenteritis was in the winter. Seventy-six per cent of the patients were 4 years of age and younger with the highest incidence (56 per cent) in children 2 years old and younger. The most common presenting symptoms and signs were diarrhoea (95 per cent), anorexia (71 per cent), abdominal pain (70 per cent), high fever (57 per cent), and frank blood in stools (48 per cent). Infive(6 per cent) patients CJC isolates were resistant to erythromycin. In all patients CJC infection was self-limited and the majority of patients required only supportive therapy.

M. N. H. CHOWDHURY ET AL.

1130 controls, CJ was isolated from the stool of one child (0.09 per cent). Table 1 shows the age and sex

TABLE 1

Age and sex distribution of 82 patients with Campylobacter jejuni/coli gastroenteritis Age group (years) 0-2 >4-6 >6-8 >8

Females (n = 41)

No. of patients (%) (n = 82)

22 10 2 2 5

24 6 7 3 1

46 (56) 16 (20) 9(11) 5 (6) 6 (7)

distribution of all patients with CJC gastroenteritis. Ages ranged from 2 days to 14 years (mean + SD, 3 + 3.5). There were 41 males and 41 females. Most of the positive isolates (76 per cent) were from the age group 0-4 years; with the highest incidence in young children (0-2 years old, 56 per cent). The peak incidence for CJC associated gastroenteritis was from January to March. Table 2 summarizes the clinical features of these 82 cases. The most common symptoms and signs were diarrhoea, anorexia, cramping abdominal pain, and

TABLE 2

Clinical features of 82 patients with Campylobacter jejuni/coli gastroenteritis Symptom or sign Diarrhoea Anorexia Abdominal pain Fever Gross blood in stool Vomiting Malaise Dehydration Arthralgia Convulsion Lethargy

Males (n = 41)

Females (n = 41)

Total (%) (n = 82)

39 28 29

39 30 28

78 (95) 58(71) 57 (70)

25 21

22 18

47 (57) 39 (48)

18 10 6 3 0 0

13 12 6 2 4 3

31 (38) 22 (27) 12(15) 5 (6) 4 (5) 3 (4)

fever. Seventy-eight (95 per cent) of the 82 patients developed diarrhoea with variable frequency of loose stools from very few to over 20 per day. Duration of diarrhoea from onset to recovery ranged from 4 days to 21 days with an average of 8.1 days. Abdominal pain was periumbilical and cramping, and it antedated Journal of Tropical Pediatrics

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Discussion Campylobacter jejuni/coli is now recognized as a major bacterial intestinal pathogen all over the world. The recovery of CJC from the stool of 1 per cent of 7369 children with gastro-intestinal symptoms indicates that the incidence of this organism is much lower than published data in other countries, e.g. 35 per cent in South Africa,12 11 per cent in Rwanda, 1 ' 4 per cent in Canada, 18 and 5 percent in Belgium.6 Campylobacter jejuni was isolated from the stool of one child without gastrointestinal symptoms (0.09 per cent of controls). These results were similar to those found in control subjects in temperate climates; the rate being 0-1.3 per cent. 6 ' 18 However, the carrier rate has been found to be much higher in developing tropical countries, e.g. South Africa (16 per cent), Bangladesh (18 per cent), and India (27 per cent). 12 - 16 - 17 We isolated C. laridis from a child aged 5 years who had severe abdominal pain and fever, but no vomiting or diarrhoea. C. laridis, found principally in seagulls, has been implicated recently in enteritis in four 159

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>2-A

Males (n = 41)

other symptoms in the majority of patients. Fortyseven (57 per cent) of the 82 patients had fever ranging from 38.4 to 40.5°C and 15 per cent of them had temperature above 40°C. Fever lasted for 1-6 days with an average of 2.8 days. The presence of frank blood in stool occurred in about half and vomiting in about one-third of the patients. Twelve (15 per cent) patients had moderate to severe dehydration. Of the 43 patients who had a complete blood count 9 (21 per cent) had anaemia and 21 (49 per cent) had leucocytosis. Leucocytosis manifested as a marked predominance of polymorphonuclear cells with a shift to the left in 14 patients (67 per cent) and as lymphocytosis in the remainder. Blood cultures were performed for only 11 patients and all the cultures were negative. Five isolates (6 per cent) of CJC were resistant to erythromycin, but all isolates were sensitive to gentamicin. Seventeen (21 per cent) of the 82 patients were admitted, and the duration of hospitalization ranged from 2 to 9 days with an average of 4.5 days. These patients were hospitalized because of high fever with or without convulsion and/or severe dehydration. Most patients recovered spontaneously on conservative management. Seventy-three per cent of the patients (60/82) were not given antibiotics. Twentytwo patients, however, were treated with antibiotics. Erythromycin was given to only eight patients and inappropriate antimicrobial agents were administered to the remainder. In the latter cases antibiotics were administered before the culture results were available. Follow-up stool cultures were performed in 30 (37 per cent) of the 82 patients. In these cases, cultures for CJC were negative 4-8 weeks after cessation of diarrhoea irrespective of whether they were treated with antibiotics or not.

M. N. H. CHOWDHURY ET AL.

higher resistance (9-15 per cent) has been reportred from other countries.22"24

patients, severe crampy abdominal pain in one, and terminal bacteraemia in an immunocompromised host in one.' 9 The reported patient with crampy abdominal pain had neither vomiting nor diarrhoea as observed in our patient. Thesefindingsconfirm that C. laridis is a potential human pathogen that appears to be closely related to C. jejuni clinically, epidemiologically, and microbiologically. It may be mistaken for C. jejuni if the appropriate laboratory screening tests (e.g. nalidixic acid sensitivity and hippurate hydrolysis) are not conducted. Differentiating this organism from C. jejuni in clinical isolates is important because it offers an epidemiological marker useful in further defining the sources and reservoirs of this species. In the present study boys and girls were equally affected by the disease. However, other studies showed the predominance of infection in males, especially those under the age of 14 years. 81415 ' 20 Karmali et al.21 in a 3-year study of 296 Campylobacter isolated from paediatric patients, have reported that 60 per cent of the patients were < 5 years old, 20 per cent were 5-10 years old and the remainder were > 10 years old. These results are in agreement with ourfindingswhich indicated that CJC associated gastroenteritis was much more prevalent in young children in Riyadh; thus 87 per cent of our patients were < 6 years old and 56 per cent were < 2 years old. Our findings indicated that CJC associated gastroenteritis was more prevalent in the winter season. This was in sharp contrast to the situation in temperate climates where the infection was more common in summer.8-15-19'22 Karmali and Fleming,13 in a detailed description of CJC gastroenteritis in 37 Toronto children, found that a presumptive diagnosis could be made on the clinical presentation alone. They reported diarrhoea in 95 per cent, frank blood in stools in 92 per cent, fever in 86 per cent, abdominal pain in 60 per cent, and vomiting in 30 per cent. A notable feature of the study was that blood appeared in the stools characteristically 2-4 days after the onset of symptoms. Dehydration was not a feature of the infection in the report from Toronto. In contrast, although diarrhoea was present in 95 per cent of our patients, our results showed that fever and frank blood in stool were present in about 50 per cent of the patients. However, abdominal pain and vomiting were found more frequently in 70 and 38 per cent, of our patients, respectively. These findings are in agreement with those of Pai et al. from Montreal18 where abdominal pain and vomiting were found in 66.6 and 36.6 per cent of children, respectively. In addition, our patients had dehydration in 15 per cent, arthralgia in 6 per cent, and convulsion in 5 per cent. Resistance of CJC to erythromycin was encountered in five patients (6 per cent). This figure is higher than that reported by Walder8 from Sweden where resistance rate of 2.6 per cent was found among 435 consecutive isolates of CJC examined. However,

1. King EO. Human infections with Vibrio foetus and a closely related vibrio. J Infect Dis 1957; 101: 119-28. 2. Holt JG. The Shorter Bergey's Manual of Determinative Bacteriology, 8th edn. Baltimore: Williams and Wilkins, 1977. 3. Middelkamp JN, Wolf HA. Infection due to a 'related' Vibrio. J Pediat 1961; 59: 318-21. 4. Wheeler WE, Borchers J. Vibrionic enteritis in infants. Am J Dis Childh 1961; 101: 60-6. 5. Darrel JH, Farrell BC, Mulligan RA. Case of human vibriosis. Br Med J 1967; ii: 287-9. 6. Butzler JP, Dekeyser P, Detrain M, Dehaen F. Related vibrio in stools. J Pediatr 1973; 82: 493-5. 7. Skirrow MB. Campylobacter enteritis: a 'new* disease. Br Med J 1977; ii: 9-11. 8. Walder M. Epidemiology of Campylobacter enteritis. Scand J Infect Dis 1982; 14: 27-33. 9. Blaser MJ, Feldman RA, Wells JG. Epidemiology of endemic and epidemic campylobacter infections in the United States. In: Newell DG (ed.) Campylobacter: epidemiology, pathogenesis and biochemistry. Lancaster: MTP Press, 1982; 3^1. 10. Lauwers S, De Boeck M, Butzler JP. Campylobacter enteritis in Brussels. Lancet 1978; i: 604-5. 11. De Mol P, Bosmans E. Campylobacter enteritis in Central Africa. Lancet 1978; i: 604. 12. Bokkenheuser VD, et al. Detection of enteric campylobacteriosis in children. J Clin Microbiol 1979; 9: 227-32. 13. Karmali MA, Fleming PC. Campylobacter enteritis in children. J Pediat 1979; 94: 527-33. 14. Chowdhury MNH, Mahgoub ES. Gastroenteritis due to Campylobacter jejuni in Riyadh, Saudi Arabia. Trans Roy Soc Trop Med Hyg 1981; 75: 359-61. 15. Chowdhury MNH. Campylobacter jejuni enteritis; a review. Trop Geogr Med 1984; 36: 215-22. 16. Blaser MJ, Glass RI, Huq MI, Stoll B, Kibriya GM, Alim ARMA. Isolation of Campylobacter fetus subsp jejuni from Bangladeshi children. J Clin Microbiol. 1980; 12: 744-7. 17. Rajan DP, Mathan VI. Prevalence of Campylobacter fetus subsp jejuni in healthy populations in Southern India. J Clin Microbiol 1982; 15: 749-51. 18. Pai CH, Sorger S, Lackman L, Sinai RE, Marks MI. Campylobacter gastroenteritis in children. J Pediat 1979; 94: 589-91. 19. Tauxe RV, Patton CM, Edmonds P, Barrett TJ, Brenner DJ, Blake PA. Illness associated with Campylobacter laridis, a newly recognized Campylobacter species. J Clin Microbiol 1985; 21: 222-5. 20. Butzler JP, Skirrow MB. Campylobacter enteritis. Clin Gastroenterol 1979; 8: 737-65. 21. Karmali MA, Penner JL, Fleming PC, Williams A, Hennesy JN. The serotype and biotype distribution of clinical isolates of Campylobacter jejuni and Campylobacter coli over a three-year period. J Infect Dis 1983; 147: 243-6. 22. Blaser MJ, Reller LB. Campylobacter enteritis. N Engl J Med 1981; 305: 1444-52.

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References

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23. Hanslo D, Fryer T, Le Roux E. Campylobacter bacteraemia in children. In: Pearson AD, Skirrow MB (eds). Second international workshop on campylobacter infections. Abstracts; 1983: 11.

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Campylobacter gastroenteritis in children in Riyadh, Saudi Arabia.

Campylobacter jejuni/coli (CJC) was isolated from the stools of 82 (1 per cent) of 7369 children with gastrointestinal symptoms during a 2-year period...
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