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Changing prevalence and antibiotic susceptibility patterns of different shigella species in Tehran, Iran

Authors:
  • Ministry of Health and Medical Education, Health Reference Laboratory, Tehran, Iran.

Abstract

During the 3 years of study period (April 2002 to April 2005) 220 strains of shigella isolated from fecal samples of patients having acute diarrhea. Shigella sonnei with 157 (78.5%) isolates had the highest frequency of isolation. Resistance to Ampicillin and Trimethoprime/sulphamethoxazole was observed in 88.5% and 98% isolates respectively. 11.5% of isolates were resistant to nalidixic acid and 5.5% to ceftriaxone. Resistance to Chloramphenicol and Ciprofloxacin was 2.5% and 1% respectively.
Changing prevalence and antibiotic
susceptibility patterns of different
shigella species in Tehran, Iran
Mohammad RahbarDepartment of Microbiology, Reference Laboratories of IranTehran Iran
Mojgan DeldariDepartment of Microbiology, Milad HospitalTehran Iran
Masoud HajiaDepartment of Microbiology, Reference Laboratories of IranTehran Iran
Citation: M. Rahbar, M. Deldari, M. Hajia: Changing prevalence and antibiotic susceptibility patterns of different shigella species in
Tehran, Iran. The Internet Journal of Microbiology. 2007 Volume 3 Number 2. DOI: 10.5580/1761
Abstract
During the 3 years of study period (April 2002 to April 2005) 220 strains of shigella isolated from fecal samples of patients having acute
diarrhea. Shigella sonnei with 157 (78.5%) isolates had the highest frequency of isolation. Resistance to Ampicillin and
Trimethoprime/sulphamethoxazole was observed in 88.5% and 98% isolates respectively. 11.5% of isolates were resistant to nalidixic acid
and 5.5% to ceftriaxone. Resistance to Chloramphenicol and Ciprofloxacin was 2.5% and 1% respectively.
Introduction
Shigelosis is an acute gastroenteritis caused by Shigella specis, including Shigella dysenteriae, Shigella flexneri,Shigella boydii and Shigella
sonnei. It is one of the most common causes of morbidity and mortality in children with diarrhea in developing countries. Worldwide,
approximately 165 million cases of shigellosis occurs and 1,100,000 death are caused by the disease per year, which two-third of the
patients are children under 5 years of age .Epidemic usually occur in area with crowding and poor sanitary conditions ,where transmission
from person to person common, or when food or water are contaminated by organism (
1
,
2
). Emergence of multiple drug resistance to cost
effective antibiotics against shigella is a matter of concern for the health authorities in developing countries.(
3
) Outbreak of shigellosis have
been reported from different parts of world. Two studies from Bangladesh showed an increasing frequency of shigella strains with multiple
resistance to ampicillin, Trmethoprime sulfamethoxazole (TMP-SMZ) and nalidixic acid .outbreaks of shigellosis caused by strains that
were resistant to ampicillin and TMP-SMZ ,or both drugs have been reported in other countries in Asia ,Africa central America and Europe.
. However, reports regarding various serogroups of shigella. In our country there are only a few documented studies regarding the
prevalence and susceptibility pattern of shigeloosis. The present study was therefore undertaken-(i) to study the incidence and serogroup
prevalence of shigella isolated from cases of dysentery during threes year period (ii) to determine drug resistance pattern and (iii) to compare
the results of present study with that of previous years regard that serogroup and antimicrobial sensitivity of shigella spp isolated.
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Material and Methods
All patients admitted to the Milad hospital in Tehran during 3 years from 2003 to 2005 with history of diarrhea of less than 7 days duration
were included in this study. A total 4351 patients were admitted. Individual case records of these patients were scrutinized. A special
Performa was designed to collect information regarding epidemiological variables such as age, sex, date of admission;other information
such as the result of faecal cultures were also included. Incomplete records were excluded. for enteric pathogens. Samples of faeces were
collected in sterile wide mouth containers and rectal swabs were transported in Cary- Blair transport medium and were processed within 2
hours of collection. The samples were examined microscopically for pus cells, RBCs, leukocyte , cysts and ova of parasites. The samples
were inoculated directly on the MacConky agar, Xylose-lysine desoxycholate (XLD), Hekton Enteric agar (HE) and, Salmonella Shigella
agar (SS). Enrichment was done on selient F broth and incubated for 6 hours. After the 6 hours subculture was done on SS agar. All plates
incubated at 35°C for overnight. All specimens were also processed for other enteropathogens by using standard laboratory procedures. For
isolation of Yersinia entercolitica samples, were inoculated on Cefsulodin irgasin Novobiocin agar ( CIN agar) and incubated at 20-25°C
for 24 hours. For isolation of Campylobacter jejuni we used Campy- Blood Agar plate (Campy-BAP) medium and after inoculation of
samples plates incubated at microaerophilic condition in 42°C for 48 hours. Finally, sorbitol Mackonky agar was used for isolation of
Enteroheamprrhagic E.coli .
All isolated enteric pathogens were identified by conventional bacteriological methods (
4
,
5
). Colonies resembling to shigella species were
identified by biochemical reaction and confirmed by slide agglutination test using polyvalent and monovalent antisera (Bahar Afshan,
Tehran Iran ). Susceptibility testing for shigella spp isolates were performed by disk diffusion methods as recommended by NCCLS. (
6
)
Commercially manufactured disks of antimicrobial agents and their concentration were as follows.Ampicllin10µg, ceftriaxone 30µg,
chloramphenicol 30 µg, nalidixic acid 30µg , ciprofloxacin 5 µg , trimethprim-sulfamethoxazole 1.25/2375µg
Results
4351 stool samples were sent to microbiology laboratory of Milad hospital for culture and susceptibility testing. In total 464 (10.15%)
Enteropathogens were isolated. The rate of isolation was: Shigella spp 220 (46. 5% ) isolates salmonella spp120(26.3%),
Enteropathogenic E.coli 100 (26.3% ), enterohemorragic E coli 16(3.5), Campylobacter jeujini 7 (1.5%). In our study shigella spp had the
highest isolation rate. Of 212 shigella strains isolated 157 (78.5) were S .sonnei followed by S.flexneri 44 ( 20%) S. boydii 16 (7.2%)
and S.dysenteriae only with 2 isolates (1%). The majority of patients with shigellosis were children under 12 years old. The mean age of
patients were 9.8 years (SD ±16.3) Microscopically examination of stool specimens showed Leukocyte and red blood cells in more than
90% of dysenteric specimens.
Result of susceptibility testing of Shigella spp to various antibiotics were as follows: Resistance to Ampicillin and Trimethoprime /
sulphamethoxazole was observed in 88.5% and 98% isolates respectively. 11.5% of isolates were resistant to nalidixic acid and 5.5% to
ceftriaxone. Resistance to Chloramphenicol and Ciprofloxacin were 2.5% and 1% respectively.
Table 1: Frequency of different entropathoges isolated from stool specimens during 2002-2005 in Milad hospital of Tehran.
Table 2: Serogroups of Shigella isolates from 2002-2005 in Milad hospital of Tehran
Discussion
The isolation rate of Shigella species from stool specimens in our study was 5% .Among entropathenic isolated bacteria, Shigella species
accounted 46.5% of isolation, and Shigella sonnei had the highest isolation rate.
The result of present study were compared with that previous studies in Tehran. In a study that carried out by Moez_Ardalan Shigella
flexneri was the predominant serogroup.(
7
) Another study by Nikkah showed that of 230 shigella isolates 61.2% were Sh flexneri. (
8
)
However in recent years there are changes in frequency of Shigella serogroups isolates in our country and S.sonnei has become predominant
species. The present study reveals that S. sonnei with 157 (71.3%) isolates had the predominant serogroup. Ranjbar also showed that of 302
shigella isolates in Tehran during 2002-2003, 178 (59% ) isolates were S. sonnei.(
9
) The data are also in keeping with those from other
countries. Reports from Saudi Arabia by Panhotra BR showed that 80% of shigella isolates were S . sonnei .(
3
) Studies in our neighbor
country Turkey are also revealed that 75-78% % of shigella isolates are S .sonnei. Serogroup.(
10
,
11
).
S. sonnei serotype is believed predominant and endemic in industrized countries and known to cause milder self limiting disease and to be
less resistant to antimicrobial agents. However recently S .sonnei has become the prevalent serotype in developing countries and has
developed multidrug resistance and is responsible for outbreaks of clinically sever disease
Antimicrobial therapy is recommended for shigellosis because it can shorten the severity and duration of illness, reduce shedding of the
organism, and prevent secondary complication and death. However antimicrobial resistance occurred among shigella spp, since the 1940s,
when sulfonamide resistance among shigella organism was first recognized in Japan(
12
) .In our study more than 88.5% of isolates were
multiple drug resistant. The previous studies also showed that 87.8% of shigella multiple resistant. Resistance to nalidixic acid as s first line
drug is going to increase in our country, In a study by Nikkah et al during 1984-1985 in Tehran ,all isolates of shigella were susceptible to
nalidixic acid(
8
) and in a report by Moez Ardalan in 2002-2003 only 1% of shigella spp were resistant to nalidixic acid.(
7
) In our study this
figure was 11 .5 %. In other countries like India resistance of S.sonnei to nalidixic acid between 2001-2002 was 94-100% (
13
,
14
) In as study
which carried out by Aysev in 1993-1996 in Turkey the resistance of Shigella spp to TMP-SMZ, Ampicillin , and chloramphenicol was
55.7%, 27.7% and 19.7% respectively There was not any resistance to nalidixic acid and ciprofloxacin in their study (
10
) In another of our
neighbor countries Pakistan in a study in Karachi by Zafar et al all isolates of shigella were susceptible to ceftriaxone, but a high rate of
resistance was observed to Cotrmoxazole (87.7%) and ampicillin (55.5%) in their study and emerging resistance against nalidixic acid
(39%) were observed. Jeong et al in Korea between 1980-200 showed that 30 and 86 % shigella isolates were resistant to Ampicillin and
nalidixic acid.(
15
) In a study by Mache et al in Ethiopia highest resistance shigella was encountered to tetracycline(63.6%) ampicillin
(70.1%) respectively. Resistance to Trimethprim- sulfametaxazol and nalidixic acid was 32,5% and 6.5% .
The relative antimicrobial susceptibility of different Shigella spp may vary geographically. It may be due to pattern of antibiotic using for
treatment of shigellosis. Further studies on the antibiotic resistance mechanism and genetic relatedness of isolates are required to understand
the progression of antibiotic resistance in shigella.
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... Shigellosis, a dysenteric disease caused by Shigella species is more prevalent in areas of poor sanitation and hygiene in developing countries. Earlier studies from Africa, Asia and Latin America reported the susceptibility of the disease in connection with lack of sanitation (Asgharet al, 2002;Abera, 2004;Bhattacharya et al., 2005;Andualem et al., 2006;Rahbar et al., 2007). Transmission of this disease is through faecal-oral route through contaminated hands, food and water and as epidemics where there are close personal physical contacts such as refugee camps, jails and temporary public settlements (Ochei and Kolhatkar, 2000). ...
... 71.4% S. flexneri isolates were observed with children less than five years of age in western Nepal. A similar result was found in Iran (Rahbar et al., 2007) and in Africa (Wasfy et al., 2000;Opintan and Newman, 2007) where children less than 12 years of age were the most exposed to shigellosis. In Northwest Ethiopia, 36.4% of Shigella strains were isolated from children below 15 years of age (Yismaw et al., 2006). ...
... The antimicrobial resistance pattern of the organism is reported to change (Parats et al., 2000;Rahbar et al., 2007).Increasing resistance to several antibiotics has been reported from Israel (Ashkenazi et al., 2003) and African countries (Wasfy et al., 2000;Yismaw et al., 2006;Opintan and Newman, 2007). The present study was designed to find out the prevalence and antibiotic resistance pattern of Shigella species in and around Ambo town (Western Addis Ababa) as there was no published data available from this part of the country. ...
... Shigellosis still accounts for a significant proportion of morbidity and mortality, especially in developing countries [31] . In this study, the majority of the Shigella species were isolated from children aged 1-10 years, which is similar to other studies [15,[31][32][33] . The changing patterns in the distribution of Shigella serogroups and serotypes have been reported from time to time [33][34][35][36] . ...
... In this study, the majority of the Shigella species were isolated from children aged 1-10 years, which is similar to other studies [15,[31][32][33] . The changing patterns in the distribution of Shigella serogroups and serotypes have been reported from time to time [33][34][35][36] . The shift in the prevalence of serogroups and the changing patterns in antimicrobial susceptibilities among Shigella isolates pose a major difficulty in the determination of an appropriate drug for the treatment of shigellosis [34,35] . ...
... Over the past decades, a significant number of Shigella isolates resistant to commonly-prescribed antimicrobials have been reported [41] . In early 1990s, many isolates were susceptible to nalidixic acid, norfloxacin, furazolidone, and gentamicin [33,35,39,40] . In the late 1990s, most isolates showed an increased resistance to these antimicrobials [42,34] , but most were susceptible to ciprofloxacin [19,43,44] . ...
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Objective To determine the antimicrobial resistance patterns of Shigella species to the most commonly used antibiotics in mid and far western part of Nepal. Methods Stool samples were collected from 458 patients who came from mid and far western region of Nepal, attending OPD & IPD Departments of Nepalgunj Medical College, Nepal, between the periods of September 2011 to March 2013. Standard microbiological procedures were used for isolation and identification of Shigella species while the disc diffusion test was used to determine the antimicrobial resistance patterns of the recovered isolates. Results A total of 65 isolates were identified as Shigella species. Shigella flexneri, Shigella dysenteriae, Shigella boydii and Shigella sonnei were accounted respectively for 43.07%, 27.69%, 21.53% and 7.69% of the total number of Shigella isolated. Resistances to nalidixic acid (95.38%), ampicillin (84.62%), co-trimoxazole (81.54%) and ciprofloxacin (46.15%) were observed. Greater number of isolates (38.46%) was recovered from those aged 1-10 years. This was statistically significant (P<0.05), compared to the other age groups. Conclusions The study revealed the endemicity of shigellosis with Shigella flexneri as the predominant serogroup. Children were at a higher risk of severe shigellosis. The results also suggest that nalidixic acid, ampicillin, co-trimoxazole and ciprofloxacin should not be used empirically as the first line drugs in the treatment of shigellosis. Periodic analysis of resistance patterns is necessary for the appropriate selection of empirical antimicrobial therapy.
... Occurrence of frequent outbreaks and multiple antibiotic resistances of cholera have been reported with increasing frequency in Iran (4)(5)(6)(7). The last cholera resistance pattern was reported by the study of Rahbar et al., during the year 2010. ...
... Such changes decrease or eliminate the flow of small hydrophilic molecules like beta-lactams [18]. Similarly high rates of resistance to the above antibiotics of 88.5% and 78.5% respectively, were reported in Iran [19]. Wilson et al. [20] observed a resistance rate of 39.7% by Shigella isolates to chloramphenicol comparable with 40% resistance rate obtained in this study. ...
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An outbreak of shigellosis occurred in a township of Nantou Conuty in central Taiwan from August to October in 1996. The infections extended to two neighboring townships and continued to the end of 1996. Forty cases were confirmed during the period, in contrast to only one confirmed case in Nantou County in 1996 before the outbreak. All of these 41 cases in 1996 were identified as infections withShigella flexneri serotype 2a. In order to trace the source of the infections, the 41 isolates recovered were analyzed by plasmid profile and pulsed-field gel electrophoresis (PFGE). There was no correlation between the plasmid profile results and the PFGE results, and the latter were used for subtyping of the 41 isolates. Twenty-two isolates (53%) had the same NotI and XbaI PFGE patterns, and 4 isolates (10%) had an additional unstable plasmid band in their NotI patterns but otherwise had the sameNotI and XbaI patterns as the 22 isolates. These 26 isolates were designated the outbreak strain, and of these, 24 appeared in eight villages in one township and 2 appeared in a neighboring township. Fourteen of the remaining 15 isolates, including the isolate recovered 7 months before the outbreak, had bothNotI and XbaI PFGE patterns closely related to those of the outbreak strain, indicating that Shigellainfections were endemic in the area. By tracing the first isolation dates of the outbreak strain in individual villages and the neighboring township, it was found that the strain spread along the major arterial road and its branch road as time passed. Our molecular typing results and epidemiological data demonstrated the endemic nature of the outbreak strain as well as a person-to-person mode of transmission for the widespread infections the strain caused.
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A study of adult patients with gastroenteritis was carried out over an 18-month period from March 1984 until August 1985, with the aim of detecting Shigella species and studying their antibiotic resistance pattern. Two thousand four hundred and eighteen stool specimens were examined and 230 isolations of Shigella were made, a detection rate of 9.5%. Of the 230 isolates, 61.2% were found to be Sh. flexneri, and resistance to ampicillin, chloramphenicol, co-trimoxazole and tetracycline was extremely high, varying from 47% of isolates for chloramphenicol to 77% for tetracycline. Resistance to nalidixic acid was not encountered. In view of the fact that this disorder tends to be a self-limiting condition in Iran, it is advisable to be selective and cautious in the use of antibiotics for treatment.
Article
The occurrence and antimicrobial resistance pattern of Shigella isolates obtained from persons in community and hospital-based studies of diarrhea and matched controls in northeastern Brazil were studied. The isolation rate of Shigella spp. from patients with diarrhea during 1988 to 1993 varied from 4.5% (26 of 575) for the urban community of Gonçalves Dias to 6.7% (12 of 179) and 5.9% (7 of 119) for Hospital Infantil and Hospital Universitário, respectively. Of the 55 Shigella isolates (45 from patients with diarrhea, 8 from controls, and 2 undetermined) 73% (40 of 55) were Shigella flexneri, 16% (9 of 55) were S. sonnei, 7% (4 of 55) were S. boydii, and 4% (2 of 55) were S. dysenteriae. Of 39 S. flexneri strains, over half were resistant to ampicillin, trimethoprim-sulfamethoxazole, or both. Over 64% were resistant to streptomycin, chloramphenicol, and tetracycline. Overall, 82% of all S. flexneri isolates were resistant to four or more antimicrobial agents tested. As elsewhere, in the northeast of Brazil, ampicillin and trimethoprim-sulfamethoxazole are no longer reliable for treatment of S. flexneri infection. Most Shigella strains were resistant to four or more antimicrobial agents. Nalidixic acid was still useful for treatment of infections due to S. flexneri.
Article
Shigella flexneri was the most common Shigella serogroup isolated in Turkey. Recently, an increase in the number of Shigella sonnei isolates was noticed. A retrospective analysis of 2,710 isolates, obtained from stools of Turkish children between January 1980 and September 1994, revealed that, between 1980 and 1987, S. flexneri was the most common subgroup. The isolation rate of S. sonneri increased steadily from 1987 to 1994 reaching to a peak of 78% of all isolates in 1991. The antibiotic susceptibility of 206 strains isolated in 1994 was also studied. A marked difference between the two species was observed for chloramphenicol (98% susceptibility in S. sonnei versus 20% in S. flexneri, ampicillin (90% vs. 18%), ampicillin-sulbactam (98% vs. 53%), and tetracycline (46% vs. 18%) (p < 0.001). Susceptibility to trimethoprim-sulphamethoxazole was similar between the two groups (42% vs. 38%). All isolates were susceptible to ciprofloxacin and ceftriaxone. Comparing our results with resistance rates in 1989, a marked increase in amplicillin (from 44.1% to 82%), chloramphenicol (from 36.7% to 56%) and trimethoprim-sulphamethoxazole (from 35.8% to 62%) resistance was observed.
Article
289 Shigella strains were isolated from children at the paediatrics department of Ankara University. 75% of the isolates were S. sonnei and 24.8% were S. flexneri. Each strain was tested for resistance to 9 antimicrobial agents. 79% of the isolates were resistant to streptomycin (S), 56% to tetracycline (T), 55.7% to trimethoprim-sulfamethoxazole (SXT), 27.7% to ampicillin (Am) and 19.7% to chloramphenicol (C). None of the isolates was resistant to ciprofloxacin, nalidixic acid, cephalothin, ampicillin-sulbactam and ceftriaxone. 56% of the isolates were resistant to 3 or more antimicrobial agents. The most frequent pattern of resistance of S. sonnei and S. flexneri strains was SXT, T, S (39.6%) and Am, SXT, T, S, C (48.6%), respectively (p < 0.0001). These results demonstrate that trimethoprim-sulfamethoxazole should not be used in the treatment of shigellosis.
Article
Prevalence of Shigellae serotypes in Bombay was studied from June 1988 to May 1991. A total of 2758 faecal specimens were collected from paediatric patients (< 12 yrs) with acute gastroenteritis. A total of 90 Shigella were isolated giving the isolation rate of 3.2%. Shigella flexneri was the predominant serogroup (73.3%) followed by Shigella dysenteriae (16.6%). All the isolates were sensitive to nalidixic acid. Eighty percent of the Shigellae were multidrug resistant. Present data were compared with the study carried out during the period of 1983-87 from the same institute. A change in the serogroup prevalence was noted wherein Shigella flexneri dominated over Shigella dysenteriae since 1985. Increase in resistance to ampicillin and cotrimoxazole was seen in Shigella flexneri strains as compared to previous years.
Article
To determine the prevalence of Shigella sero-groups and resistance pattern of isolates to commonly used antibiotics in Jimma. Cross-sectional survey. The study was conducted in Jimma, southwest Ethiopia. A total of 384 paediatric out-patients with diarrhoea aged 14 years and below were studied. Stool specimens were collected from children presenting with diarrhoea using Cary-Blair transport medium and buffer treated swabs from Jimma hospital and Jimma health centre. Isolation, biochemical characterisation, sero-grouping and antibiotic sensitivity testing were performed according to standard methodology in the Microbiology laboratory of Jimma University. Out of the 77 Shigella strains isolated, sero-group A comprised 29.9%, B 40.3%, C 19.5% and D 10.4%. Among all Shigella sero-groups, highest resistance was encountered to tetracycline (63.6%), ampicillin (70.1%), cephalothin (57.1%), trimethoprim-sulphamethoxazole (32.5%) and chloramphenicol (40.3%) whileleast resistance was observed to gentamicin (1.3%), polymyxin B (3.9%) and nalidixic acid (6.5%). Gentamicin, polymyxin B and nalidixic acid were found to be the drugs of choice for cases related with shigellosis.
Article
Shigellosis has been a major cause of dysentery for many years at Vellore, south India. In the last two years the number of Shigella being isolated from samples of faeces from patients with diarrhoea has decreased (5% isolation rate in 1997 to 3.9% in 2001), although the microbiological methods and media used have not changed. Also, the nalidixic acid (NA) resistance has increased for S. sonnei (now 94%). This is noteworthy, since NA has been recommended for the empirical treatment of patients suspected to have shigellosis and this concept needs to be reconsidered based on available data.