Antimicrobial Agents and Chemotherapy, February 1998, p. 440-443, Vol. 42, No. 2
0066-4804/98/$04.00+0
Copyright © 1998, American Society for Microbiology. All rights reserved.
Antimicrobial Resistance in Shigella
flexneri and Shigella sonnei in Hong Kong, 1986 to 1995
Yiu-wai
Chu,1
Elizabeth T. S.
Houang,1
Donald J.
Lyon,1,*
Julia M.
Ling,1
Tak-keung
Ng,2 and
Augustine F. B.
Cheng1
Department of Microbiology, The Chinese
University of Hong Kong, The Prince of Wales Hospital, Shatin, New
Territories,1 and
Department of
Pathology, Princess Margaret Hospital, Kowloon,2
Hong Kong
Received 30 May 1997/Returned for modification 7 August
1997/Accepted 14 November 1997
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ABSTRACT |
Three hundred and thirty-three Shigella isolates
obtained in 1986 to 1995 were tested for their susceptibilities to 19 antimicrobial agents. Nalidixic acid resistance had emerged in 59.6%
of Shigella flexneri isolates during 1994 to 1995, with all
tested resistant isolates having the mutation in gyrA
encoding the Ser-83 alteration. Multiresistance (resistance to four or
more agents) was more common in S. flexneri than in
Shigella sonnei.
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TEXT |
Bacillary dysentery is an important
cause of traveler's diarrhea worldwide (13, 14, 16, 18).
Appropriate antibiotic therapy reduces the duration of symptoms and
excretion of organisms (15) but increases the risk of
developing antibiotic resistance. High frequencies of resistance in
Shigella flexneri (2, 6, 12) and Shigella
sonnei (1) to many of the first-line antimicrobial agents have been reported in recent years from many parts of the world.
The purpose of this study was to review the antimicrobial susceptibility patterns of Shigella spp. isolated in Hong
Kong from 1986 to 1995, with particular reference to resistance to the
4-quinolones.
Bacterial strains.
We studied all the available 144 Shigella isolates obtained from 1988 to 1995 at the Prince
of Wales Hospital (PWH) in Hong Kong and 90 1995 isolates obtained at
the Princess Margaret Hospital (PMH) in Hong Kong. In addition, 99 isolates that had been collected in 1986 to 1987, obtained from the
same laboratories, studied by Ling et al. (7), and stored
since then at 
70°C were also included for comparison. Both
hospitals are regional general hospitals serving a predominantly urban
area with a population of approximately 2 million, and PMH has the
Infectious Diseases Unit serving all Hong Kong, with a population of 6 million. The primary medium for Shigella isolation was
desoxycholate-citrate agar (DCA) (Oxoid, Basingstoke, United Kingdom)
at PWH and DCA plus xylose-lysine-desoxycholate agar (Oxoid) at PMH.
The identification of the 222 S. flexneri and 111 S. sonnei isolates was confirmed by standard laboratory methods
(4). Of 204 isolates of S. flexneri which were
serotyped, 148 were type 2, 27 were type 1, 20 were type 3, 7 were type
4, 1 was type 6, and 1 was the X variant.
Antimicrobial susceptibility testing.
MICs for 19 antimicrobial agents were determined by the agar dilution method as
previously described (19). The 19 antimicrobial agents
used in this study were ampicillin, chloramphenicol, nalidixic acid, sulfamethoxazole, trimethoprim, and tetracycline (all from Sigma Chemical Co., St. Louis, Mo.), amoxicillin-clavulanic acid (SmithKline Beecham Pharmaceuticals, Philadelphia, Pa.),
amikacin, and cefepime (all from Bristol-Myers Squibb Co., Princeton,
N.J.), cefotaxime and gentamicin (both from Hoechst Marion
Roussel, Paris, France), cefuroxime and ceftazidime (both from
Glaxo Group Research Ltd., Greenford, Middlesex, United Kingdom),
piperacillin (Lederle Laboratories, Pearl River, N.Y.), ciprofloxacin
(Bayer AG, Leverkusen, Germany), imipenem (Merck & Co., Inc., West
Point, Pa.), netilmicin (Schering Canada Inc., Pointe Claire,
Québec, Canada), ofloxacin (Daiichi Pharmaceutical Co., Ltd.,
Tokyo, Japan), and sparfloxacin (Rhône-Poulenc Rorer,
Vitry-sur-Seine, France). Inocula of 104 CFU/spot
were inoculated onto Iso-Sensitest agar (Oxoid) with a multipoint
inoculator (Dynatech Laboratories, Alexandria, Va.), and the plates
were incubated at 37°C for 18 h. The MIC was defined as the
lowest concentration which inhibited visible growth. Control strains
Escherichia coli NCTC 10418 and Pseudomonas
aeruginosa NCTC 10662 were included. The rates of resistance to
antimicrobial agents were expressed by using the breakpoints of the
National Committee for Clinical Laboratory Standards (10).
Detection of the gyrA mutation.
A previously
described PCR-restriction fragment length polymorphism
method (11) for detecting the gyrA mutation
encoding the Ser-83 alteration was performed on 55 S. flexneri isolates, all showing nalidixic acid MICs of 
32
µg/ml, and 12 randomly selected susceptible isolates as negative
controls.
Results.
Table
1 shows the
geometric-mean MIC, MIC at which 50% of the isolates are
inhibited (MIC50), MIC90, and the percentage of resistance for 14 of the 19 antimicrobial agents. No isolates were
resistant to imipenem, cefepime, ceftazidime, cefotaxime, or
amikacin, and MIC data for these isolates are not shown in the table.
The S. flexneri isolates had high frequencies of resistance to ampicillin, amoxicillin-clavulanic acid, chloramphenicol,
tetracycline, trimethoprim, and sulfamethoxazole. There was a
marked increase in resistance to nalidixic acid, rising from 0% in
1986 and 1987 isolates to 59.6% in 1994 and 1995 isolates and an
increase in the geometric-mean MICs for the fluoroquinolones, although
only two isolates were resistant to ciprofloxacin (2 µg/ml). The
Ser-83 mutation was detected only among the 55 isolates of S. flexneri with nalidixic acid MICs of 32 µg/ml, all of which
also showed ciprofloxacin MICs of 0.25 µg/ml. These
mutation-positive isolates had significantly higher MICs than
mutation-negative isolates from the same time period for tetracycline,
trimethoprim, sulfamethoxazole, chloramphenicol, gentamicin,
imipenem, cefepime, and amoxicillin-clavulanic acid as well as
the 4-quinolones (P < 0.03 to P < 0.0001 by the Mann-Whitney test). All mutation-positive, nalidixic
acid-resistant isolates were of serotype 2. In the S. sonnei
isolates, high frequencies of resistance were also seen for some
agents. With the exception of tetracycline, trimethoprim, and
sulfamethoxazole, S. sonnei isolates had significantly
lower MICs than S. flexneri for all agents tested
(P < 0.02 to P < 0.0001 by the
Mann-Whitney test).
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TABLE 1.
MICs and percentages of resistance of 14 antimicrobial
agents in 222 S. flexneri and 111 S. sonnei isolatesa
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Table 2 compares the resistance patterns
of isolates of both species for two periods: 1986 to 1987 and 1994 to
1995. For S. sonnei, the proportions of isolates
showing resistance to four or more agents were not statistically
different (13 of 34 versus 9 of 38; P > 0.05 by the
chi-square test). For S. flexneri, a significantly greater
proportion of isolates was resistant to at least four agents in 1994 to
1995 (38 of 65 versus 88 to 94; P < 0.001 by the
chi-square test). One antibiogram showing resistance to seven
antimicrobials was seen in 47% of S. flexneri isolates from
1994 to 1995.
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