Department of Microbiology, The Chinese University of Hong Kong, The Prince of Wales Hospital, Shatin, New Territories, Hong Kong SAR, China
Received 6 October 2002; returned 4 December 2002; revised 14 January 2003; accepted 21 January 2003
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Abstract |
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Keywords: community-acquired infections, antimicrobial susceptibilities
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Introduction |
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In Hong Kong, healthcare is provided by the Hospital Authority, the Department of Health and private doctors. The Hospital Authority manages hospitals and provides follow-up services to discharged patients, whereas the Department of Health mainly provides consultation to general outpatients. Services provided by these two organizations are largely subsidized by the government, and patient waiting times are frequently long. Patients with acute symptoms, who can afford higher consultation fees, may visit private doctors and hospitals to obtain a faster service. There are no particular criteria by which patients select private doctors, other than convenience (closeness of clinics to home), word-of-mouth by other patients and competititive consultation fees. According to official figures for 2001, there are 1.5 doctors per 1000 population (http://www.info.gov.hk/censtatd/eng/hkstat/hkinf/health/health_4_index.html). With a population of 6.7 million, there are 10 050 doctors, of whom an estimated 3500 are primary care doctors.2
Published local susceptibility results are usually based on hospital isolates,37 whereas reports on community-acquired organisms are few. There is only one detailed report on the susceptibility patterns of general practice organisms in Hong Kong.8 There may be greater demand for such data in general practice than in hospitals, since specimens are often not submitted for culture from general practitioners.
In this study of the Hong Kong region, we aimed to investigate prospectively culture-positive infections in patients visiting general practitioners, and to determine the susceptibility of these isolates to commonly used and newer antimicrobial agents.
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Materials and methods |
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Results |
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Table 1 shows the type and distribution of specimens. The most common specimen was a throat swab (33%), followed by urine (26%) and sputum (16%). The other specimens constituted 6% or less. The culture-positive rate ranged from 17% (stool or rectal swab) to 80% (ear swab), with an average of 28%. Wound swab and pus gave the next highest culture-positive rate of 68% and 57%, respectively.
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Antimicrobial resistance of Gram-negative bacteria
More than 60% of E. coli isolates were resistant to ampicillin, but only 16% were resistant in the presence of clavulanic acid (Table 3). More than 50% were resistant to 4 mg/L cefuroxime, but <5% to the third-generation cephalosporins ceftriaxone or cefotaxime, and none to ceftazidime or imipenem. Thirty per cent were resistant to gentamicin, 2% to netilmicin and 0% to amikacin. Although 50% were resistant to nalidixic acid, 1625% were resistant to the fluoroquinolones. Forty or more per cent were resistant to the other antibiotics, such as trimethoprim, sulfamethoxazole, chloramphenicol or tetracycline. Significantly more E. coli isolates were resistant to cefuroxime (P < 0.01), gentamicin, nalidixic acid and ofloxacin (P < 0.05) in this study, as compared with the previous report.8
Only 3% of Klebsiella spp. were resistant to the combination of ampicillin and clavulanic acid (Table 3). Ten per cent or fewer were resistant to cefuroxime or cefamandole, but none was resistant to the third-generation cephalosporins or imipenem. Resistance to aminoglycosides or the fluoroquinolones was low, being 05%. Although fewer isolates were resistant to gentamicin, nalidixic acid or ofloxacin as compared with our previous study,8 the difference was not significant (P > 0.05).
More than 60% of Proteus spp. and Morganella spp. were resistant to ampicillin, but none was resistant in the presence of clavulanic acid (Table 3). More than 10% (1218%) were resistant to the fluoroquinolones, but 35% were resistant to gemifloxacin. All were susceptible to ceftriaxone, cefotaxime, imipenem, netilmicin and amikacin. Significantly more isolates of the present study were resistant to ampicillin or ceftazidime as compared with the previous study (P < 0.05).8
Resistance to the third-generation cephalosporins or aminoglycosides was generally low (46%) in the enterobacters (Table 3). Only 2% were resistant to the fluoroquinolones, including the newer ones, such as moxifloxacin or gemifloxacin. Nine per cent of salmonellae were resistant to ampicillin, whereas all were susceptible to ampicillin + clavulanic acid, the second- and third-generation cephalosporins, aminoglycosides and the fluoroquinolones; however, 18% were resistant to chloramphenicol.
Antibiotic resistance in P. aeruginosa and acinetobacters was low, with all strains being susceptible to ceftazidime, imipenem, meropenem, aminoglycosides or fluoroquinolones (Table 3).
Less than 40% of H. influenzae were resistant to ampicillin, but only one isolate remained resistant to ampicillin in the presence of clavulanate (Table 4). ß-Lactamase was detected in nine isolates, which represented 43% of ampicillin-resistant strains and 14% of all isolates. Forty-seven per cent were resistant to cefaclor and 1119% to chloramphenicol or tetracycline. All were resistant to erythromycin, 69% to clarithromycin, but only 23% were resistant to the second- and third-generation cephalosporins and fluoroquinolones. Significantly fewer strains were resistant to ampicillin than in the previous study (P < 0.01).
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Antimicrobial resistance of Gram-positive bacteria
Table 5 shows antimicrobial resistance in S. aureus, Streptococcus pneumoniae, ß-haemolytic streptococci and enterococci. Three (2%) strains of S. aureus were resistant to methicillin. Resistance to aminoglycosides (05%) or fluoroquinolones (2%) was low. None was resistant to vancomycin. More than 80% of S. pneumoniae were resistant to 0.06 mg/L penicillin, all of which had MICs 0.120.25 mg/L. Resistance to clarithromycin, erythromycin or tetracycline was high (90%), but none was resistant to ampicillin, cefotaxime or ceftriaxone. Resistance to the fluoroquinolones was also low, with 2% to sparfloxacin or gemifloxacin, but 0% to levofloxacin or moxifloxacin. Although 10% of ß-haemolytic streptococci were resistant to penicillin, all belonged to groups C and G. Resistance to levofloxacin or moxifloxacin (0.51%) was low, but higher to gemifloxacin, ofloxacin or sparfloxacin (46%). However, resistance to clarithromycin was high (33%). None of the enterococci was resistant to 8 mg/L penicillin or ampicillin and vancomycin, and <10% (49%) were resistant to fluoroquinolones.
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Discussion |
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Throat swabs were the most common specimens collected, followed by urine. However, throat swabs together with sputa constituted 49% of all specimens, whereas urine constituted 26%; both figures are comparable to that reported in our last study (48% and 28%, respectively).8 Thus, most patients sought medical attention because of respiratory problems, whereas urinary symptoms were the next most common complaint. Urinary tract infection is more commonly seen in females, and this may have led to the large number of urine samples and high vaginal swabs collected from females, and the resulting male:female ratio = 1:1.23.
Also, for a similar reason (the large numbers of throat swab and urine collected), it is not surprising that ß-haemolytic streptococci and E. coli top the list of organisms isolated. However, this is in contrast to what was observed in our last study when H. influenzae was the most common organism isolated, with E. coli and ß-haemolytic streptococci being the third and seventh most common, respectively.8 The small number of H. influenzae strains isolated could indicate that chest infections caused by this organism had decreased in importance. Previously, 13% of sputa yielded H. influenzae,8 whereas only 9% yielded the organism in this study. It is difficult to speculate why this is so as H. influenzae type b vaccination was not given routinely. The isolation of enterobacteria and non-enterobacteria, such as P. aeruginosa and acinetobacters from respiratory specimens probably represented colonization rather than true pathogens. The comparatively large numbers of N. gonorrhoeae isolated from urethral swabs indicated the importance of gonorrhoea in the community.
Penicillin resistance in S. pneumoniae was indeed a problem in Hong Kong (81%), with an almost five-fold increase over 10 years,8 although the organism was mainly isolated from respiratory specimens and the resistance was low-level (MICs < 1 mg/L). The third-generation cephalosporins and the newer fluoroquinolones remained active against this organism. Accumulating evidence has shown that patients with pneumonia caused by pneumococci with intermediate susceptibility to penicillin respond well to treatment with sufficient doses of intravenous penicillin.1719 However, local penicillin concentration may not be high enough against infections by such strains at other sites, for example meningitis.20
Ampicillin resistance remained at 6070% in E. coli. However, fluoroquinolone resistance to ofloxacin increased considerably, from 622%,8 and from 018% in Proteus and Morganella, the organisms commonly causing urinary tract infection. Whether this was related to the frequent prescription of fluoroquinolones for treatment of this infection requires further investigation. Although resistance to the third-generation cephalosporins was not a problem in the Gram-negatives, these mainly intravenous drugs would not be a good choice for treating community-acquired infections.
There were three strains of methicillin-resistant S. aureus (MRSA), indicating that MRSA was not only a hospital phenomenon.21,22 Our enterococci were mainly isolated from urine and had remained fairly susceptible to fluoroquinolones. Vancomycin-resistant enterococci (VRE) were not present in our collection. Coque et al.23 also did not find any VRE in their survey of healthy volunteers.
It is surprising to find a significant decrease in ampicillin resistance in H. influenzae (from 64%8 to 39%, P < 0.01) although the proportion of ß-lactamase-producing strains were similar (40%24 versus 43%) and were also similar to that reported by Doern et al.25 However, resistance to macrolides remained high, even to clarithromycin (69%). Second- and third-generation cephalosporins and the fluoroquinolones remained active (3% resistance).
Although 10% of ß-haemolytic streptococci were resistant to penicillin, none was group A. The newer fluoroquinolones would probably be the next drugs of choice, rather than the macrolides, for infections caused by this group of organisms.
Penicillin, as in other parts of the world, would no longer be effective in treating gonorrhoea.2628 However, the proportion of ß-lactamase-producing strains was much lower in our study: 18% versus 75% in Indonesia26 and 37% in Mongolia.27 With the considerable high level of resistance to fluoroquinolones (>30%) and spectinomycin (15%), ceftriaxone would be the only drug of choice.
In order to investigate patterns of antibiotic use, doctors were asked to indicate the antibiotics they would prescribe to individual patients. However, since this was voluntary, and possibly inaccurate, detailed results are not included here, but will be discussed briefly. Available information showed that ampicillin was the most commonly prescribed antibiotic, followed by cefuroxime, co-amoxiclav, cloxacillin, cefaclor, co-trimoxazole and clarithromycin, each constituted 516% of the total prescription given (some patients received more than one antibiotic). A total of 2934 patients received antibiotics, although only 1293 specimens became culture-positive (Table 1). There was therefore much overuse of antibiotics. This may have been because patients demanded excess drugs, since the consultation fee often included the cost of medicine. A recent article2 indicated that 22% of 801 doctors who responded to a survey on antibiotic usage felt that they were prescribing antibiotics too often for upper respiratory infections. We suggest that antibiotics should only be prescribed if there is a high suspicion of infection. Specimens should be taken for culture and antibiotics stopped, if appropriate, for instance when the culture results are negative. First-line antibiotics should be chosen and, according to antibiotic susceptibility results, the duration of the course of treatment should be adequate, and probably involve cycling of antibiotics.29
To conclude, in our study, fluoroquinolone resistance was relatively high in organisms causing urinary tract infection. Intermediate penicillin resistance in pneumococci was alarming. The newer fluoroquinolones, or third-generation cephalosporins, would be active against organisms causing respiratory infections. Antibiotic resistance was on the rise, although the trend varied in different organisms. The distribution of organisms and their antibiotic resistance varied, so that frequent surveys are warranted to provide information on the drugs of choice for different infections.
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Acknowledgements |
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Footnotes |
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References |
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