Surveillance is a critical aspect of antibiotic resistance control. Susceptibility data periodically collected from patients can be used to construct antibiograms for monitoring of resistance trends and guidance of empirical treatment.1

The Working Group of Collaboration between the Centre for Health Protection (CHP) and Private Hospitals on Safe Use of Antibiotics and Infection Control (the “Working Group”) was established to exchange information regarding infection prevention and to promote safe antibiotic use. Members included the Infection Control Branch of the CHP and the Hong Kong Private Hospitals Association. Each year, the Infection Control Branch collected from and shared the susceptibility data with private hospitals. The resulting antibiograms were uploaded to the CHP website.2

Hong Kong runs a dual-track healthcare system, in which the private sector complements the public system with a range of general and specialist services. In accordance with the market-set price principle, private hospitals and out-patient clinics establish their charges based on the costs of services provided. Although private sector expenses can be severalfold higher than the expenses of their public counterparts, services provided by the private sector are often considered more flexible and personalised; thus, they are more appealing to individuals with the ability and interest in payment for such services. In 2018, private hospitals provided approximately 5000 beds for >370 000 in-patients, which constituted approximately 17% of all in-patients in Hong Kong.3 4

The objective of this study was to analyse the antibiogram data collected from private hospitals in Hong Kong by describing the temporal trends of non-susceptibility percentages in this setting. The results may provide insights regarding the current level of antibiotic resistance in private hospitals, in comparison with other settings; they may guide the establishment of future surveillance methods.

The surveillance data submitted by all 12 private hospitals during the period from 2014 to 2019 were included in this study. Please refer to the Acknowledgement for the membership of the Working Group and their affiliated hospitals/institutions.

Considering the antibiotic resistance situations in Hong Kong and other countries, as well as the health effects of various bacterial species, members of the Working Group agreed upon six targeted bacteria for the annual submission of antibiotic susceptibility testing (AST) results, including: Staphylococcus aureus, Escherichia coli, Klebsiella spp, Pseudomonas aeruginosa, Acinetobacter spp, and Streptococcus pneumoniae (since 2015).

Resistant strains of the targeted bacteria can cause increased morbidity and mortality because of limited treatment options. International health authorities have set clear priorities in their efforts to control multidrug-resistant organisms (MDROs).5 6 The definitions for MDROs used in this study were as follows: methicillin-resistant S aureus (MRSA) demonstrated resistance to methicillin, oxacillin, cefoxitin, or cloxacillin; extended-spectrum beta-lactamase-producing (ESBL+) E coli or Klebsiella spp were defined as E coli or Klebsiella spp isolates with positive ESBL test results; carbapenem-resistant Enterobacteriaceae (CRE) were defined as E coli or Klebsiella spp with resistance to a carbapenem (ertapenem, imipenem, or meropenem); multidrug-resistant P aeruginosa (MRPA) demonstrated simultaneous resistance to 11 drugs under four classes of antibiotics (beta-lactams, carbapenems, aminoglycosides, and fluoroquinolones); multidrug-resistant Acinetobacter spp (MDRA) demonstrated simultaneous resistance to 12 drugs under five classes of antibiotics (cephalosporins, fluoroquinolones, aminoglycosides, beta-lactams [± beta-lactamase inhibitor], and carbapenems). Tests to identify MRPA and MDRA were performed in accordance with Hospital Authority guidelines, although piperacillin assessment was omitted. Multidrug-resistant strains of S pneumoniae have not been defined.

The following data (concerning the previous calendar year) were annually collected from the Infection Control Teams of individual private hospitals: identification number and date for admission or attendance; location of specimen collection (in- or out-patient); specimen type (eg, sputum or mid-stream urine) and specimen date (collection, request, or laboratory registration); identification number of isolates within the same specimen; and AST results of each targeted bacterium. Only isolates from clinical specimens (rather than screening specimens) were submitted.

The AST results were divided into three categories: “susceptible”, “intermediate”, and “resistant”. “Intermediate” and “resistant” were collectively regarded as “non-susceptible” (NS). Interpretations by private hospital microbiology laboratories were based on Clinical Laboratory Standards Institute definitions.

Repeated isolates were de-duplicated for each calendar year using the first isolate in each admission, location, specimen group, and targeted bacterium. Importantly, some isolates may not have been tested for susceptibility to all antibiotics listed. The NS percentages for each antibiotic were calculated based on the proportion of isolates tested for that antibiotic. The Cochran–Armitage trend test was used for temporal trends. P values <0.05 were considered statistically significant. All analyses were performed using Stata 14.2 (Stata Corp, College Station [TX], US).

Patient consent was not obtained because aggregated patient data were used without identifying information.2 Ethics approval was obtained. This manuscript adheres to the STROBE statement checklist of cross-sectional studies for items to be included.

The total number of isolates per year, NS percentages, and MDRO percentages for isolates from both in- and out-patients were calculated for S aureus (Table 1), E coli (Table 2), Klebsiella spp (Table 3), P aeruginosa (Table 4), Acinetobacter spp (Table 5), and S pneumoniae (Table 6). Key in-patient results are highlighted below.

There were approximately 4100 to 5800 S aureus isolates per year (Table 1); respiratory specimens comprised 50% and wound/pus swab specimens comprised approximately 35% (online Supplementary Table). The NS percentage for clindamycin ranged from 24% to 31%. The NS percentages for co-trimoxazole and fusidic acid were low (1%-2% and 3%-5%, respectively). Staphylococcus aureus showed full susceptibility to both vancomycin and linezolid (ie, NS percentages of 0%). The overall prevalence of MRSA was 19% to 22%. For analysis of blood specimens, 29 to 73 isolates were obtained from in-patients each year; of these, 10% to 18% were MRSA.

There were approximately 7900 to 9700 E coli isolates per year (Table 2); nearly 70% were from urine and approximately 10% were from wound/pus swabs. The NS percentages for amoxicillin-clavulanate and cefuroxime (parenteral) were moderately high (25%-33% and 36%-38%, respectively). The NS percentages for fluoroquinolones were also moderately high (eg, 31%-37% for levofloxacin). The NS percentages for nitrofurantoin and carbapenems were low (4%-8% and 0%-1%, respectively). In terms of MDROs, ESBL+ E coli demonstrated moderate prevalence (25%-28%), while carbapenem-resistant E coli was uncommon (0.1%-0.7%) among all isolates.

There were approximately 2400 to 3400 Klebsiella isolates per year (Table 3); >30% were from urine and >30% were from respiratory specimens. The NS percentages were somewhat high: 16% to 24% for amoxicillin-clavulanate, 25% to 30% for cefuroxime (parenteral), 12% to 18% for levofloxacin, and 18% to 26% for ciprofloxacin. The NS percentage for carbapenems ranged from 0% to 2%, with an increasing trend during the study period. In terms of MDROs, ESBL+ Klebsiella demonstrated low prevalence (13%-17%), while carbapenem-resistant Klebsiella was uncommon (0.2%-1.3%) among all isolates.

There were approximately 1300 to 1800 P aeruginosa isolates per year (Table 4); approximately 60% were from respiratory specimens and 15% were from wound/pus swabs. The NS percentage for the antipseudomonal beta-lactams piperacillin-tazobactam was generally low (6%-11%), whereas it was very high for ticarcillin-clavulanate (63%-74%). The NS percentages for aminoglycosides were also generally low (3%-11% for gentamicin and 1%-5% for amikacin). The NS percentage for ciprofloxacin remained consistent throughout the study period (14%-15%). The prevalence of MRPA was very low (0.0%-0.3%).

There were approximately 400 to 500 Acinetobacter isolates per year (Table 5); they were mostly from respiratory specimens, wound/pus swabs, and urine (70%, 12%, and 10%, respectively). The NS percentages for sulbactam-containing antibiotics were 7% to 17% (ampicillin-sulbactam) and 8% to 15% (cefoperazone-sulbactam). The NS percentages for fluoroquinolones (eg, ciprofloxacin) ranged from 13% to 25%. The NS percentages for carbapenems were somewhat high values (8%-20% for imipenem and 8%-19% for meropenem). The overall prevalence of MDRA ranged from 2.2% to 7.8%.

There were approximately 300 to 600 S pneumoniae isolates per year (Table 6); approximately 90% were from respiratory specimens. The NS percentages for beta-lactams were low (2%-9% for penicillin, 2%-10% for cefotaxime, and 1%-7% for ceftriaxone). The NS percentages for fluoroquinolones (eg, levofloxacin) were low (0%-3%); the NS percentages for macrolides (eg, erythromycin) were very high (71%-79%). Streptococcus pneumoniae showed full susceptibility to vancomycin (ie, NS percentage of 0%).

To our knowledge, this is the first analysis of susceptibility data among private hospitals in Hong Kong. Such information provides important guidance for clinical management and infection control measures in the private sector. Here, we consider our findings within local and international contexts.

Staphylococcus aureus infections are usually treated by amoxicillin-clavulanate, cloxacillin, or cefazolin unless contra-indicated (eg, in cases of drug allergy) or MRSA is suspected. For mild and superficial infections, oral agents such as clindamycin and co-trimoxazole can be considered, particularly when such treatment is supported by AST results. Routine combination treatment with aminoglycosides for serious infections is no longer recommended because this carries a risk of nephrotoxicity.7

Methicillin-resistant S aureus bacteraemia is a serious condition with substantial mortality (>30%).8 Methicillin-resistant S aureus is prevalent in Hong Kong; in 2020, it comprised 43.1% of S aureus isolates among all clinical specimens in public hospitals, as well as 46.6% of isolates from blood cultures.9 Residential Care Home for the Elderly (RCHE) resident carriage rates reportedly range from 30.1% to 37.9%.10 11 In Australia, MRSA is present in 17% to 22% of blood and other specimens.12 In the UK, MRSA was present in 6.0% of invasive isolates in 201913; this low rate could be related to the extensive surveillance and infection control efforts that resulted in a remarkable 86% decrease in bloodstream infections (from 7700 to 1114 per year) from 2003 to 2012.14 Moreover, the prevalence of MRSA among S aureus isolates from human specimens decreased from 14% in 2013 to 7% in 2017.15 The prevalence of methicillin resistance should be considered when selecting empirical therapy for patients with S aureus infections.

Vancomycin is a key component of therapy for serious MRSA infections. Consistent with the low prevalence of vancomycin resistance worldwide,16 vancomycin-resistant S aureus was absent from our dataset. Staphylococcus aureus rarely demonstrates resistance to linezolid17; as expected, S aureus isolates in this study showed full susceptibility to linezolid. However, although the NS percentages for co-trimoxazole and fusidic acid were low, these agents should serve as adjuncts only instead of monotherapy in serious infections.

Susceptible strains of E coli and Klebsiella spp are usually treatable by amoxicillin-clavulanate or cefuroxime.18 However, ESBL-producing strains should be suspected in cases of serious infection because of Enterobacteriaceae prevalence in Hong Kong, where ESBL-producing E coli is regarded as a critical MDRO.18

Community spread is an important source of ESBL-related infections; food animals are presumed to serve as a major reservoir.19 For instance, the isolation rate from pig offal is 52.4%.20 Among public hospitals, the percentage of resistance to third-generation cephalosporins (“3GC”) as a surrogate marker for ESBL production among E coli is approximately 26%9; this value is similar to our findings. Furthermore, 17.0% to 18.6% of E coli isolates from community urinary specimens demonstrate ESBL-producing activity.9 Among RCHE residents, 55.9% were reported to be carriers of ESBL-producing bacteria.9 In the UK, 12% of E coli isolates from blood specimens showed ESBL-producing activity15; Singaporean public hospitals identified ESBL-producing activity in 25.2% of E coli isolates and 28.2% of Klebsiella isolates in 2017.21 From 2014 to 2019, the percentages of ESBL-producing isolates among Klebsiella isolates at public hospitals in Hong Kong were 19% to 22%.9

Surveillance data regarding ESBL prevalence can be affected by changes in laboratory practice over time. Specifically, the Clinical and Laboratory Standards Institute revised the cephalosporin breakpoints in 2014, thus eliminating the need to perform ESBL testing for clinical management—testing remains necessary for some infection control purposes and epidemiological investigations.22 However, not all laboratories have adopted the revised approach and the change remains controversial.23 The clinical specimen data in this study indicate that all participating private hospitals have continued to perform ESBL testing for Enterobacteriaceae isolates.

For serious infections caused by ESBL-producing organisms, carbapenems are the most effective treatments.18

Our findings indicate that carbapenem resistance remains uncommon but is increasing. Among the known carbapenem resistance mechanisms, carbapenemase production is the most important from an infection control perspective, considering its propensity to spread to other organisms.24 Carbapenem-resistant Enterobacteriaceae is often resistant to multiple classes of antibiotics, which hinders treatment.25 The prevalence of this high-priority MDRO is increasing worldwide,5 6 presumably in relation to heightened awareness, modified screening practices, and increased transmission.26

Public hospitals in Hong Kong reported increasing NS to carbapenem among E coli isolates from 0.2% in 2016 to 0.4% in 2020 (NS percentage of 1.1%-1.8% for Klebsiella).9 Carbapenem-resistant E coli has become a major target of infection control efforts in public hospitals.27 In contrast, CRE was not found among RCHE residents in a 2018 study.10

The limited treatment choices for CRE infection include beta-lactam agents such as ceftazidime-avibactam (inactive against metallo-beta-lactamases), aztreonam (active against metallo-beta-lactamases alone), and cefiderocol (active against all major classes of beta-lactamases); the choices also include non-beta-lactam agents such as intravenous colistin or tigecycline (if no alternative is available). A single dose of oral fosfomycin may be used for uncomplicated cystitis. Generally, these agents are either less readily available in Hong Kong (beta-lactams)28 or may cause severe adverse effects (eg, nephrotoxicity for colistin and increased all-cause mortality for tigecycline).29

Piperacillin ± tazobactam and ticarcillin-clavulanate are commonly recommended for the treatment of P aeruginosa infections. Our data indicated susceptibility to piperacillin-tazobactam and a lack of susceptibility to ticarcillin-clavulanate. Thus, the use of ticarcillin-clavulanate should be supported by AST results. For serious infections, combination treatment (eg, beta-lactam and aminoglycoside) may be required to achieve synergistic effects.18

The prevalence of MRPA in our study was consistently low (0.0%-0.3%), consistent with data from public hospitals (0.02%-0.06% for 2014-2018).27 Data from other sources indicate higher prevalences of MRPA (eg, 12%-14% among blood isolates, according to the European Centre for Disease Prevention and Control).30 However, the definition of MRPA can vary among sources.31 For instance, the European Centre for Disease Prevention and Control uses combined resistance to three or more antibiotic groups. The strict definition of simultaneous resistance to four antibiotic classes used in Hong Kong may at least partially contribute to the overall low prevalence.

Acinetobacter can survive for prolonged periods in dry environments, which facilitates nosocomial transmission.32 Sulbactam-containing beta lactams are highly effective against Acinetobacter.18

Similar to MRPA, definitions of MDRA vary. In the UK, multi-resistant Acinetobacter spp or multi-resistant Acinetobacter baumannii (MRAB) demonstrate co-resistance to aminoglycosides and 3GC; the term MRAB-C refers to MRAB with carbapenem resistance.33 Using an MDRA definition identical to ours, public hospitals reported a decreasing MDRA prevalence (from 24% to 9% in 2014 to 201827); another study indicated that 0.6% of 1028 RCHE residents were carriers of MDRA.10 In analyses of carbapenem-resistant Acinetobacter alone, the prevalence in public hospitals ranged from 44% in 2014 to 53% in 201911; 9.1% of RCHE residents were carriers.11

Antibiotic-resistant Acinetobacter is classified as a ‘critical threat’ by the World Health Organization and an ‘urgent threat’ by the US Centers for Disease Control and Prevention. Thus, although its prevalence is decreasing, MDRA should be closely monitored for any rebound.

The primary treatments for invasive pneumococcal infection are beta-lactams (penicillin G or 3GC) for susceptible strains and vancomycin for penicillin-resistant strains (plus 3GC for meningitis).

In Europe, the prevalence of penicillin resistance among S pneumoniae isolates is approximately 12% to 14% (2015-2019, invasive isolates)30; the prevalence of macrolide resistance is approximately 14% to 16%. In Australia, these values are 3% to 6% and >20% to 25%, respectively.12 Our findings indicated a low NS percentage for penicillin but a very high NS percentage for macrolides; these findings are compatible with the recommendation that macrolides should not be used as monotherapy during empirical treatment of infections in Hong Kong.18 Fluoroquinolone resistance was previously reported to be high34 (>13.3% for levofloxacin), although recent data from laboratory surveillance by the CHP in the community setting indicate lower resistance (0.0%-4.4% in 2014-2019).9 Our data are similar to the community values, as expected for an organism that most commonly causes community-acquired pneumonia.18

Since the introduction of pneumococcal vaccination, the disease burden caused by penicillin- and erythromycin-resistant strains has decreased in the US.5 In Hong Kong, approximately 180 invasive pneumococcal infections are reported each year.35 Similar to other countries, Hong Kong has gradually made pneumococcal vaccination available to children, older adults, and high-risk individuals for >10 years.35 As vaccine coverage increases, it would be prudent to assess the changes in disease burden caused by resistant strains of pneumococcus.

Compared with public hospitals, private hospitals tend to have lower MDRO prevalences, particularly for MRSA and MDRA, while following an overall similar prevalence pattern (ie, increasing CRE, stable ESBL, decreasing MDRA, and negligible MRPA). Nonetheless, further MDRO monitoring (particularly for CRE and MDRA) is warranted.

There may be multiple reasons for the lower overall NS percentages, which could not be assessed using the data collected in this study (eg, case composition, antibiotic consumption, and diagnostic practices). However, the physical environment and isolation policy within private hospitals may contribute to a generally lower NS percentage. A key private hospital prescribes single-room isolation for all MDRO carriers with strict contact precautions.36 A more spacious environment with fewer beds per cubicle could theoretically lead to a lower cross-contamination rate through indirect contact (eg, by shared toilets), which is a main route for MDRO spread. With respect to staffing, the infection-control-nurse-to-bed ratio may be more likely to meet (personal communication) the level recommended by the CHP (1:150 for acute hospitals).37 Sufficient single-patient rooms and staffing (eg, nursing) are regarded as crucial components of efforts to reduce healthcare-associated colonisations and infections.38 39

Notably, the NS percentage was generally lower among out-patient isolates than among in-patient isolates, consistent with the reported literature.40

First, the AST data were stratified by both location (in- and out-patient) and specimen groups. The stratification of antibiogram data can facilitate antibiotic stewardship programmes by exposing important differences in susceptibility.41 Second, the collected data spanned a 6-year period with a large number of isolates, enabling the application of a consistent methodology that can enhance trend analysis accuracy. Third, MDRO prevalences were collected; such data are not required by the World Health Organization42 but are frequently regarded as key information in international surveillance reports.5 12 15 30

Cautious interpretation of the findings is necessary. First, a subset of the antibiotic-bacterium combinations were tested in a smaller proportion of isolates (<70%), which could have led to biased assessment. Second, because member hospital laboratories had different levels and types of accreditation, inter-laboratory practice variations could have influenced the AST results. Third, the specimen group classification was arbitrary. Fourth, differences in case composition among hospitals may lead to misleading conclusions if direct head-to-head comparison is performed. Finally, CRE was defined by susceptibility results, rather than specific tests for carbapenemase detection.

Our findings provide important insights concerning antibiotic resistance at private hospitals in Hong Kong. Although the overall situation in private hospitals is considered satisfactory, there remains a need for sustained efforts in resistance surveillance, infection control, and antibiotic stewardship.

Concept or design: L Lui.
Acquisition of data: L Lui
Analysis or interpretation of data: All authors.
Drafting of the manuscript: L Lui.
Critical revision of the manuscript for important intellectual content: All authors.

All authors had full access to the data, contributed to the study, approved the final version for publication, and take responsibility for its accuracy and integrity.

All authors have disclosed no conflicts of interest.

Infection Control Branch would like to express her appreciation to private hospitals for providing the AST data consistently over the years.

Membership of The Working Group of Collaboration between CHP and Private Hospitals on Safe Use of Antibiotics and Infection Control (in alphabetical order):
H Chen (Chairperson), Infection Control Branch, Centre for Health Protection, Department of Health, Hong Kong
Raymond WH Yung (Co-Chairperson), Hong Kong
Sanatorium & Hospital, Hong Kong
Ada Chan, Union Hospital, Hong Kong
WC Chan, Hong Kong Sanatorium & Hospital, Hong Kong
YM Cheng, Precious Blood Hospital (Caritas), Hong Kong
T Cheuk, Matilda International Hospital, Hong Kong
Christina Cheung, St Paul’s Hospital, Hong Kong
Eddie Cheung, Hong Kong Adventist Hospital–Stubbs Road, Hong Kong
Gary Cheung, Matilda International Hospital, Hong Kong
Joe Cheung, Hong Kong Adventist Hospital–Stubbs Road, Hong Kong
Billy SH Chui, Evangel Hospital, Hong Kong
August Fok, Hong Kong Adventist Hospital–Tsuen Wan, Hong Kong
Clara DK Kwok, Gleneagles Hospital Hong Kong, Hong Kong
Maggie MK Kwok, St Teresa’s Hospital, Hong Kong
Mooris Lai, Union Hospital, Hong Kong
Conita Lam, St Paul’s Hospital, Hong Kong
Wendy Lam, Canossa Hospital (Caritas), Hong Kong
MY Lau, Precious Blood Hospital (Caritas), Hong Kong
Patrick PL Lau, Hong Kong Baptist Hospital, Hong Kong
Andy Leung, Hong Kong Adventist Hospital–Tsuen Wan, Hong Kong
SL Loke, St Teresa’s Hospital, Hong Kong
L Lui, Infection Control Branch, Centre for Health Protection, Department of Health, Hong Kong
WH Seto, Gleneagles Hospital Hong Kong, Hong Kong
Winnie LH Wan, Evangel Hospital, Hong Kong
Cindy YY Wong, Hong Kong Baptist Hospital, Hong Kong
LC Wong, Infection Control Branch, Centre for Health Protection, Department of Health, Hong Kong
WO Wong, Canossa Hospital (Caritas), Hong Kong
KL Yan, Union Hospital, Hong Kong
PW Yu, Hong Kong Sanatorium & Hospital, Hong Kong
ST Yuen, St Paul’s Hospital, Hong Kong

This research received no specific grant from any funding agency in the public, commercial, or not-for-profit sectors.

This study was approved by the Hong Kong Department of Health Ethics Review Board (Ref: LM 275/2021). The requirement for patient consent was waived by the Ethics Review Board.

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