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Antimicrobial Resistance (AMR) Surveillance in Public Hospitals and Clinics - Hospital Authority AMR Data (2022)

Release date: 17 April 2024

Background

The HKSAR Government attaches great importance to the threat of antimicrobial resistance (AMR). A High Level Steering Committee (HLSC) chaired by the Secretary for Health has been established to formulate strategies and implement actions to combat AMR in Hong Kong. The second Hong Kong Strategy and Action Plan on Antimicrobial Resistance (2023 - 2027) (Action Plan) was issued in November 2022.

The Action Plan sets out monitoring of situation of AMR as one of the strategic actions. Strategic intervention 1.2.1 of the Action Plan recommended to continue AMR surveillance based on the Global Antimicrobial Resistance Surveillance System (GLASS), developed by the World Health Organization (WHO). As such, microbiological data with antimicrobial susceptibility test (AST) results of patients from public hospitals and clinic of the Hospital Authority (HA) were collected and analysed. Since the first Action Plan on AMR was published in 2017, the situation of 2016 has been chosen as the baseline for comparison. One-way Cochran-Armitage test was used to look for trends from 2016 to 2022. P-value of less than 0.05 was considered statistically significant.

This is the sixth report which includes the findings of blood, urine and stool specimens from year 2016 to 2022.




Method

Surveillance was conducted following the recommendations of the WHO GLASS Manual for Early Implementation (2015) with areas of local adaptation as summarised below:

  • Six WHO priority organisms, namely Escherichia coli, Klebsiella pneumoniae, Staphylococcus aureus, Salmonella species (spp.), Acinetobacter spp. and Streptococcus pneumoniae were reported.
  • Location of onset was classified as community-onset (CO) (organism isolated from blood specimen collected in non-inpatient services or within 48 hours after hospital admission) or hospital-onset (HO) (organism isolated from blood specimen collected more than 48 hours after hospital admission). As Salmonella spp. and Streptococcus pneumoniae rarely cause hospital-associated infections, related antimicrobial susceptibility test (AST) results were interpreted as “community (undifferentiated) onset”.
  • For each surveillance period (one calendar year), only the first result would be reported for each patient per specimen type per organism for the same location of onset.
  • AST result being “Intermediate” or “Resistant” was considered “Non-susceptible”, while AST results derived from less than ten isolates per calendar year were excluded from the analysis.
  • To avoid misleading or interference by selection bias, percentages of non-susceptibility[1] (NS%) derived from less than 70% of total isolates were not reported (or remarked to remind readers to interpret with caution).
  • Positive cultures for the same organism within 14 days from the same patient would be regarded as a single episode even if the first was of CO while the second or the rest were of HO (“Day-14” rule).

This report adopts the revised fluoroquinolones interpretive criteria for Enterobacterales[2] (excluding Salmonella spp.) released by the Clinical and Laboratory Standards Institute in its CLSI Guideline in 2019, and the revised piperacillin / tazobactam interpretive criteria for Enterobacterales in 2022.

Where appropriate, AST results for broad-spectrum antimicrobials identified by experts in HA (“Big Guns”) were examined because of their importance in treating resistant infections. For Salmonella spp. and Streptococcus pneumoniae, since infections caused by these organisms are usually treated by first-line antimicrobials, NS% of respective first-line antimicrobials were reported.


Results

Overview of patients with blood culture

The number of patients with blood culture slightly increased from 140,000 in 2021 to 145,000 in 2022. Amongst patients with blood culture collected each year, over 50% aged 65 years or above. The percentage of patients with positive blood culture remained stable from 2016 to 2022 (around 10-11%).

Overview of WHO priority organisms isolated from blood (by applying WHO GLASS definition on location of onset)

The overall distribution of the six WHO priority organisms cultured from blood was similar from 2016 to 2022, with the three commonest organisms in 2022 being Escherichia coli, Klebsiella pneumoniae and Staphylococcus aureus (isolated from 37.1%, 13.6% and 12.9% of patients with positive blood culture respectively). The case count for Streptococcus pneumoniae (<50 cases), Salmonella spp. (about 200 cases) and Acinetobacter spp. (about 200 cases) remained low and stable. Regarding the location of onset, Escherichia coli, Klebsiella pneumoniae, Salmonella spp. and Streptococcus pneumoniae were predominantly CO, while Acinetobacter spp. was predominantly HO. More than half of Staphylococcus aureus isolated were CO.

In general, continual downward trends on non-susceptibility on some antimicrobials for the WHO priority organisms were observed in 2022. Below summarises the overall pattern of non-susceptibility on antimicrobials as of end-2022.

Antimicrobial susceptibility test results for WHO priority organisms

Escherichia coli

In 2022, continuous downward trends with mild increase were observed for ceftazidime (HO: 23.2% in 2021→20.3% in 2022), cefepime (CO: 23.6%→16.1%; HO: 33.1%→21.4%) and gentamicin (CO: 28.9%→24.1%; HO: 35.3%→30.4%) when compared with baseline in 2016. For community-onset Escherichia coli bacteraemia, although an increasing trend was still seen for several antimicrobials, steady state maintained for the NS% of cefuroxime (CO: 30.1%→31.5%) and cefotaxime (CO: 27.8%→28.9%). Meanwhile, the NS% for amikacin (CO: 0.7%→1.2%) and ertapenem (CO: 0.1%→0.2%) showed an increasing trend for the first time since the beginning of surveillance (2016 – 2022).

Klebsiella pneumoniae

Despite decreasing trend was observed for cefepime during 16-20 (CO: 8.4%→5.5%) and 16-21 (CO: 8.4%→5.6%), a mild rebounce in the NS% was observed for cefepime (CO: 8.4%→6.8% & HO: 20.3%→22.7%). At the same time, rebounce in the NS% for gentamicin (CO: 5.5%→5.2% & HO: 14.6%→15.5%) was also observed. For hospital-onset cases, the increasing trends for meropenem (HO: 1.2%→4.0%), ertapenem (HO: 2.9%→5.0%) and imipenem (HO: 1.3%→6.8%) have plateaued since 2021. For community-onset case, the NS% for imipenem (CO: 0.2%→1.3%) and amikacin (CO: 0.3%→0.6%) showed increasing trend for the first time since the beginning of surveillance (2016 – 2022).

Staphylococcus aureus

No significant change in trend was observed for Staphylococcus aureus isolated from blood. The NS% for oxacillin[3] remains high at 40% for CO isolates and 56% for HO isolates from 2016 to 2022.

Salmonella species

An increasing trend was observed for ampicillin (62.4%→76.8%) in 2016 – 2021 and 2016 – 2022. On the other hand, the NS% for cefotaxime (6.9%→3.5%), cefoperazone/sulbactam (5.9%→0.0%), imipenem (remained 0%) and azithronycin (5.8%→1.6%) remained <10% with decreasing trend observed from 2016 to 2022. However, these findings should be interpreted with caution as less than 70% of the isolates were tested.

Acinetobacter species

Increasing trends were observed in 2016 – 2021 and 2016 – 2022 for amikacin (HO: 21.5%→38.6%), ampicillin/ sulbactam (HO: 52.5%→72.9%), gentamicin (HO: 27.9%→44.8%), imipenem (HO: 60.2%→78.9%), meropenem (HO: 59%→80.3%) and levofloxacin (HO: 55.7%→76.5%). At the same time, the NS% for piperacillin/ tazobactam (HO: 63.6%→79.5%), ceftazidime (HO: 38.4%→48.2%), cefoperazone/ sulbactam (HO: 55.6%→73.0%) and cefepime (HO: 67.2%→78.9%) showed increasing trend for the first time since the beginning of surveillance (2016 – 2022).

Streptococcus pneumoniae

Increasing trends were observed for cefotaxime (0.9%→9.5%) and penicillin (0.7%→4.2%) in 2016 – 2021 and 2016 – 2022.


Recommendations

The NS% on antimicrobials for Escherichia coli and Klebsiella pneumoniae continued to decrease from 2021 to 2022. Besides, the NS% on some drug-bug combinations were peaked in 2021 and reduced in 2022 (such as Amoxicillin/ clavulanate isolated from blood for hospital-onset Klebsiella pneumoniae bacteraemia). Antibiotic Stewardship Programme (ASP) in public hospitals should be continued and promoted, aiming to optimize the use of antibiotics by providing evidence-based antibiotic prescription guidance for common infections. (Objective 6 of the Hong Kong Strategy and Action Plan on AMR 2023-2027), Meanwhile, sustained attention should be paid to emerging drug-bug combinations that showed increasing resistance against especially, the “Big Guns” such as:

  • Acinetobacter spp. – piperacillin/ tazobactam (community-onset and hospital-onset bacteraemia), ceftazidime (community-onset and hospital-onset bacteraemia), cefoperazone/ sulbactam (community-onset and hospital-onset bacteraemia) & cefepime (Isolated from blood for hospital-onset bacteraemia)

The above findings/trend have been disseminated to working partners of HA for management as appropriate.


[1] Non-susceptibility percentage means the proportion of isolates tested for susceptibility to a particular antimicrobial, with the test result being non-susceptible.

[2] The family previously known as Enterobacteriaceae is now classified under the new order Enterobacterales. This change was documented in the Manual of Clinical Microbiology, 12th ed., chapter 40 and the 2019 European Committee on Antimicrobial Susceptibility Testing (EUCAST) breakpoint tables.

[3] Sensitivity testing results of penicillinase stable penicillins (oxacillin, cloxacillin and methicillin) and cefoxitin towards Staphylococcus aureus were collectively grouped as oxacillin following the recommendation of CLSI.




Method

Surveillance was conducted following the recommendations of the WHO GLASS Manual for Early Implementation (2015) with areas of local adaptation as summarised below:

  • Two WHO priority organisms, namely Escherichia coli and Klebsiella pneumoniae were reported.
  • Location of onset was classified as community-onset (CO) (organism isolated from urine specimen collected in non-inpatient services or within 48 hours after hospital admission) or hospital-onset (HO) (organism isolated from urine specimen collected more than 48 hours after hospital admission).
  • For each surveillance period (one calendar year), only the first result would be reported for each patient per specimen type per organism for the same location of onset.
  • Antimicrobial susceptibility test (AST) result being “Intermediate” or “Resistant” was considered “Non-susceptible”, while AST results derived from less than ten isolates per calendar year were excluded from the analysis.
  • Only midstream urine specimens were included for analysis, and positive urine culture was defined as specimen with pure growth of organism reaching bacterial count which was equal to or greater than 105 colony-forming units per millilitre (cfu/ml).
  • To avoid misleading or interference by selection bias, percentages of non-susceptibility[1] (NS%) derived from less than 70% of total isolates were not reported (or remarked to remind readers to interpret with caution).

This report adopts the revised fluoroquinolones interpretive criteria for Enterobacterales[2] (excluding Salmonella spp.) released by the Clinical and Laboratory Standards Institute in its CLSI Guideline in 2019, and the revised piperacillin / tazobactam interpretive criteria for Enterobacterales in 2022.

Where appropriate, AST results for broad-spectrum antimicrobials identified by experts in HA (“Big Guns”) were examined because of their importance in treating resistant infections.


Results

Overview of patients with urine culture

The total number of patients with urine culture collected decreased from around 331,000 in 2021 to 299,000 in 2022 (9.7% decrease). The percentage of patients with positive urine culture remained stable over the past years at around 14 – 15%.

Overview of WHO priority organisms isolated from urine (by applying WHO GLASS definition on location of onset)

The overall distribution of the two WHO priority organisms cultured from urine was similar from 2016 to 2022. The commonest organism isolated from urine in 2022 was Escherichia coli. Regarding the location of onset, Escherichia coli and Klebsiella pneumonia were predominantly CO.

Antimicrobial susceptibility test results for WHO priority organisms

Escherichia coli

The decreasing trend for cefuroxime (IV) (CO: 24.7%→23.9%), cefuroxime (oral) (CO: 50.7%→42.5%; HO: 61%→53.4%), co-trimoxazole (CO: 39.2%→30.9%; HO: 45.4%→39.7%) and nitrofurantoin (CO: 2.9%→1.3%; HO: 4.3%→1.3%) continued to be observed in 2022 when compared to baseline in 2016. However, the NS% for amoxicillin/ clavulanate fluctuated in the community-onset (CO: 19.6%→20.5%) while it showed an increasing trend in the hospital-onset (HO: 27.5%→29.5%) for the first time since the beginning of surveillance for 2016 – 2022.

Klebsiella pneumoniae

Downward trends were continuously observed for cefuroxime (oral) (CO: 46.6%→34.7%; HO: 49.6%→44.9%), co-trimoxazole (CO: 25.1%→19.3%; HO: 37.0%→28.3%) and nitrofurantoin (CO: 49.9%→39.5%; HO: 54.2%→39.9%) in both community-onset and hospital-onset for 2016 – 2022.


Recommendations

Overall, the decreasing trends of non-susceptibility could maintain for both Escherichia coli and Klebsiella pneumoniae towards most antimicrobials while new increasing trend such as the rebound of non-susceptibility of hospital-onset Escherichia coli infection against amoxicillin/ clavulanate was observed, further monitoring would be continued.  The above findings were shared with working partners of HA for their further investigation and management as appropriate.


[1] Non-susceptibility percentage means the proportion of isolates tested for susceptibility to a particular antimicrobial, with the test result being non-susceptible.

[2] The family previously known as Enterobacteriaceae is now classified under the new order Enterobacterales. This change was documented in the Manual of Clinical Microbiology, 12th ed., chapter 40 and the 2019 European Committee on Antimicrobial Susceptibility Testing (EUCAST) breakpoint tables.




Method

Surveillance was conducted following the recommendations of the WHO GLASS Manual for Early Implementation (2015) with areas of local adaptation as summarised below:

  • Two WHO priority organisms, namely Salmonella spp. and Shigella spp. were reported.
  • Location of onset would be collectively considered as “Community (undifferentiated)-onset” as a whole instead of adopting the definition by WHO (which defines specimens collected 2 calendar days after hospital admission as hospital-onset) as infections caused by these organisms are mostly community-associated and rarely are hospital-associated.
  • For each surveillance period (one calendar year), only the first result would be reported for each patient per specimen type per organism for the same location of onset.
  • Antimicrobial susceptibility test (AST) result being “Intermediate” or “Resistant” was considered “Non-susceptible”, while AST results derived from less than ten isolates per calendar year were excluded from the analysis.
  • To avoid misleading or interference by selection bias, percentages of non-susceptibility[1] (NS%) derived from less than 70% of total isolates were not reported (or remarked to remind readers to interpret with caution).

This report adopts the revised fluoroquinolones interpretive criteria for Enterobacterales[2] (excluding Salmonella spp.) released by the Clinical and Laboratory Standards Institute in its CLSI Guideline in 2019, and the revised piperacillin / tazobactam interpretive criteria for Enterobacterales in 2022.


Results

Overview of patients with stool culture

The total number of patients with stool culture collected increased from around 44,000 in 2021 to 37,000 in 2022 (15.9% decrease). The percentage of patients with positive stool culture remained stable over the past years at around 10%.

Overview of WHO priority organisms isolated from stool (by applying WHO GLASS definition on location of onset)

The overall distribution of the two WHO priority organisms cultured from stool was similar since start of surveillance in 2016. The commonest organism isolated from stool in 2022 was Salmonella spp.

Antimicrobial susceptibility test results for WHO priority organisms

Salmonella spp.

A continual increasing trends were observed for NS% ampicillin (CO: 59.9%→71.6%) and ciprofloxacin (CO: 52.1%→59.1%) in 2016 – 2021 and 2016 – 2022. However, NS% for ceftriaxone continued to rebound in 2022 when compared with the trough in 2020 while the decreasing trend was no longer observed in 2022.

Shigella spp.

Decreasing trends were seen for ampicillin (57.6%→41.7%) and co-trimoxazole (81.8%→58.3%) in 2016 – 2021 and 2016 – 2022.


Recommendations

In view of statistically significant increasing trend of non-susceptibility for isolates of Salmonella spp. towards ampicillin and ciprofloxacin, further monitoring would be warranted.  The above findings/trend have been disseminated to working partners of HA for management as appropriate.


[1] Non-susceptibility percentage means the proportion of isolates tested for susceptibility to a particular antimicrobial, with the test result being non-susceptible.

[2] The family previously known as Enterobacteriaceae is now classified under the new order Enterobacterales. This change was documented in the Manual of Clinical Microbiology, 12th ed., chapter 40 and the 2019 European Committee on Antimicrobial Susceptibility Testing (EUCAST) breakpoint tables.

Acknowledgement

We would like to acknowledge stakeholders from HA, including the Information Technology & Health Informatics Division, Quality and Safety Division, Strategy and Planning Division, and various Working Groups for the provision of input and comment to facilitate the compilation of findings for the year 2022.