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Non-Susceptibility Trends Among Haemophilus Influenzae And Journal of Antimicrobial Chemotherapy (2008) 62, Suppl. 2, ii97–ii103 doi:10.1093/jac/dkn356 Non-susceptibility trends among Haemophilus influenzae and Moraxella catarrhalis from community-acquired respiratory tract infections in the UK and Ireland, 1999–2007 Ian Morrissey1*, Kirsty Maher1, Laura Williams1, Jemma Shackcloth1, David Felmingham1 Downloaded from https://academic.oup.com/jac/article/62/suppl_2/ii97/690887 by guest on 04 October 2021 and Rosy Reynolds2 on behalf of the BSAC Working Parties on Resistance Surveillance 1Quotient Bioresearch Limited, Microbiology, 7-9 William Road, London NW1 3ER, UK; 2Department of Medical Microbiology, Southmead Hospital, Southmead Road, Bristol BS10 5NB, UK Objectives: To determine the antimicrobial susceptibility of Haemophilus influenzae and Moraxella catarrhalis causing community-acquired respiratory tract infections in the UK and Ireland from 1999/ 2000 to 2006/07. Methods: Sentinel laboratories across the UK and Ireland contributed up to a fixed quota of isolates of defined organisms per annum. A central laboratory confirmed the isolates’ identities, measured MICs by the BSAC agar dilution method and undertook further testing by standard methods. The variability of the MIC method was assessed by repeated annual testing of control isolates. BSAC and EUCAST breakpoints were used. Statistical analysis adjusted for inter-centre variation by random effects logistic regression. Results: A total of 7371 H. influenzae and 2529 M. catarrhalis isolates were investigated. Over 90% of the H. influenzae isolates were susceptible to most of the antimicrobials tested, the exceptions being ampicillin (84.6% susceptible), trimethoprim (84.0%), cefuroxime (82.9%), amoxicillin (77.2%) and cefa- clor (11.7%). For M. catarrhalis, resistance was solely due to b-lactamase (prevalence over 91%) redu- cing susceptibility to penicillins only. There was little evidence of decreased antimicrobial susceptibility between 1999 and 2007 in either pathogen, except for a reduction in susceptibility to tri- methoprim in H. influenzae (90.3% to 82.6%, P < 0.00001). On the other hand, tetracycline susceptibility in H. influenzae increased over this period in the UK and Ireland (96.5 to 98.8%, P 5 0.00008). Conclusions: Despite increased resistance in respiratory pathogens from other parts of the world, the susceptibility of H. influenzae and M. catarrhalis to all agents, except tetracycline and trimethoprim in the case of H. influenzae, has remained constant during this longitudinal study. Keywords: resistance, surveillance, MIC, breakpoint Introduction H. influenzae had been found in the same hospital in 1974.3 Other reports from the same period acknowledge that ampicillin Haemophilus influenzae and Moraxella catarrhalis (formerly resistance was rare in the 1970s.4 Interestingly, another study Branhamella catarrhalis or Neisseria catarrhalis)areimportant found ampicillin resistance but not tetracycline resistance in a respiratory pathogens, with the former being the more prevalent collection of 40 H. influenzae isolates from the USA around the bacterium associated with community-acquired pneumonia and same time.5 During the 1970s there was no specific surveillance acute exacerbations of chronic obstructive airways disease, whereas programme like those that exist today, and it is unclear what the latter is found most commonly in patients with sinusitis.1 sampling and testing differences there may have been between Tetracycline resistance has been documented in H. influenzae the two studies discussed above. However, at that time, efforts since the early 1970s,2 with a small collection of USA isolates were beginning to be made to standardize susceptibility methods (n ¼ 35) from 1972 showing complete resistance to this agent.3 for use when testing H. influenzae.6 In that study, no isolate was found to be ampicillin-resistant, Between the mid-1970s and early 1990s, the susceptibility of although the authors state that some ampicillin-resistant UK isolates of H. influenzae was evaluated in a more formal ..................................................................................................................................................................................................................................................................................................................................................................................................................................... *Corresponding author. Tel: þ44-20-7388-7320; Fax: þ44-20-7388-7324; E-mail: [email protected] ..................................................................................................................................................................................................................................................................................................................................................................................................................................... ii97 # The Author 2008. Published by Oxford University Press on behalf of the British Society for Antimicrobial Chemotherapy. All rights reserved. For Permissions, please e-mail: [email protected] Morrissey et al. way at the London Hospital, led by the late Professor across the UK and Ireland submitted up to 50 S. pneumoniae and J. D. Williams. A collection of 952 H. influenzae isolates H. influenzae and 25 M. catarrhalis each winter (October–April) from from 1977 included 1.6% that were resistant to ampicillin (all of 1999 to 2007, excluding samples taken .48 h after hospitalization. these being b-lactamase-positive) and 2.7% resistant to tetra- These isolates were re-identified using standard methods, and MICs cycline.7 Repeat surveillance in 1981 (with a larger collection of and susceptibility were determined using BSAC standard methods. 1841 isolates) indicated that resistance to ampicillin in the UK had risen almost 4-fold to 6.2%, whereas tetracycline resis- 8 tance remained fairly static at 3.1%. Unlike in 1977, some Results b-lactamase-negative ampicillin-resistant (BLNAR) isolates were found (0.9% of all isolates), BLNAR being defined as Isolate numbers and patient demographics b-lactamase non-producing strains with ampicillin MIC 4 mg/ L.8–10 In 1986, further increases in ampicillin resistance were The numbers of H. influenzae and M. catarrhalis isolates tested observed (then at 7.8%), but the rise was not as dramatic as that and source data are shown in Table 1. Each pathogen had a seen between 1977 and 1981. BLNAR accounted for 1.6% of all group of core antibiotics that were tested each year, whereas Downloaded from https://academic.oup.com/jac/article/62/suppl_2/ii97/690887 by guest on 04 October 2021 H. influenzae in 1986, almost double that for 1981.9 Tetracycline other antibiotics were either excluded or introduced in more recent years. Both pathogens were investigated for the presence resistance was 2.7% in 1986, thus with little change from 1977, 25 despite complete resistance reported from a collection of 35 iso- of b-lactamase. The total collection of isolates included 7371 lates from a USA hospital (tetracycline, MIC range 6.3– H. influenzae and 2529 M. catarrhalis. Almost the entire collec- 12.5 mg/L) in 1972.3 The final study of the London Hospital tion of isolates originated from sputum samples (.93%). series, in 1991, showed a further increase in ampicillin resist- Throughout, patient characteristics were very similar for ance, up to 14.4%. The increase in BLNAR was even greater either pathogen year on year. Most isolates were from the 60–69 with these isolates and accounted for 5.8% of all H. influenzae year and 70–79 year old age groups (Table 1), and patients with in 1991. By this time, tetracycline resistance dropped 4-fold to either pathogen were approximately evenly split between female 1.4%.10 Two other studies of susceptibility in H. influenzae in and male (Table 1). Slightly more than 50% of the isolates origi- the UK were carried out in the mid-1990s,11,12 where amoxicil- nated from hospitalized patients (collected within 48 h of admis- lin resistance was around 16%, with b-lactamase prevalence sion), with most of the remainder from General Practice hardly changed since the early 1990s. Cefaclor resistance was (Table 1). Country of origin was also very similar for both 14% and clarithromycin resistance 4% in the mid-1990s.11,12 pathogens: 61% from England, 13% from Scotland, 11% from Tetracycline susceptibility was not assessed in either of these Wales, 10% from the Republic of Ireland and 5% from Northern studies. Ireland (data not shown). This is not surprising because collec- Unlike H. influenzae, M. catarrhalis was only recognized as tion targets were based on a set number of each isolate per a bacterial pathogen, rather than a commensal, in the mid-1970s country. All these characteristics did not alter significantly from and even as recently as the late 1980s was often still referred to year to year (statistical analysis not shown), with the exception as N. catarrhalis and dismissed as clinically irrelevant.13 Studies of care setting where in the last two seasons (2005/06 and 2006/ on penicillins in the 1960s suggest that this pathogen was sus- 07) a significantly higher proportion came from General Practice ceptible to ampicillin at that time.14 The first reported (56% of both pathogens compared with 40% to 44% for the first b-lactamase-producing M. catarrhalis were found in Sweden in six seasons). 1976, at a prevalence rate of 3.8%.15 A study
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