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Ireland at CRE crisis point

Clinicians warn that urgent action is required to ensure that carbapenem-resistant Enterobacteriaceae (CRE) do not become endemic in the Irish health system. Catherine Reilly reports

A ‘national emergency’ that is ‘spiralling out of control’.

Clinicians are describing the spread of carbapenem-resistant Enterobacteriaceae (CRE) in Ireland’s acute hospital system in such unequivocal terms.

Recent outbreaks of gram-negative bacteria resistant to the carbapenem class of antibiotics – the ‘drugs of last resort’ for life-threatening infections – have seriously impacted several acute hospitals and long-term care facilities (LTCFs) in Ireland.

The CRE subset carbapenemase-producing Enterobacteriaceae (CPE) – which are Enterobacteriaceae non-susceptible to carbapenem via production of a carbapenemase enzyme, and are of huge concern globally – have been implicated in Irish and international outbreaks. These carbapenemases include Klebsiella pneumoniae Carbapenemase (KPC), Verona Integron-encoded Metallo-β-lactamase (VIM), Oxacillinase-48-type carbapenemases (OXA-48) and New Delhi Metallo-β-lactamase (NDM).

On 24 August 2016, Tallaght Hospital notified a CRE outbreak to the HSE Department of Public Health-East. This CRE outbreak has constituted Ireland’s largest to date and involves OXA-48 CRE. In November 2016, an internal HSE document described the scale of the outbreak as “unprecedented” in Ireland. In the 18 months to February 2017, Tallaght says it treated 528,077 adult patients – 142 of whom were identified as carriers of CRE. Most affected patients were aged in their seventies, the Medical Independent (MI) understands.

Since 2015 there have been three invasive cases and no deaths “directly attributable” to CRE, according to the hospital. Cases are still occurring but the hospital says they have reduced substantially.

In December 2016 an outbreak of VIM CRE was notified by Mayo University Hospital (outbreak status has been since ‘stood down’). There were 11 colonisations and five invasive CRE cases over a period of 27 months, according to the Saolta University Health Care Group. Two patients died where CRE was identified as a contributing factor to their death. “None of them were acquired in Mayo University Hospital. The first case in 2014 with sepsis and the second case in November 2016 with multi-organ failure,” said the spokesperson.

In January 2017 St Luke’s Hospital, Kilkenny notified a “small contained outbreak” in a surgical ward (“it has ended”, stated Ireland East Hospital Group). University Hospital Waterford also experienced an outbreak in 2016, involving OXA-48 and NDM CRE, while an increase in CPE incidence is under investigation at St James’s Hospital Dublin as of March 2017.

Sporadic KPC CPE cases have continued to be identified in the midwest, where CRE may have become endemic (see panel page 5). There are also two LTCFs actively dealing with outbreaks: one in the northwest and the other in west Dublin. The latter is directly related to the Tallaght Hospital outbreak. Various types of CRE have circulated and not all of the recent outbreaks in Ireland would be inter-related.

Confirmed CPE cases have increased almost 10-fold from 2013 to 2016, according to statistics from the National Carbapenemase Producing Enterobacteriaceae Reference Laboratory(48 confirmed CPE cases in 2013; 81 in 2014; 140 in 2015; and 369 in 2016).

CRE outbreaks in Irish healthcare have principally involved colonisation (typically termed ‘CRE cases’); yet carriers serve as a reservoir that facilitate proliferation and increased risk of infection. Healthy people colonised with CRE would not usually suffer ill-effects. However, vulnerable patients in hospitals and other care facilities are at risk of bloodstream infection, particularly those requiring invasive medical devices, and CRE invasive infection is associated with mortality of over 50 per cent. In Ireland there have been deaths associated with CRE. The HSE, however, did not respond conclusively on a query as to whether it held such figures.

Records obtained by MI following a Freedom of Information (FoI) request to the HSE show that major manpower deficits, insufficient infrastructure and equipment, and a highly under-resourced and uncoordinated national response, brought Tallaght Hospital to the brink of effective closure as an acute care service.

The documentation also revealed laborious and complicated reporting lines within the upper echelons of the HSE and acute hospital network, limiting the capability for urgent and effective response.

Some three weeks after notification of the outbreak, Minister for Health Simon Harris was moved to ask Department officials – in an email sent on the night of 14 September – to find out “if there is an outbreak” of CRE at Tallaght Hospital. The hospital did not inform the Dublin Midlands Hospital Group (DMHG) about the outbreak until 14 September.

On 16 September, a note came through to the Department of Health, via HSE Acute Hospitals, from the Group. Two adult wards had been closed to admissions, the Group stated, and this would have a “temporary impact” on bed availability and elective admissions at the hospital.

Yet the impact at Tallaght was anything but temporary. Over the coming weeks, the hospital faced a huge battle to contain the rapidly evolving crisis.

The hospital stated that there were eight CRE cases in August 2016; this rose to 31 in September (and one invasive case) and 37 in October. In November, there were 25 cases (and one invasive case), 11 in December and nine in both January and February. Thousands of screenings have been undertaken: 9,891 from August 2016 to February 2017 inclusive, hitting a peak of 1,929 in November.

‘Major patient safety issue’

Irish health authorities have been well aware of the threat posed by CRE for several years, but it has not been high on an agenda dominated by more visible and relatable problems such as the trolley crisis and long hospital waiting lists. However, leading figures in Irish microbiology warn that this country is fast running out of time.

Dr Eleanor McNamara, President of the Irish Society of Clinical Microbiologists (ISCM), said the window of opportunity to stop CRE from becoming endemic in the hospital system is “diminishing rapidly”. The Society wrote to Minister Harris in July and October of 2016 requesting a meeting to discuss, update and advise him on the threat posed by CRE and risk mitigation interventions, but this request has not yet been realised.

Dr McNamara said there were recent ongoing outbreaks which were “nearly crippling” acute services. She said outbreak incidents can effectively “bring a hospital to its knees, and affect its ability to deliver the acute services that it is mandated to do”.

She added: “Overall, this is a major patient safety issue. As one of my colleagues had said, if we had an outbreak of blood-borne virus infections, acquired in hospitals, there would be a national outcry, and yet here we are having healthcare-associated infections occurring with an almost untreatable organism, and there isn’t an emergency national outbreak team being pulled together with dedicated resources.”

Dr McNamara emphasised that a longer-term strategic focus in parallel to an emergency response is equally as important. A national action plan on antimicrobial resistance (AMR) that is resourced, actioned and auditable is also an essential requirement, added Dr McNamara.

“We have had emergencies, like a few years ago, with Ebola and novel strains of influenza, and everybody knew about it. And plans were implemented. However, CRE is a global emergency of even greater significance in some respects than Ebola, because it is affecting everybody now – in health sectors across the world – and basically we are not getting that level of energy, attention and focused reaction to it,” added Dr McNamara.

“We need to have coordinated action – unfortunately at the moment it is all very uncoordinated,” added Dr McNamara on the current national efforts.

Prof Martin Cormican, Professor of Bacteriology at NUI Galway, told MI that “if we are to have any chance of controlling this, we need much more effective leadership from the Minister for Health and the Department of Health than we have seen to date”.

A number of Irish hospitals experiencing major outbreaks have “managed to limit spread” but at “considerable cost and disruption of service”.

More broadly, measures taken to date to control CPE “have not been effective overall”, he said.

“Although spread in hospitals is almost certainly the biggest problem at present, there has been spread in some nursing homes and it is likely that spread in homes and in the wider community and the environment are likely to become increasingly common as the problem continues to spiral out of control.”

Consultant Microbiologist Dr Rob Cunney, Clinical Lead for the HSE/RCPI Clinical Programme on Healthcare Associated Infections (HCAI) and AMR, agrees with colleagues that an urgent response is needed to prevent CRE becoming endemic, certainly in the hospital system.

The problem requires “a properly focused and resourced response”, along the lines of that adopted in Israel some years ago, when local measures failed.

A HSE spokesperson told MI there is a “work plan” produced by its Multi-Drug Resistant Organisms Taskforce [aka AMR/HCAI Taskforce] and a “proposal” to the HSE senior management team around “resource requirements for addressing CRE”. A national action plan on AMR is also being developed by the Department of Health and the Department of Agriculture, Food, and the Marine.

“[CRE] is something that is being taken very seriously by the [HSE] Leadership Team, much more than we have seen before. I am hoping that will translate into a properly resourced response,” Dr Cunney commented.


The crucial importance of clear lines of communication and escalation, and prompt access to emergency resourcing at a national level, are writ large when surveying the Tallaght crisis.

Several weeks after the outbreak notification, on 9 November 2016, a HSE Public Health report described Tallaght Hospital as “overwhelmed”.

It stated: “The hospital has been overwhelmed by this organism and efforts to contain it have been hindered by the contagiousness of this plasmid, the prolonged duration of colonisation, the inadequate number of single rooms, the lack of dedicated equipment, the inadequate [number of] clinical microbiologists, laboratory staff, infection control nurses and general nursing staff…”

Many hospitals throughout the country “have even fewer resources to deal with a situation like this and the country as a whole is extremely vulnerable”, it added.

In the early days following outbreak notification, finding funding for replacement mattresses for those that failed an audit was proving difficult. It was also recommended that dedicated staff provide care for CRE patients but this was “not possible due to financial and staff shortages”, according to a report from the HSE Department of Public Health-East on 23 September. Some agency staff were also refusing to work at Tallaght Hospital.

Longstanding CRE problem in midwest

A “particular problem” with CRE exists in the midwest region “at large”, which is reflected in the hospital population, according to the HSE.

There were 31 new CRE detections across the UL Hospitals Group in 2016, and no invasive bloodstream infections, stated the Group. There were 60 new CRE detections across the Group during 2015.

“With large ‘Nightingale’ wards the norm in the older parts of the building, managing contacts between patients carrying CRE and others remains a challenge.”

The UL Hospitals Group refurbished an inpatient ward at a cost of €400,000 to facilitate an infection prevention and control “cohort ward”; it refurbished another ward, at a cost of €300,000, at UHL due to infection prevention and control “concerns”, including replacement of infrastructure such as sinks; it says it has also invested in additional cleaning and deep cleaning measures.

“ULH has developed a quality improvement plan in regard to CRE, which incorporates much of the NHS Toolkit for the Control of CRE 2013. This includes an intensive screening programme; use of an isolation ward for newly detected or known positive patients to reduce the risk of cross-transmission; flagging all CRE positive and CRE contacts through the management, surveillance and reporting software ICNet; and reporting new cases appropriately through the microbiology team.”

More complex antibiotics are referred to the microbiology team before being prescribed, says the Group.

Nevertheless, there have been concerns expressed about management of CRE at UHL. In summer 2015, Clinical Lead for the HSE/RCPI Clinical Programme on HCAI/AMR Dr Rob Cunney visited the hospital. He reported to senior HSE management about “issues relating to resources, clinical and corporate governance, and cross-divisional governance that appear to be contributing to the ongoing outbreak”.

The report by Dr Cunney and a colleague, dated July 2015, described how “the current CRE outbreak in UHL and surrounding areas is already a major patient safety issue”.

The report noted that there had been 87 cases of CRE colonisation detected at UHL, of which 22 had resulted in CRE infection, with at least two deaths related to CRE infection.

The outbreak was being sustained due to transmission in community settings, with further transmission in UHL facilitated by infrastructural, staffing and procedural issues.

The infection prevention and control team at UHL had made huge efforts to put in place control measures and their workload was “immense”.

The report also referred to high levels of broad spectrum antibiotic use and “lack of ownership” of the CRE response by clinicians and senior management.

It noted that the extent of CRE may be underestimated across other acute and non-acute settings due to limitations in surveillance and screening in line with national guidance.

In response to the paper, CEO of UL Hospitals Group, Prof Colette Cowan outlined the measures taken to date and said it continued to “utilise every opportunity to stem the spread of CRE”.


There are numerous entities involved in tackling AMR/HCAI, but no single responsible body with a clear, and adequately resourced, lead operational remit in the case of outbreak.

The HSE’s Multi-Drug Resistant Organisms Taskforce does not have an operational role in response to outbreaks. The HSE/RCPI Clinical Programme, clinically led by Dr Cunney, devises quality improvement projects focused on hand hygiene, device related infection and antibiotic stewardship.

The HPSC is responsible for coordinating national surveillance of CRE (including CRE outbreaks), and providing operational support for the management of outbreaks where required. HSE Departments of Public Health are responsible for coordinating regional surveillance, providing operational support for management of outbreaks or, in some cases, leading outbreak control teams depending on the outbreak setting.

The Clinical Programme sits under the HSE Quality Improvement Division, while the HPSC and public health departments are under the remit of the HSE Health and Wellbeing Division.

The HSE said there are two separate reporting mechanisms in the public hospital network for escalation of CRE outbreaks.

Firstly, all hospital outbreaks are required to be notified to the local HSE Department of Public Health and, from there, to the HPSC. Secondly, hospitals and community healthcare institutions “can escalate issues relating to CRE, or other HCAI, via the HSE Accountability Framework” (eg, from hospital to Hospital Group to HSE Acute Care Division to HSE Senior Management Team). Therefore, in the case of a hospital outbreak, the corporate line of accountability runs from the hospital CEO/general manager reporting to the CEO of the Hospital Group reporting to the divisional lead of Acute Hospitals.

Neither the HSE National Office for Health and Wellbeing nor Quality Improvement Division have a formal role in the escalation or reporting of outbreaks, according to the HSE. By press time, the HSE had not confirmed when Director General Mr Tony O’Brien was informed of the Tallaght Hospital outbreak by HSE managers*.

‘Not under control’

On 22 September 2016, just over a week on from Minister Harris’s internal Department enquiry as to whether there was an outbreak at Tallaght Hospital, Consultant Microbiologist at the HPSC Dr Karen Burns informed senior HSE managers: “We all need to be clear that this outbreak is not under control.”

The hospital was detecting approximately one new patient per day, with around 40 patients to date and 14 inpatients affected at the time of Dr Burns’s note. It was likely to “go on for a protracted period of time” and there was a “significant risk that a similar situation to Limerick is likely to evolve, whereby screening will continue to detect patients returning to the hospital who picked up CRE on an earlier admission”.

Dr Burns made reference to stretched manpower in crucial areas at Tallaght Hospital and in the HPSC, which has only 0.5 WTE consultant microbiologists (the recruitment process is still “ongoing” for a 0.5 WTE consultant microbiologist to cover a seconded staff member, according to the HSE. The HPSC is also still attempting to fill the position of Director following the retirement of Dr Darina O’Flanagan in May 2016).

In his reply to Dr Burns, and HSE colleagues, HSE Director of Quality Improvement Dr Philip Crowley said the situation showed “how thin the national resource is in this area”.

After visiting Tallaght Hospital, Dr Burns reported on 27 September that there were 16 inpatients with known CRE: nine were accommodated in a ward that was fully single en-suite and six were in isolation on a second ward.

“One patient was transferred to ICU last night and is being treated for CRE infection. Contacts of known CRE cases are being screened for CRE carriage. There are approximately 47 confirmed patients with CRE in the year to date…we suspect that this issue may have started in the hospital during Q4 2015 and grumbled on at a low level, prior to being identified and notified as an outbreak this August.”

Throughout the crisis, there appeared to be a complicated chain of escalation and information sharing among senior HSE management. On 28 September, for example, Director of Health and Wellbeing Dr Stephanie O’Keeffe, referred to “a lot of traffic on this and need to be careful it is being directed in the right way”.

On 5 October, Dr Burns of the HPSC reported to senior HSE management of further concerns following a visit to the hospital. She wrote that there was nothing to indicate to the general public visiting the hospital that there was an ongoing outbreak.

“There has been no formal media communication from the hospital to advise people to attend only if absolutely necessary,” she added.

Moreover it was not always clear to healthcare professionals, including doctors, which patients had CRE.

On 27 October, as the hospital examined alternatives to ensure patients could access scheduled care, a CRE Outbreak Meeting at Tallaght Hospital – which included hospital management, HSE, DMHG and HPSC representatives – heard that private hospitals had raised concerns regarding accepting CRE patients. It was also noted at this meeting that “other hospitals are not following national guidelines”, which MI understands as a reference to the Guidelines for the Prevention and Control of Multi-drug resistant organisms (MDRO) excluding MRSA in the healthcare setting, which outlines screening protocols.

At this meeting, CEO of the hospital Mr David Slevin advised of the need to screen five nursing homes (as of mid-March 2017, the HSE has commenced screening in one of these nursing homes. Tallaght Hospital’s laboratory has facilitated this by processing the samples).

The HSE Public Health report of 9 November 2016 noted that there had been 79 cases of CRE at Tallaght Hospital from July to the end of October 2016 (and 91 in total for 2016).

There were 32 CRE positive inpatients on six wards, all in isolation as of 9 November, according to the HSE document. Furthermore, there were 52 CRE contacts cohorted on 12 wards. Eight beds were blocked due to cohorting of CRE contacts.

The HSE report noted that many patients had tested positive for more than one OXA-48-like positive bacterial species. “As a result there is no defined bacterial species or antiobiogram associated with this outbreak which hindered the initial recognition of the situation.” Another characteristic that contributed to the spread “was the time taken for contacts to become culture positive which can take up to four weeks”.

Of the CRE cases when first positive samples were taken (January 2015-October 2016), most were on the Crampton, Gogarty and Lynn wards. Five were in the ITU and four in the CCU.

The infection control nurse staffing levels were 3.3 whole-time equivalents for 430 beds. They were at “breaking point”, according to the HSE document, and there did not appear to be qualified staff available to hire. The hospital had just 1.7 WTE consultant microbiologists. Furthermore, the most recent hand hygiene audits for September 2016, during the outbreak, did not achieve 90 per cent compliance (the HSE-mandated KPI).

There had been instances of more than three days to isolate a CRE patient, while there were regularly more than 10 beds blocked due to cohorting and isolation and, on one day, 45 beds were blocked. Moreover, while weekly screen of high risk patients (ICU, haematology, oncology, renal, dialysis, major GI or vascular surgery, trauma and orthopaedics) was recommended as a control measure “it is not yet in place for all areas due to the burden of testing”.

According to the report, the only way to prevent the spread of CRE nationally would be to follow the Israeli example (Schwaber et al, 2011) of a “properly funded national taskforce along with a plan and the funding to improve the national hospital infrastructure and bring it in line with HIQA standards for the prevention of healthcare associated infections”.

 ‘National concern’

By the middle of November, it appeared that HSE Acute Hospitals was managing to commit to, and coordinate, a number of measures to assist Tallaght, and the exhaustive efforts of key hospital staff were making some headway. The DMHG said its management team “helped secure funding for essential diagnosing equipment and works”.However, towards the end of 2016, Mayo University Hospital notified an outbreak involving a different type of CRE.

On 19 December, in an email to HSE Director of Health and Wellbeing Dr O’Keeffe, Director of Quality Improvement Dr Crowley and Director of Acute Hospitals Mr Liam Woods, and colleagues, Dr Burns of the HPSC described the “evolving situation” in Mayo as highlighting that “CRE is a public health emergency of national concern”.

Dr Burns was providing advice to the hospital’s recently appointed consultant microbiologist.

The outbreak may have begun much earlier than the date it was notified to Public Health on 2 December, she reported. There had been cases in the ICU, orthopaedic ward, a medical ward, a paediatric case and a dialysis patient. Screening had been limited to the ICU, haematology and oncology, with resourcing issues involved.

“It is a VIM type, which is unusual in Ireland to date and indicates that there may be a significant local VIM problem which has evolved unchecked,” wrote Dr Burns.

Meanwhile, by early 2017, CRE remained an ongoing concern at Tallaght Hospital. According to the hospital, the HSE made a “significant contribution” to its additional funding requirements to manage this situation in 2016. Discussions to provide additional funding for 2017 are ongoing with the HSE.

Tallaght Hospital said it had two WTE consultant microbiologists in early August 2016, increasing to 2.7 later that month.  Troublingly, the current figure is “temporarily” at 1.8 WTE “due to a full-time retirement”, with a replacement due to begin in June.  “A consultant working 0.1 WTE has been appointed to help with clinical work and antimicrobial stewardship.”

The number of WTE infection control nurses in August 2016 was 3.3 and is now 4.1, according to the hospital.

Tallaght Hospital now has two molecular systems running for the detection of CRE – the Genexpert system, which gives a result in about an hour, has been used for new patient admissions since 28 November 2016.  The Flowflex system, which can process 96 samples every five hours, has been run every day at a set time since 19 December 2016 “as part of routine screening of patients”.

The hospital requires specialised software to manage hospital infections and is using a temporary in-house IT solution for tracking CRE cases. It also “has plans to develop a new 72-bed unit, which will assist staff in managing such infections in the future”.


MI understands that Tallaght Hospital has high use of third generation cephalosporins, fluoroquinolones and carbapenems. Experts agree that appropriate antibiotic prescribing is a key feature of tackling AMR. Some hospitals have invested more than others in antimicrobial stewardship, noted Dr Cunney of the Clinical Programme.

In May, the HPSC will coordinate a national point prevalence survey (PPS) of hospital-acquired infections and antimicrobial use, as part of a European-wide PPS. The recently published PPS for LTCFs found that, of 10,044 LTCF residents who were counted, some 981 were prescribed antibiotics.

Dr Cunney said there are high levels of antibiotic use in Irish nursing homes, and the indication is often not clear. He emphasised the need for establishment of resourced antimicrobial stewardship teams in the community.

At the ISCM, Dr McNamara agrees that both stewardship teams and consultant microbiologists overseeing infection control/AMR activities in the community are badly needed.

Dr McNamara also underlined that Ireland needs to develop its eHealth national capabilities urgently. She said it was difficult to fathom that national e-prescribing is not in place in the acute hospital system, given its capability of real-time monitoring of antibiotic prescribing and the wider issue of reducing medication-related errors.

Dr McNamara said patients are being transferred between acute hospitals and also from primary care settings without knowledge of their CRE carrier status. She said it is essential to find out which patients are affected by CRE.

“However the whole issue of CRE screening is challenging, labour intensive and costly,” she continued. “The laboratories haven’t been resourced for it, and methods are complex. The logistics of identifying the patients for screening, then resourcing to do the screen, and communicating of the results, particularly across hospitals, is really difficult.”

A national electronic healthcare record (EHR) would assist significantly with surveillance and management of issues such as CRE, the HSE’s Chief Information Officer Mr Richard Corbridge told MI.  The EHR business case is still with the Department of Health for consideration after approval by the HSE last summer.


In response to the increased incidence of CRE in Ireland and associated outbreaks during 2016, voluntary enhanced CRE surveillance scheme was discontinued at the end of last year.

Effective from January 2017, all Irish microbiology labs are required to report information directly to the HPSC on a quarterly basis (the HPSC will be publishing quarterly reports).

Meanwhile, HIQA intends to “continue to closely monitor this situation during 2017, through the undertaking of a revised approach to monitoring against the National Standards for the Prevention and Control of Healthcare Associated Infection and we will be publishing a guidance document on this in the coming months”.

*After the Medical Independent (MI) went to press, the HSE provided the following comment on when growing concerns about CRE were escalated to HSE DG Mr Tony O’Brien:

“The National Directors of Health and Wellbeing and Acute Services proposed, on behalf of the National HCAI/AMR Taskforce, the need for a national coordinated response to CPE outbreaks at the January meeting of the Leadership Team. A paper prepared by the Clinical Programme for HCAI/AMR in December 2016 informed these discussions.

“The Leadership Team requested a detailed report on the actions required to address CPE in the healthcare system, along with relevant costings, for consideration at a further Leadership Team meeting. A report outlining a series of priority actions was presented to the Leadership Team at their meeting in March 2017. This proposed response was approved subject to some further work on costings.”


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