VULNERABLE patients with cancers such as leukaemia were "exposed to risk that could have been lower" if Glasgow's superhospital had been designed and built correctly, investigators have found.
However, the long-awaited review into the £842 million Queen Elizabeth University Hospital (QEUH) and Royal Hospital for Children (RHC) concluded that there is "no clear evidence" linking these failures to avoidable deaths.
It also finds no clear link between cases of Cryptococcus fungal infection found in two cancer patients who died, and the presence of pigeons on the campus.
Cryptococcus neoformans is a pathogen found widely in the environment, often in bird droppings, that can be harmful to people with compromised immune systems.
It was originally believed that the pigeon droppings in a plant room on the 12th floor may have led the fungus to enter the hospital's ventilation system, leading at-risk patients to inhale contaminated air.
However, investigators say there is "not a sound evidential basis" to link the patients' infections and subsequent deaths to "the presence or proximity of pigeons or their excrement".
The report states: "In the specific instance of the pigeon and excrement found in the hospital near an air inlet, we understand that where the pigeon remains were found does not match the air systems supplying specific parts of the hospital where certain patients affected by one microorganism (Cryptococcus) spent much of their in-patient care.
"The presence of pigeons within or in the vicinity of the hospital, or defects on the building that would allow the entry of a pigeon or other bird carrying a specific organism capable of causing a serious infection in a vulnerable person are not sufficient to establish a strong association or causative link."
The independent probe, chaired by Dr Andrew Fraser and Dr Brian Montgomery, was commissioned by Health Secretary Jeane Freeman in January 2019 following the deaths of three patients who had contracted unusual infections during treatment.
A 10-year-old boy who was being treated for blood cancer at the QEUH was the first to die in December 2019, with a post-mortem indicating that a infection with Cryptoccocus neoformans was a contributory factor in his death.
READ MORE: Crown Office invesitgating death of boy, 10, who contracted infection linked to pigeon droppings
In January 2019, 73-year-old cancer patient Gail Armstong who had tested positive for the bug during treatment at the QEUH in November 2018 - before being discharged for palliative care - also died.
The infection was said not to have been a factor in the grandmother's death, but both fatalities are still being probed by the Crown Office.
Then in February 2019, grandmother Mito Kaur died at the QEUH with a diagnosis of multi-system disorder, although a rare Mucor organism had been detected in her system shortly before she passed away.
This infection was initially considered to be a cause of the 63-year-old's death, but this conclusion was subsequently overturned in a review by the Crown Office which blamed it on flu instead.
A separate review is also underway into 80 cases of bloodstream infections which may have caused harm to or killed children treated at the RHC since it opened in 2015.
Today's report does not offer any explanation about the potential sources of any of these infections, but concludes that the design of the hospital "did not effectively reconcile conflicting aims of energy efficiency and meeting guidance standards for air quality".
Children and adults with cancers including leukaemias "have been exposed to risk that could have been lower if the correct design, build and commissioning had taken place”, said the review, particularly in relation to ventilation design and water systems.
Investigators added: "The Review takes the view that, in the design, construction and commissioning of QEUH, the client and construction contractors set out to comply with standards consistent with a more conventional hospital; they should have taken greater account of the needs of all potential patients including those in the high risk groups such as severely immuno-compromised patients.
"The remedies required to tackle the serious infection clusters, systemic shortcomings and sub-optimal design and operation, have come at great cost.
"They have had substantial impact on patients’ and families’ wellbeing although without directly attributable deaths, and substantial public expense that extends from pharmacy costs through to capital investment in water systems.
"The effect on staff, the displacement of patients, and very careful planning that has resulted in order to meet patient needs and minimise delays in treatment, are also amongst indirect but immeasurable costs."
READ MORE: Jeane Freeman announces public inquiry into QEUH and Edinburgh hospital builds
However, they said problems had and were being remedied.
They said: "NHS [Greater Glasgow and Clyde] has put in place, and is still working on, improvements to the wards where these vulnerable patients are managed.
"This includes replacement of water, drainage and ventilation systems in order to minimise the risk of infection to patients who will receive their cancer treatment there."
External communication by NHS GGC about serious problems with the building and possible links to infectious disease events was criticised as “inadequate and reactive”, while investigators also discovered "friction" among infection control colleagues even before the facilities opened.
READ MORE: Health board sues lead contractor over troubled hospital build
The review states: "From the outset, the three ICDs who, between them, had IP&C [Infection Prevention and Control] responsibilities for the whole hospital complex, did not work successfully as a team.
"Distrust mounted; distrust in the capability of management to listen to and address concerns and issues, and distrust of outside sources of support to management.
"There was extensive and inconclusive correspondence between ICDs [infection control doctors], with Estates and Facilities management, and general management of the hospital.
"Management and technical information was not forthcoming that was needed to inform ICDs’ decision-making."
They found shortcomings in independent scrutiny and safeguards during the project, which they said was "not sufficient", and the governance of the hospitals' design, build, commissioning and maintenance "did not adequately take account of the scale and complexity, and specialist nature of the building project".
NHS GGC has already launched legal action suing the lead contractor, Multiplex, for £73m in damages in relation to problems with the water and ventilation systems, the glass panels on the exterior of the building, the heating system and the atrium roof, as well as issues with internal fabric moisture ingress and the pneumatic transport system that links all the hospitals on the site.
A joint public inquiry is also due to take place into the construction of both the QEUH and the new children's hospital in Edinburgh - whose opening was delayed by ventilation flaws last year.
Both complexes were built by Multiplex.
Jane Grant, Chief Executive said: “This has been a very difficult period for our patients, their families and our staff for which we apologise.
“The findings highlight several areas of learning for NHSGGC. We remain fully committed to applying the learning from this experience.
"We also remain focused on remedying any ongoing consequences of decisions and actions taken when designing, building and commissioning of the hospitals and in their maintenance.
“The report highlights issues concerning previous ways of working in one area of the Board with regard to Infection Prevention and Control. We recognise that there are still issues to be addressed concerning the organisation’s culture."
In a statement after the review was published, Scottish Government health secretary Jeane Freeman said: “The patients and families most affected by the issues raised in the report will be understandably concerned and distressed by some of the findings of the Independent Review. I have been clear that those who have been affected deserve answers to the many questions they are entitled to ask – and this review is an important step in delivering that.
“The report provides a wealth of information for the forthcoming Public Inquiry into the construction of the QEUH and the Royal Hospital for Children and Young People in Edinburgh for which the Remit and Terms of Reference have now been published.
“In addition to the Public Inquiry, an Oversight Board, led by Scotland’s Chief Nursing Officer Fiona McQueen, will report on infection prevention and control practices at the hospital.
“We also await the results of a case note review of all recorded Gram-negative bloodstream infections in children who received haemato-oncology treatment from the opening of the Royal Hospital for Children in Glasgow until the start of this year. This team is also considering whether these children were put at risk because of the physical environment in which they were cared for.”
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