The Case

A 5-day old male infant with congenital heart disease including aortic atresia and double outlet right ventricle was transferred to the pediatric intensive care unit (PICU) from an outside hospital. His initial procedure was a median sternotomy with bilateral pulmonary artery banding and intracardiac line placement on hospital day 5. The patient recovered in the PICU until postoperative day 18, when he underwent a Norwood procedure with Sano shunt, removal of bilateral pulmonary artery bands, and revision of his median sternotomy. Mediastinal and pleural drains were placed at this time along with a peritoneal dialysis catheter. Chest closure was delayed until postoperative day 3, following routine practice, and performed under anesthesia at the bedside in PICU.

Staphylococcus aureus bacteremia was identified on postoperative day 7 (after the Norwood procedure). Narrowing of the Sano shunt due to possible vegetation was identified on postoperative day 19, requiring venoarterial extracorporeal membrane oxygenation (VA-ECMO) through lines placed in the open chest wound in the PICU. An additional revision sternotomy and Sano shunt takedown was performed the next day, during which he was found to have florid mediastinitis including multiple pockets of purulent material and a rind of inflammatory tissue surrounding the heart. The chest tissue culture collected during surgery demonstrated Aspergillus fumigatus. The patient returned to PICU with an open chest to optimize antibacterial and antifungal therapies for a hospital-acquired invasive fungal infection in an immunocompetent infant. This patient was discharged home on long-term antifungal therapy but at age 7 months, he presented to the Emergency Department (ED) in cardiac arrest of unclear etiology and resuscitation was unsuccessful.

In response to this case, the hospital undertook a comprehensive investigation and root cause analysis. A retrospective review of Aspergillus cultures from the same OR and PICU did not find any other cases of postoperative Aspergillus. Environmental assessment of the OR did not reveal any sources of contamination. However, the OR supply room was not on a schedule for routine terminal cleaning, was not connected to the OR’s high-efficiency particulate air (HEPA) filtration system, had a slightly positive air pressure differential to the OR, and the storage room door was left open during surgery, leading to potential contamination of OR air with supply room air. In the PICU patient room, high levels of dust on the bedside T-bar, ceiling tiles and curtains suggested inadequate cleaning, the patient’s bed was located directly below the air supply vent, and stained ceiling tiles indicated a leaking pipe in the bathroom ceiling, which served as a potential source of Aspergillus colonization and contamination. Environmental cultures of the area around the leaking pipe grew Aspergillus species that was not A. fumigatus.

The Commentary

By Elizabeth Partridge, MD, MPH, Daniel Dodson, MD, MS, Mary Reilly, MHA, BSN, RN, CIC and Stuart H. Cohen, MD

Background & Significance

Aspergillus species are ubiquitous environmental molds found in soil, water, dust, and decaying vegetation. Spores are approximately 2.5-3.0 um in size and can contaminate hospital environments through foot traffic, ventilation, and water systems. Surgical site infections (SSIs) due to Aspergillus are rare but well described in the medical literature among immunocompetent adults, most commonly after cardiac surgery, resulting in sternal wound infections, mediastinitis, and endocarditis. Aspergillosis after cardiac surgery has a reported mortality rate of 93%.¹Only a few pediatric cases of Aspergillus SSIs after cardiac surgery have been reported, also with high mortality.^2-5

Postoperative infections caused by environmental molds should prompt an immediate epidemiologic evaluation of potential infectious sources and institutional infection prevention protocols. Aspergillus SSIs have been linked to contaminated ventilation systems, contaminated equipment, and environmental air associated with construction.^1,6,7Although in many cases, a source of Aspergillus is not identified, Aspergillus SSIs provide opportunities to evaluate and improve existing infection prevention practices. In this case, the hospital’s investigation was appropriately multipronged and included review of institutional epidemiology, as well as environmental and equipment protocols,^8,9each revealing important and generalizable opportunities for improvement in patient safety practices.

It seems most likely, in this case, that the Aspergillus originated from the ceiling and/or air supply system in the patient’s PICU room and bathroom, although other sources could not be ruled out. This finding raises questions about the safety of performing post-cardiac open surgical procedures in the ICU versus the OR. For example, ICU patient rooms lack the ventilation controls to decrease particulates and bacteria in the air and the strict cleaning protocols required in ORs. On the other hand, there are also risks associated with transporting unstable patients to the OR and delaying procedures while awaiting OR availability. Although the literature on this topic is limited, several studies have shown similar outcomes between patients undergoing cardiac re-explorations in the OR vs ICU, including mortality, deep sternal wound infection and sepsis rates.^10-12The safety of procedures performed in the ICU has been demonstrated particularly for planned or non-urgent interventions, including delayed sternal closure.¹³ Although it is routine practice at many hospitals to perform chest closure procedures in the PICU, this practice does put a stronger spotlight on environmental management in the PICU.

Multipronged Approach to Improving Safety

Epidemiology

After identifying this case, the hospital’s infection control team appropriately reviewed all Aspergillus cultures from surgical procedures performed in their pediatric cardiothoracic operating room and PICU. Although they did not find any other cases of postoperative Aspergillus, this review could have been accomplished more quickly with an ongoing, real-time, all-location, surveillance system to support early identification of outbreaks and sentinel infections. Hospital infection prevention teams can use surveillance software to proactively identify, investigate and mitigate nosocomial infections wherever they occur within the facility. In addition, whole genome sequencing of the Aspergillus fumigatus isolate would be recommended for comparison to environmental samples and future cases.^14,15

Environment

The hospital’s investigation appropriately included an environmental assessment of all hospital areas pertaining to the case.¹⁶For this event, pertinent locations would include the OR, the adjacent supply room containing cardiac surgery equipment, the PICU patient room and bathroom, and the PICU equipment and ECMO storage room. Given the known association of Aspergillus with ventilation systems, a thorough evaluation of the maintenance protocols for ventilation systems is also recommended.¹⁶Particle counts should meet specific filtration efficiency ratings in all relevant areas. Construction activity, not relevant to this case, is a known risk factor for increased levels of environmental molds in proximity.^8,16,17

In this case, the hospital’s investigation revealed significant environmental concerns in the OR supply room and the patient’s PICU room and bathroom. To address the OR supply room problem, the hospital should institute weekly terminal cleans with ongoing cleaning-log audits. Ideally, the supply room’s air supply would be connected to the OR’s HEPA filtration system. An alternative, perhaps more feasible, approach would be to convert the supply room’s air pressure to negative pressure relative to the OR while instructing staff to keep the supply room door closed to avoid contamination of the OR with supply room air.

The patient’s PICU room and bathroom require mold remediation, which would include deep cleaning and replacement of water-stained ceiling tiles. It is important to clarify and optimize bedside and unit cleaning protocols to include dusting walls, air vents, lights, and ceilings with lint cleaners. Disposable privacy curtains should be changed when visibly soiled, after discharge of patients on isolation precautions, or every 6 months (whichever comes first).¹⁸Strategies for minimizing environmental contamination from long hospital stays and allowing periodic deep cleaning are to 1) limit the number and size of personal items and 2) mandate patient room changes every 14 days.^19,20To prevent dust and mold collection, ceiling tiles should be replaced with products that are wipeable and have flush installation. Air vent diffuser chambers should be adjusted to ensure proper air circulation without direct flow toward the patient's bed.¹⁸Routine inspections of the unit by a multidisciplinary team of auditors can help to safeguard against unintended “drift” from environmental best practices. Such a team should include the unit manager and representatives from units such as Environmental Services, Environmental Health & Safety, Infection Prevention, and Facility Operations and Maintenance.

Equipment & Materials

Finally, an event of this type provides an opportunity to evaluate scheduled protocols for operation, maintenance, and storage of intra- and post-operative equipment. To minimize the risk of nosocomial fungal infections, hospitals should implement measures to prevent dust accumulation and “standing water” inside reusable equipment. For example, ECMO machines should use HEPA-filtered vacuums to remove dust from exhaust vents and hoods to redirect air flow away from sterile fields. Equipment covers should be used to prevent dust accumulation between uses. Water in heater-cooler machines should be emptied and refilled after each use. All these interventions necessitate staff education and ongoing audits. To help identify which surgical equipment (i.e., ECMO and heater-cooler machines) is used on which patient, and on what date, a tracking system is useful.¹⁶

While some centers have shown comparable post-operative infection rates between patients undergoing invasive cardiac procedures in the ICU vs OR,¹²there is inherent infection risk performing these procedures in a non-OR setting. Therefore, careful consideration should be given to the types and durations of invasive procedures performed at bedside. In non-emergent cases for which the risks of relocating the patient are deemed too great, it is essential that the ICU adopt infection prevention strategies that mimic those used in the OR. These include limiting room traffic with only essential personnel present, using sterile trays with OR instruments, requiring a pre-procedure sterile scrub for all individuals participating in the procedure, HEPA filter installation, enhanced environmental monitoring and cleaning.

Take Home Points

• Postoperative infections caused by environmental molds should prompt a thorough investigation to identify possible sources of infection and address gaps in existing infection prevention practices. Contaminated air handlers and air-supply vents are the most common sources of opportunistic fungal infections when a source is identified.
• Delayed surgical wound closure and invasive sterile bedside procedures may place patients at greater risk of a postoperative infection from environmental pathogens than procedures taking place in an operating room.
• Enhanced environmental cleaning of hospital rooms may help reduce the risk of postoperative infections from bedside procedures.
• Evaluation of equipment cleaning, maintenance and storage are an essential part of an investigation and prevention of environmental contamination.
• Interventions instituted at the time of a case investigation are subject to drift. On-going auditing by a multidisciplinary team can help maintain optimal infection prevention strategies.

Elizabeth Partridge, MD, MPH
Associate Clinical Professor
Pediatrics, Infectious Disease
Medical Director of Infection Prevention for UC Davis Children’s Hospital
UC Davis Health
epartridge@ucdavis.edu

Daniel Dodson, MD, MS
Assistant Clinical Professor
Pediatrics, Infectious Disease
UC Davis Health
dsdodson@ucdavis.edu

Mary Reilly MHA, BSN, RN, CIC
Director of Hospital Epidemiology and Infection Prevention
UC Davis Health
mreilly@ucdavis.edu

Stuart H. Cohen, MD
Chief, Division of Infectious Diseases
Director of Hospital Epidemiology and Infection Prevention
Professor
UC Davis Health
Stcohen@ucdavis.edu

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