Risk factors for cerebrospinal fluid shunt infections during an outbreak: a case–control study

Journal of Hospital Infection 105 (2020) 78e82 Available online at www.sciencedirect.com

Journal of Hospital Infection journal homepage: www.elsevier.com/locate/jhin

Risk factors for cerebrospinal fluid shunt infections during an outbreak: a caseecontrol study A.K. McAlpine, L.J. Sauve, J.C. Collet, D.M. Goldfarb, E. Guest, P.J. McDonald, A. Zheng, J.A. Srigley* British Columbia Children’s Hospital, Vancouver, British Columbia, Canada

A R T I C L E

I N F O

Article history: Received 18 September 2019 Accepted 12 December 2019 Available online 20 December 2019 Keywords: Outbreak Shunt Infection CSF

S U M M A R Y

Background: There are few published reports of cerebrospinal fluid (CSF) shunt infection outbreaks. In 2017e2018, British Columbia Children’s Hospital (BCCH) experienced an increase in CSF shunt infections co-incident with a move to new operating rooms and a change in shunt catheters used. Aims: To describe how an outbreak was detected, investigations were undertaken to determine the cause, risk factors associated with CSF shunt infection during the outbreak, and changes implemented to attempt to control the outbreak. Methods: Retrospective caseecontrol study. Population included patients who underwent new shunt insertion or revision. Univariate logistic regression models were fitted for each of the variables. Associations with P-values <0.2 were considered of potential interest for further investigation. Findings: There were six cases of CSF shunt infection and 19 controls. The causative organism was different in each case. The only risk factors that met the criteria for further investigation were being a neonate at the time of surgery [odds ratio (OR) 9.0, 95% confidence interval (CI) 0.7e125.3, P¼0.10] and the presence of gastrointestinal disease (OR 3.8, 95% CI 0.5e26.2, P¼0.18). No association was found with the operating room used or the surgical staff. In response to the outbreak, human traffic through the operating rooms was limited, rigid adherence to the wearing of surgical masks was enforced, and return to the previous CSF shunt catheters used was implemented. Conclusion: No modifiable risk factors were associated with CSF shunt infection. After implementation of surgical protocol changes, no further cases of CSF shunt infection linked to the outbreak were identified. ª 2019 The Healthcare Infection Society. Published by Elsevier Ltd. All rights reserved.

Introduction Ventriculoperitoneal shunt (VPS) and other cerebrospinal fluid (CSF) shunt insertions are indicated for the management of hydrocephalus in children, but complications are common * Corresponding author. Address: 4500 Oak Street, Vancouver, BC, V6H 3N1, Canada. Tel.: þ1 604 875 2000x5208. E-mail address: [email protected] (J.A. Srigley).

[1]. Infection of the shunt is a well-described complication associated with significant morbidity and mortality [2]. Patient risk factors for CSF shunt infections include: premature birth [3], younger age [3], previous shunt infection [3], aetiology of hydrocephalus [4] and the presence of a gastrostomy tube [5,6]. The peri-operative risk factors for shunt infections include: experience of the neurosurgeon [7], use of a neuroendoscope [3], longer duration of shunt procedure [8], improper patient skin preparation, shaving of hair [9],

https://doi.org/10.1016/j.jhin.2019.12.012 0195-6701/ª 2019 The Healthcare Infection Society. Published by Elsevier Ltd. All rights reserved.

A.K. McAlpine et al. / Journal of Hospital Infection 105 (2020) 78e82 exposure of large areas of the patient’s skin during the procedure, shunt revision within 12 months [10], postoperative CSF leak [11], breached gloves [11] and high level of protein in CSF before surgery [12]. While the risk factors for CSF shunt infections in children have been well studied, there is very little description in the literature of the phenomenon of CSF shunt infection ‘outbreaks’ in hospitals. Starting in January 2018, British Columbia Children’s Hospital (BCCH) witnessed an increase in CSF shunt infections following some major changes at the hospital. In April 2017, the VPS catheters had been changed. The reason for this change was that the new catheters were deemed to be a better fit for the valve system favoured by BCCH neurosurgeons; both the previous and new catheters were impregnated with rifampicin and clindamycin. Shortly thereafter, construction of a new hospital building was completed, with new operating rooms (ORs) becoming fully operational on 29th October 2017. During that period, from a baseline of zero CSF shunt infections in the preceding 2 years, the hospital experienced six cases from 30th January to 9th August 2018. This meets the Centers for Disease Control and Prevention’s clinical definition of an ‘outbreak’ in that there was ‘the occurrence of more cases of disease than expected in a given area or among a specific group of people over a particular period of time’ [13]. It also represented an incidence rate of 13.6% during that time period, well above the rate of 6.0% [95% confidence interval (CI) 5.1e7.2%] reported among hospitals belonging to the Hydrocephalus Clinical Research Network (HCRN) e of which BCCH is a member e in 2016 [14]. Given the high potential for morbidity and mortality associated with these infections, a retrospective caseecontrol

2

Outbreak concern. Initial meeting and start of investigation

79

study was conducted to identify any potential causes, and changes were implemented to try to reverse the surge in cases. This paper describes the findings of the caseecontrol study and the control measures that were implemented.

Methods Description of the outbreak and control measures The outbreak was identified following the detection of three CSF shunt infections between 30th January and 4th April 2018. A timeline showing the cases, detection of the outbreak and infection control measures is shown in Figure 1. An initial meeting was held in April 2018 between infection prevention and control (IPAC) and neurosurgery staff to discuss the cases, and assess whether there had been any changes in practice. Other surgical departments were contacted to see if they had noted a similar increase in infection rates, which would have suggested a potential environmental source in the newly built ORs. This proved not to be the case, with other departments reporting an unchanged incidence of surgical site infections (SSIs). Nevertheless, concern about the outbreak persisted, and a multi-disciplinary team e consisting of medical microbiologists and IPAC, nursing and neurosurgery staff e was created in June 2018. An internal audit was initiated to try to identify any obvious risk factors. Since environmental or catheter-related concerns were deemed the most likely causes, these areas were investigated first. Concerns were raised by the OR staff about unnecessary foot traffic through the ORs, and the fact that high surgical case rates were resulting in too many intraabdominal surgeries being performed in the neurosurgical OR.

Formal audit initiated. Inquiries to catheter manufacturer. Air flow in rooms checked. Non-CSF surgeries in neurosurgical OR limited. Reduced traffic in ORs

Catheter brand changed. Automatic door sensor disabled. Masking before opening equipment. UV disinfection. Enlarged 'no entry' signs

1

0

Jan-18

Feb-18

Mar-18

Apr-18

May-18

Jun-18

Jul-18

Aug-18

Sep-18

Oct-18

Figure 1. Epidemic curve and implementation of control measures. CSF, cerebrospinal fluid; OR, operating room; UV, ultraviolet.

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Control measures were implemented immediately, including attempting to limit potentially contaminated cases performed in the neurosurgical OR and putting signage on the door to limit traffic through the ORs during CSF shunt cases. Air flow in the ORs was checked and found to be satisfactory. The manufacturer of the new shunt catheter and other local and HCRN member hospitals using the same brand of catheter were contacted to see if they had noted any changes in their CSF shunt infection rates, but no increases were reported. Despite the initial measures, three additional cases of CSF shunt infection were identified between 27th June and 9th August 2018. Further control measures were implemented in August 2018 after the audit was completed and presented to the relevant departments, including reverting to the previous brand of CSF catheter, disabling the automatic door opener after surgery had commenced, enlarging the ‘no entry’ signs outside the ORs, and enforcing that everyone in the ORs was fully masked before any equipment was opened. Ultraviolet-C disinfection of the ORs was also implemented at the end of each postoperative day. These measures remain in place as of the time of writing.

Definitions and identification of cases and controls The study population included patients who underwent new shunt insertion or shunt revision at BCCH from 29th October 2017 to 30th June 2018. The list was obtained from the surgical suites systems analyst. Patients who only had external ventricular drains inserted were excluded. A case was defined as a patient experiencing shunt infection within 90 days of a new shunt insertion or shunt revision at BCCH. To meet this definition, a patient needed to have an internalized CSF shunting device in place AND a bacterial or fungal pathogen(s) identified from the CSF AND at least one of the following: e fever (temperature 38 C); e neurological signs or symptoms (presence of any new neurological findings on examination, new or worsening lethargy, or worsening headache); e abdominal signs or symptoms (new or worsening abdominal cramps, tenderness on palpation, or the presence of guarding or rigidity); or e signs or symptoms of shunt malfunction or obstruction (evidence of new or worsening hydrocephalus, detected either by a rapidly enlarging head circumference (in children aged <2 years) or on computed tomography scan. Controls were defined as any patient from the study population without a shunt infection as defined above.

Data collection Charts were reviewed and information from the following categories was obtained for each case and control: demographics and patient history; clinical features; surgical details including the OR in which surgery took place, staff present (including assistants), length of the procedure, use of endoscopy or other instrumentation, and use and timing of preoperative antibiotics; peri-operative risk factors including the number of neurosurgical operations in the preceding 90 days, the urgency of the procedure, and the use of chlorhexidine

wipes; and SSI details (if present). National Surgery Quality Improvement Program chart reviews were used to obtain the data when available.

Statistical analysis Univariate logistic regression models were fitted for each of the predictors/variables of interest, and odds ratios, with 95% CI, were calculated. Associations with P-values <0.2 were considered of potential interest for further investigation.

Results In the time frame examined (Figure 1), there were six cases of CSF shunt infection and 19 controls. The causative organism was different in each case, and included Klebsiella aerogenes, Pseudomonas aeruginosa, Staphylococcus aureus, Staphylococcus epidermidis, Staphylococcus haemolyticus and Streptococcus mitis. The clinical features of the case patients are summarized in Table I. The median time from insertion of the shunt to symptom onset was 10 days. Fever and abdominal symptoms were common presenting problems, followed by neurological abnormalities (often a decreased level of consciousness or lethargy). Evidence of shunt malfunction was present in 66% of cases. There was a wide range of white blood cell counts in CSF, from three to 1775. One of the six cases died. The peri-operative risk factors are shown in Table II. Being a neonate and the presence of gastrointestinal disease were the only risk factors to meet the statistical criteria for further interest. Age, sex and a history of prematurity were not associated with increased risk of CSF shunt infection. There was no association between CSF shunt infection and the OR, the surgeon or learner involved, the American Society of Anesthesiologists’ assessment score, or whether the case was urgent or elective. In addition, there was no association between the length of surgery and the risk of infection. The use of chlorhexidine wipes was not well documented, but the limited data indicate it was not associated with CSF shunt infections. Similarly, there was no evidence that the use of endoscopy, which was not used in any of the cases, or preoperative intravenous antibiotics had any effect. In addition, the length of the procedure was not linked to infection.

Table I Clinical features Variable

Time from shunt insertion to symptom onset, median (days) Fever Neurological symptoms Abdominal symptoms Shunt malfunction WBC count in cerebrospinal fluid, median Mortality within 30 days Mortality >30 days

Resultsa

10 (5e53) 4 (66.7) 3 (50.0) 4 (66.7) 4 (66.7) 490 (3e1775) 0 1 (16.7)

WBC, white blood cell. a Data are presented as median (range) or N (%) of patients.

A.K. McAlpine et al. / Journal of Hospital Infection 105 (2020) 78e82 Table II Peri-operative risk factors Casesa

Neonate at time of surgery Oesophageal/ gastric/ intestinal disease Premature birth Age, median (years) No surgery in preceding 90 days One operation in preceding 90 days Two operations in preceding 90 days Elective case status Urgent case status Emergency case status Use of intraoperative antibiotics Use of an endoscope Attending surgeon A Attending surgeon B Attending surgeon C Presence of a resident Presence of a fellow Shunt accessed post surgery Shunt not accessed post surgery a

2 (33.3)

Controlsa

Odds ratio (95% P-value confidence interval)

1.9

8 (42.1) 5.00 (0.46e54.04) 0.67 3.1

0.99 (0.86e1.15)

0.89

3 (50.0) 13 (68.4) Reference

-

1 (16.7)

4 (21.1) 1.08 (0.09e13.5)

2 (33.3)

2 (10.5) 4.33 (0.42e44.43) 0.231

1 (20.0)

4 (21.1) Reference

3 (50.0)

8 (42.1) 1.50 (0.12e19.44) 0.51

1 (20.0)

7 (36.8) 0.57 (0.03e11.85) 0.54

1 (16.7)

1 (5.3)

0

3 (16)

0.61

-

3.6 (0.19e38.34) 0.39

-

-

3 (50.0)

8 (42.1) Reference

-

3 (50.0)

3 (15.8) 2.67 (0.33e21.32) 0.94

0

10th December 2019. That infection occurred on 15th January 2019, and was related to skin breakdown over the shunt hardware from a bilevel positive airway pressure device in a premature neonate. Given that the patient had a specific risk factor, it was not believed to be related to the previous cluster.

1 (5.3) 9.00 (0.65e125.32) 0.10

3 (50.0%) 4 (21.1) 3.75 (0.54e26.19) 0.18

4 (66.7)

81

8 (42.1) -

-

5 (83.3) 16 (84.2) 1.00 (0.08e11.93) 1.00 4 (66.7) 14 (73.7) 0.77 (0.11e5.61)

0.80

2 (33.3)

1 (5.3) 5.33 (0.34e82.83) 0.23

3 (50.0)

8 (42.1) -

-

Data are presented as median (range) or N (%) of patients.

Post surgery, the number of times the shunt was accessed for CSF sampling was not associated with increased risk of CSF shunt infection. Although there was no evidence linking the change in catheter model to the infections, the brand of catheter used was reverted to that used prior to the outbreak in August 2018. Since implementation of the measures in Figure 1, only one further case of CSF shunt infection has been identified as of

Discussion This study aimed to describe an outbreak of CSF shunt infections at the study institution. Shunt infections are known to be associated with serious morbidity and mortality [15], as well as prolonged hospital stay and the need for repeat surgery. As a result, it was important to identify the cause of the outbreak and implement measures to arrest it. Multiple variables were examined in order to identify any possible associations with the outbreak. In terms of demographics, no obvious risk factors emerged, but there was a trend towards significance in infections in neonates and those with gastrointestinal disease. This is in keeping with previous studies that had similar findings [3,5]. The organisms cultured were unusual in that only 50% were Staphylococcus spp., while 33% were Gram-negative bacteria. Previous studies in developed countries have shown an overwhelming preponderance of staphylococcal species (75%) with a paucity of Gram-negative organisms [1]. Only studies in Kenya and Turkey showed similar rates of Gram-negative VPS infection (40% and 43%, respectively) [12,16]. The reasons for this relatively high number of Gram-negative infections are unclear. Peri-operative risk factors indicated that no specific OR, surgeon, assistant or staff member was associated with increased CSF shunt infections. In addition, the duration of surgery was not a risk factor. Postoperatively, shunts were accessed relatively infrequently, so it was difficult to ascertain if this was a risk or not. Previous studies have failed to demonstrate a clear association, and a very low risk of infection secondary to percutaneous access of CSF from a shunt reservoir has been reported [17]. With regards to the changes implemented, no definitive evidence was found to implicate the change to the new ORs in the outbreak. In addition, the change in shunt catheters was never shown to be causative. Regarding the other control measures, specifically the limitation of human traffic through the ORs, recent studies have demonstrated that the recurrent opening of doors into ORs allows contaminated air to flow into them [18], although the effect on infection rates in surgery is unknown. To the authors’ knowledge, there are no data demonstrating that the mandatory wearing of face masks prior to the opening of all surgical instrumentation reduces SSIs. There is evidence that the use of ultraviolet light after conventional cleaning methods reduces the risk of bacterial contamination in ORs [19,20]. A strength of this study is that it is, to the authors’ knowledge, the first investigation of a documented CSF shunt infection outbreak. This paper reports what was investigated and the hospital actions in response, and notes that there have been no new cases related to the outbreak since the changes. This study has several limitations. First, since the numbers of cases and controls were small, the study was underpowered to detect significant associations. The fact that most risk factors studied did not meet statistical criteria for further

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investigation does not rule them out as significant contributors to CSF shunt infection in this situation. Second, with regards to the changes implemented, as several changes were made simultaneously in an attempt to halt the outbreak, it is difficult to know which, if any, were responsible for the improvements noted. It is also possible that awareness of the increase in CSF shunt infections by all team members led to changes in behaviour that were not measured which contributed to the improvement. In summary, this paper reports an outbreak of CSF shunt infections in a children’s hospital in Canada. The outbreak was detected quickly due to the low baseline rate of infections. Prompt investigation found no obvious causes, but identified patients that were at higher risk. Changes in equipment and OR protocols were implemented, and no further cases related to the outbreak have been reported. Conflict of interest statement None declared. Funding sources None.

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