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Risk factors for cerebrospinal fluid shunt infections during an outbreak: a case–control study
Journal Pre-proof Risk factors for cerebrospinal fluid shunt infections during an outbreak: A case control study McAlpine AK, Sauve LJ, Collet JC, D.M. Goldfarb, Guest E, McDonald PJ, Zheng A, Srigley JA PII:
S0195-6701(19)30533-X
DOI:
https://doi.org/10.1016/j.jhin.2019.12.012
Reference:
YJHIN 5870
To appear in:
Journal of Hospital Infection
Received Date: 18 September 2019 Accepted Date: 12 December 2019
Please cite this article as: AK M, LJ S, JC C, Goldfarb D, E G, PJ M, A Z, JA S, Risk factors for cerebrospinal fluid shunt infections during an outbreak: A case control study, Journal of Hospital Infection, https://doi.org/10.1016/j.jhin.2019.12.012. This is a PDF file of an article that has undergone enhancements after acceptance, such as the addition of a cover page and metadata, and formatting for readability, but it is not yet the definitive version of record. This version will undergo additional copyediting, typesetting and review before it is published in its final form, but we are providing this version to give early visibility of the article. Please note that, during the production process, errors may be discovered which could affect the content, and all legal disclaimers that apply to the journal pertain. © 2019 Published by Elsevier Ltd on behalf of The Healthcare Infection Society.
Title Page
Risk factors for cerebrospinal fluid shunt infections during an outbreak: A case control study McAlpine AK, Sauve LJ, Collet JC, Goldfarb DM, Guest E, McDonald PJ, Zheng A, Srigley JA
All work conducted at British Columbia Children’s Hospital, 4480 Oak Street, Vancouver, British Columbia, Canada, V6H 3N1
Corresponding author: Jocelyn Srigley - [email protected], Phone. (604) 875-2000 ext. 5208. Mailing Address: 4500 Oak St Vancouver, BC V6H 3N1
Key words: Outbreak Shunt Infection CSF
1
Abstract/Summary Background: There are few published reports of cerebrospinal fluid (CSF) shunt infection outbreaks. In 2017-2018, 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 done to determine the cause, risk factors associated with CSF shunt infection during the outbreak, and changes implemented to attempt to control it. Methods: Retrospective case-control study. Population included patients who underwent new shunt insertion or revision. Univariate logistic regression models were fitted for each of the variables. Associations with pvalues less than 0.2 were considered of potential interest for further investigation. Findings: There were 6 cases of CSF shunt infection and 19 controls. The causative organism was different in each case. The only risk factors that met criteria for further investigation were being a neonate at the time of surgery (odds ratio [OR] 9.0, 95% confidence interval [CI] 0.7-125.3, p=0.10) and the presence of gastrointestinal disease (OR 3.8, 95% CI 0.5-26.2, p=0.18). 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.
2
Introduction: Ventriculoperitoneal shunt (VPS) and other cerebrospinal fluid (CSF) shunt insertions are indicated for the management of hydrocephalus in children, but complications are common.[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] etiology of hydrocephalus,[4] and the presence of a gastrostomy tube.[5, 6] The perioperative 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] 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 a high CSF protein pre-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 after some major changes had been made 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 October 29, 2017. During that period, from a baseline of zero CSF shunt infections in the preceding two years, the hospital experienced six cases from January 30 to August 9, 2018. This meets the Center for Disease Control (CDC) 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% CI 5.1%-7.2%) reported among hospitals belonging to the Hydrocephalus Clinical Research Network (HCRN) – of which BCCH is a member – in 2016.[14] Given the high potential for morbidity and mortality associated with these infections, a retrospective case-control 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 case-control 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 January 30, 2018, and April 4, 2018. A timeline showing the cases, detection of the outbreak, and infection control measures is shown in Figure I. An initial meeting was held in April between infection prevention and control (IPAC) and neurosurgery to discuss the cases and assess whether there had been any changes in
3
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 multidisciplinary team consisting of medical microbiologists, IPAC, nursing, and neurosurgery 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 intra-abdominal surgeries being performed in that OR. Control measures were immediately implemented, including attempting to limit potentially contaminated cases done in the neurosurgical OR and putting signage on the door to limit traffic through the OR during CSF shunt cases. Airflow in the ORs was checked and found to be satisfactory. We contacted the manufacturer of the new shunt catheter and other local and HCRN member hospitals using the same brand of catheter to see if they had noted any changes to their CSF shunt infection rates, but no increases were reported. Despite the initial measures, three additional cases of CSF shunt infection were identified between June 27 and August 9, 2018. Further control measures were implemented in August after the audit was completed and presented to the relevant departments, including changing back to the previous brand of CSF catheter, disabling the automatic door opener after surgery had commenced, enlarging the ‘No Entry’ signs outside the OR, and enforcing that everyone in the OR 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 October 29, 2017, to June 30, 2018. The list was obtained from the surgical suites systems analyst. Patients who only had external ventricular drains (EVDs) inserted were excluded. A case was defined as a patient experiencing shunt infection within 90 days after 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: a) fever (temperature ≥38º C), OR b) neurological signs or symptoms (presence of any new neurological findings on examination, new or worsening lethargy, or worsening headache), OR
4
c) abdominal signs or symptoms (new or worsening abdominal cramps, tenderness on palpation, or the presence of guarding or rigidity), OR d) signs or symptoms of shunt malfunction or obstruction (evidence of new or worsening hydrocephalus, detected either by a rapidly enlarging head circumference [in children <2 years] or on CT 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 the surgery took place in, staff present (including assistants), length of the procedure, use of endoscopy or other instrumentation, and use and timing of pre-operative antibiotics; perioperative 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 (NSQIP) 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% confidence intervals, were calculated. Associations with p-values less than 0.2 were considered of potential interest for further investigation Results: In the time frame examined (Figure I), there were 6 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 the Streptococcus mitis group. The clinical features of the case patients are summarized in Table I. The median length from insertion of the shunt to the onset of symptoms 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 CSF white blood cell counts, from 3 to 1775. One of the 6 cases died. The peri-operative risk factors are shown in Table II. Only being a neonate and the presence of gastrointestinal disease met the statistical criteria for further interest. Age, sex and a history of prematurity were not associated with an increased risk of CSF shunt infection. There was no association between CSF shunt infection and the operating room, the surgeon or learner involved, the American Society of Anesthesiologists (ASA) 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.
5
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 pre-operative intravenous antibiotics had any effect. The length of the procedure was also not linked to infection. Post-surgery, the number of times the shunt was accessed for CSF sampling was not associated with an increased risk of CSF shunt infection. Although there was no evidence linking the change in catheter model to the infections, the brand of catheter was changed back to the model that was used prior to the outbreak in August 2018. After the measures in Figure I were implemented, only one further case of CSF shunt infections has been identified as of December 10, 2019. That infection occurred on January 15, 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.
Discussion: In this study, we aimed to describe an outbreak of CSF shunt infections at our institution. Shunt infections are known to be associated with serious morbidity and mortality,[15] as well as prolonged hospital stays and the need for repeat surgeries. As a result, it was important that we tried to identify the cause of the outbreak and implement measures to arrest it. We examined multiple variables to attempt to find 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 also unusual in that only 50% were Staphylococcus species, 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. Perioperative risk factors indicated that no specific OR, surgeon, assistant or staff member was associated with increased CSF shunt infections, nor was the duration of surgery 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
6
causative. Regarding the other control measures, specifically the limitation of human traffic through the OR, 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. There are, to our knowledge, no data demonstrating that the mandatory wearing of face masks prior to the opening of all surgical instrumentation reduces surgical site infections. There is evidence that the use of ultraviolet light after conventional cleaning methods reduces the risk of bacterial contamination in operating rooms.[19, 20] The strengths of this study were that this is, to our knowledge, the first investigation of a documented CSF shunt infection outbreak. We report what was investigated and the hospital actions in response, and note since the changes, there have been no new cases related to the outbreak. This study has several limitations. First, since the numbers of cases and controls were small, the study was underpowered to detect statistically significant associations. The fact that most risk factors studied did not meet statistical criteria for further investigation does not rule them out as being significant contributors to CSF shunt infection in this situation. Second, with regards to the changes implemented, because 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 let to changes in behavior we did not measure that contributed to the improvement. In summary, we report 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 subsequently, no further cases related to the outbreak have been reported.
References: [1] Hanak BW, Bonow RH, Harris CA, Browd SR. Cerebrospinal Fluid Shunting Complications in Children. Pediatric neurosurgery. 2017;52(6):381-400. [2] Prusseit J, Simon M, von der Brelie C, Heep A, Molitor E, Volz S, et al. Epidemiology, prevention and management of ventriculoperitoneal shunt infections in children. Pediatric neurosurgery. 2009;45(5):325-36. [3] McGirt MJ, Zaas A, Fuchs HE, George TM, Kaye K, Sexton DJ. Risk factors for pediatric ventriculoperitoneal shunt infection and predictors of infectious pathogens. Clinical infectious diseases : an official publication of the Infectious Diseases Society of America. 2003;36(7):858-62. [4] Serlo W, Fernell E, Heikkinen E, Anderson H, von Wendt L. Functions and complications of shunts in different etiologies of childhood hydrocephalus. Child's nervous system : ChNS : official journal of the International Society for Pediatric Neurosurgery. 1990;6(2):92-4. [5] Oterdoom LH, Marinus Oterdoom DL, Ket JCF, van Dijk JMC, Scholten P. Systematic review of ventricular peritoneal shunt and percutaneous endoscopic gastrostomy: a safe combination. Journal of neurosurgery. 2017;127(4):899-904. [6] Vui HC, Lim WC, Law HL, Norwani B, Charles VU. Percutaneous endoscopic gastrostomy in patients with ventriculoperitoneal shunt. The Medical journal of Malaysia. 2013;68(5):389-92.
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[7] Cochrane DD, Kestle JR. The influence of surgical operative experience on the duration of first ventriculoperitoneal shunt function and infection. Pediatric neurosurgery. 2003;38(6):295-301. [8] Cheng H, Chen BP, Soleas IM, Ferko NC, Cameron CG, Hinoul P. Prolonged Operative Duration Increases Risk of Surgical Site Infections: A Systematic Review. Surgical infections. 2017;18(6):722-35. [9] Horgan MA, Piatt JH, Jr. Shaving of the scalp may increase the rate of infection in CSF shunt surgery. Pediatric neurosurgery. 1997;26(4):180-4. [10] Merkler AE, Ch'ang J, Parker WE, Murthy SB, Kamel H. The Rate of Complications after Ventriculoperitoneal Shunt Surgery. World neurosurgery. 2017;98:654-8. [11] Kulkarni AV, Drake JM, Lamberti-Pasculli M. Cerebrospinal fluid shunt infection: a prospective study of risk factors. Journal of neurosurgery. 2001;94(2):195-201. [12] Yakut N, Soysal A, Kepenekli Kadayifci E, Dalgic N, Yilmaz Ciftdogan D, Karaaslan A, et al. Ventriculoperitoneal shunt infections and re-infections in children: a multicentre retrospective study. British journal of neurosurgery. 2018;32(2):196-200. [13] CDC Epidemiology Glossary USA: Centers for Disease Control and Prevention; 2015 [updated Page last reviewed: January 21, 2015. Epidemiology Glossary]. Available from: https://www.cdc.gov/reproductivehealth/data_stats/glossary.html. [14] Kestle JR, Holubkov R, Douglas Cochrane D, Kulkarni AV, Limbrick DD, Jr., Luerssen TG, et al. A new Hydrocephalus Clinical Research Network protocol to reduce cerebrospinal fluid shunt infection. Journal of neurosurgery Pediatrics. 2016;17(4):391-6. [15] Turgut M, Alabaz D, Erbey F, Kocabas E, Erman T, Alhan E, et al. Cerebrospinal fluid shunt infections in children. Pediatric neurosurgery. 2005;41(3):131-6. [16] Ochieng N, Okechi H, Ferson S, Albright AL. Bacteria causing ventriculoperitoneal shunt infections in a Kenyan population. Journal of neurosurgery Pediatrics. 2015;15(2):150-5. [17] Spiegelman L, Asija R, Da Silva SL, Krieger MD, McComb JG. What is the risk of infecting a cerebrospinal fluid-diverting shunt with percutaneous tapping? Journal of neurosurgery Pediatrics. 2014;14(4):336-9. [18] Weiser MC, Shemesh S, Chen DD, Bronson MJ, Moucha CS. The Effect of Door Opening on Positive Pressure and Airflow in Operating Rooms. The Journal of the American Academy of Orthopaedic Surgeons. 2018;26(5):e105-e13. [19] Simmons S, Dale C, Jr., Holt J, Passey DG, Stibich M. Environmental effectiveness of pulsed-xenon light in the operating room. American journal of infection control. 2018;46(9):1003-8. [20] El Haddad L, Ghantoji SS, Stibich M, Fleming JB, Segal C, Ware KM, et al. Evaluation of a pulsed xenon ultraviolet disinfection system to decrease bacterial contamination in operating rooms. BMC infectious diseases. 2017;17(1):672.
8
Figures:
Figure I: Epidemic Curve and Implementation of Control Measures 2
Outbreak concern Initial meeting and start of investigation
Formal audit initiated Inquiries to catheter manufacturer Airflow in rooms checked Non-CSF surgeries in neurosurgical OR limited Reduced traffic in ORs
Catheter brand changed Automatic door sensor disabled Masking pre-equipment opening 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
9
Tables:
Table I Clinical Features Variable Median days from OR to symptoms
Results 10 (5-53)
Fever
4 (66.7)
Neurological symptoms
3 (50.0)
Abdominal symptoms
4 (66.7)
Shunt malfunction
4 (66.7)
Median CSF WBC
490 (3-1775)
Mortality within 30 days
0
Mortality > 30 days
1 (16.7)
* Data are presented as median (range) or number (%) of patients.
Table II Perioperative Risk Factors Cases* Neonate at surgery 2 (33.3) Esophageal/gastric/ 3 (50.0%) intestinal disease Premature birth 4 (66.7)
Controls* 1 (5.3) 4 (21.1) 8 (42.1)
Odds Ratio 9.00 (0.65 – 125.32) 3.75 (0.54-26.19) 5.00 (0.46-54.04)
P value 0.10 0.18 0.67
Age, median years
1.9
3.1
0.99 (0.86-1.15)
0.89
0 Operations in preceding 90 days
3 (50.0)
13 (68.4)
Reference
-
1 Operation in preceding 90 days
1 (16.7)
4 (21.1)
1.08 (0.09-13.5)
0.61
2 Operations in preceding 90 days
2 (33.3)
2 (10.5)
4.33 (0.42-44.43)
0.231
Elective Case Status
1 (20.0)
4 (21.1)
Reference
-
10
Urgent Case Status
3 (50.0)
8 (42.1)
1.50 (0.12-19.44)
0.51
Emergency Case Status
1 (20.0)
7 (36.8)
0.57 (0.03-11.85)
0.54
Use of intraoperative antibiotics
1 (16.7)
1 (5.3)
3.6 (0.19-38.34)
0.39
Use of an endoscope
0
3 (16)
-
-
Attending surgeon A
3 (50.0)
8 (42.1)
Reference
-
Attending surgeon B
3 (50.0)
3 (15.8)
2.67 (0.33-21.32)
0.94
Attending surgeon C Presence of a resident
0 5 (83.3)
8 (42.1) 16 (84.2)
1.00 (0.08-11.93)
1.00
Presence of a fellow
4 (66.7)
14 (73.7)
0.77 (0.11-5.61)
0.80
Shunt accessed post 2 (33.3) 1 (5.3) 5.33 surgery (0.34-82.83) Shunt not accessed 3 (50.0) 8 (42.1) post surgery * Data are presented as median (range) or number (%) of patients.
0.23 -
11
S0195-6701(19)30533-X
DOI:
https://doi.org/10.1016/j.jhin.2019.12.012
Reference:
YJHIN 5870
To appear in:
Journal of Hospital Infection
Received Date: 18 September 2019 Accepted Date: 12 December 2019
Please cite this article as: AK M, LJ S, JC C, Goldfarb D, E G, PJ M, A Z, JA S, Risk factors for cerebrospinal fluid shunt infections during an outbreak: A case control study, Journal of Hospital Infection, https://doi.org/10.1016/j.jhin.2019.12.012. This is a PDF file of an article that has undergone enhancements after acceptance, such as the addition of a cover page and metadata, and formatting for readability, but it is not yet the definitive version of record. This version will undergo additional copyediting, typesetting and review before it is published in its final form, but we are providing this version to give early visibility of the article. Please note that, during the production process, errors may be discovered which could affect the content, and all legal disclaimers that apply to the journal pertain. © 2019 Published by Elsevier Ltd on behalf of The Healthcare Infection Society.
Title Page
Risk factors for cerebrospinal fluid shunt infections during an outbreak: A case control study McAlpine AK, Sauve LJ, Collet JC, Goldfarb DM, Guest E, McDonald PJ, Zheng A, Srigley JA
All work conducted at British Columbia Children’s Hospital, 4480 Oak Street, Vancouver, British Columbia, Canada, V6H 3N1
Corresponding author: Jocelyn Srigley - [email protected], Phone. (604) 875-2000 ext. 5208. Mailing Address: 4500 Oak St Vancouver, BC V6H 3N1
Key words: Outbreak Shunt Infection CSF
1
Abstract/Summary Background: There are few published reports of cerebrospinal fluid (CSF) shunt infection outbreaks. In 2017-2018, 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 done to determine the cause, risk factors associated with CSF shunt infection during the outbreak, and changes implemented to attempt to control it. Methods: Retrospective case-control study. Population included patients who underwent new shunt insertion or revision. Univariate logistic regression models were fitted for each of the variables. Associations with pvalues less than 0.2 were considered of potential interest for further investigation. Findings: There were 6 cases of CSF shunt infection and 19 controls. The causative organism was different in each case. The only risk factors that met criteria for further investigation were being a neonate at the time of surgery (odds ratio [OR] 9.0, 95% confidence interval [CI] 0.7-125.3, p=0.10) and the presence of gastrointestinal disease (OR 3.8, 95% CI 0.5-26.2, p=0.18). 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.
2
Introduction: Ventriculoperitoneal shunt (VPS) and other cerebrospinal fluid (CSF) shunt insertions are indicated for the management of hydrocephalus in children, but complications are common.[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] etiology of hydrocephalus,[4] and the presence of a gastrostomy tube.[5, 6] The perioperative 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] 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 a high CSF protein pre-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 after some major changes had been made 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 October 29, 2017. During that period, from a baseline of zero CSF shunt infections in the preceding two years, the hospital experienced six cases from January 30 to August 9, 2018. This meets the Center for Disease Control (CDC) 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% CI 5.1%-7.2%) reported among hospitals belonging to the Hydrocephalus Clinical Research Network (HCRN) – of which BCCH is a member – in 2016.[14] Given the high potential for morbidity and mortality associated with these infections, a retrospective case-control 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 case-control 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 January 30, 2018, and April 4, 2018. A timeline showing the cases, detection of the outbreak, and infection control measures is shown in Figure I. An initial meeting was held in April between infection prevention and control (IPAC) and neurosurgery to discuss the cases and assess whether there had been any changes in
3
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 multidisciplinary team consisting of medical microbiologists, IPAC, nursing, and neurosurgery 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 intra-abdominal surgeries being performed in that OR. Control measures were immediately implemented, including attempting to limit potentially contaminated cases done in the neurosurgical OR and putting signage on the door to limit traffic through the OR during CSF shunt cases. Airflow in the ORs was checked and found to be satisfactory. We contacted the manufacturer of the new shunt catheter and other local and HCRN member hospitals using the same brand of catheter to see if they had noted any changes to their CSF shunt infection rates, but no increases were reported. Despite the initial measures, three additional cases of CSF shunt infection were identified between June 27 and August 9, 2018. Further control measures were implemented in August after the audit was completed and presented to the relevant departments, including changing back to the previous brand of CSF catheter, disabling the automatic door opener after surgery had commenced, enlarging the ‘No Entry’ signs outside the OR, and enforcing that everyone in the OR 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 October 29, 2017, to June 30, 2018. The list was obtained from the surgical suites systems analyst. Patients who only had external ventricular drains (EVDs) inserted were excluded. A case was defined as a patient experiencing shunt infection within 90 days after 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: a) fever (temperature ≥38º C), OR b) neurological signs or symptoms (presence of any new neurological findings on examination, new or worsening lethargy, or worsening headache), OR
4
c) abdominal signs or symptoms (new or worsening abdominal cramps, tenderness on palpation, or the presence of guarding or rigidity), OR d) signs or symptoms of shunt malfunction or obstruction (evidence of new or worsening hydrocephalus, detected either by a rapidly enlarging head circumference [in children <2 years] or on CT 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 the surgery took place in, staff present (including assistants), length of the procedure, use of endoscopy or other instrumentation, and use and timing of pre-operative antibiotics; perioperative 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 (NSQIP) 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% confidence intervals, were calculated. Associations with p-values less than 0.2 were considered of potential interest for further investigation Results: In the time frame examined (Figure I), there were 6 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 the Streptococcus mitis group. The clinical features of the case patients are summarized in Table I. The median length from insertion of the shunt to the onset of symptoms 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 CSF white blood cell counts, from 3 to 1775. One of the 6 cases died. The peri-operative risk factors are shown in Table II. Only being a neonate and the presence of gastrointestinal disease met the statistical criteria for further interest. Age, sex and a history of prematurity were not associated with an increased risk of CSF shunt infection. There was no association between CSF shunt infection and the operating room, the surgeon or learner involved, the American Society of Anesthesiologists (ASA) 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.
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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 pre-operative intravenous antibiotics had any effect. The length of the procedure was also not linked to infection. Post-surgery, the number of times the shunt was accessed for CSF sampling was not associated with an increased risk of CSF shunt infection. Although there was no evidence linking the change in catheter model to the infections, the brand of catheter was changed back to the model that was used prior to the outbreak in August 2018. After the measures in Figure I were implemented, only one further case of CSF shunt infections has been identified as of December 10, 2019. That infection occurred on January 15, 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.
Discussion: In this study, we aimed to describe an outbreak of CSF shunt infections at our institution. Shunt infections are known to be associated with serious morbidity and mortality,[15] as well as prolonged hospital stays and the need for repeat surgeries. As a result, it was important that we tried to identify the cause of the outbreak and implement measures to arrest it. We examined multiple variables to attempt to find 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 also unusual in that only 50% were Staphylococcus species, 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. Perioperative risk factors indicated that no specific OR, surgeon, assistant or staff member was associated with increased CSF shunt infections, nor was the duration of surgery 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
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causative. Regarding the other control measures, specifically the limitation of human traffic through the OR, 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. There are, to our knowledge, no data demonstrating that the mandatory wearing of face masks prior to the opening of all surgical instrumentation reduces surgical site infections. There is evidence that the use of ultraviolet light after conventional cleaning methods reduces the risk of bacterial contamination in operating rooms.[19, 20] The strengths of this study were that this is, to our knowledge, the first investigation of a documented CSF shunt infection outbreak. We report what was investigated and the hospital actions in response, and note since the changes, there have been no new cases related to the outbreak. This study has several limitations. First, since the numbers of cases and controls were small, the study was underpowered to detect statistically significant associations. The fact that most risk factors studied did not meet statistical criteria for further investigation does not rule them out as being significant contributors to CSF shunt infection in this situation. Second, with regards to the changes implemented, because 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 let to changes in behavior we did not measure that contributed to the improvement. In summary, we report 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 subsequently, no further cases related to the outbreak have been reported.
References: [1] Hanak BW, Bonow RH, Harris CA, Browd SR. Cerebrospinal Fluid Shunting Complications in Children. Pediatric neurosurgery. 2017;52(6):381-400. [2] Prusseit J, Simon M, von der Brelie C, Heep A, Molitor E, Volz S, et al. Epidemiology, prevention and management of ventriculoperitoneal shunt infections in children. Pediatric neurosurgery. 2009;45(5):325-36. [3] McGirt MJ, Zaas A, Fuchs HE, George TM, Kaye K, Sexton DJ. Risk factors for pediatric ventriculoperitoneal shunt infection and predictors of infectious pathogens. Clinical infectious diseases : an official publication of the Infectious Diseases Society of America. 2003;36(7):858-62. [4] Serlo W, Fernell E, Heikkinen E, Anderson H, von Wendt L. Functions and complications of shunts in different etiologies of childhood hydrocephalus. Child's nervous system : ChNS : official journal of the International Society for Pediatric Neurosurgery. 1990;6(2):92-4. [5] Oterdoom LH, Marinus Oterdoom DL, Ket JCF, van Dijk JMC, Scholten P. Systematic review of ventricular peritoneal shunt and percutaneous endoscopic gastrostomy: a safe combination. Journal of neurosurgery. 2017;127(4):899-904. [6] Vui HC, Lim WC, Law HL, Norwani B, Charles VU. Percutaneous endoscopic gastrostomy in patients with ventriculoperitoneal shunt. The Medical journal of Malaysia. 2013;68(5):389-92.
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[7] Cochrane DD, Kestle JR. The influence of surgical operative experience on the duration of first ventriculoperitoneal shunt function and infection. Pediatric neurosurgery. 2003;38(6):295-301. [8] Cheng H, Chen BP, Soleas IM, Ferko NC, Cameron CG, Hinoul P. Prolonged Operative Duration Increases Risk of Surgical Site Infections: A Systematic Review. Surgical infections. 2017;18(6):722-35. [9] Horgan MA, Piatt JH, Jr. Shaving of the scalp may increase the rate of infection in CSF shunt surgery. Pediatric neurosurgery. 1997;26(4):180-4. [10] Merkler AE, Ch'ang J, Parker WE, Murthy SB, Kamel H. The Rate of Complications after Ventriculoperitoneal Shunt Surgery. World neurosurgery. 2017;98:654-8. [11] Kulkarni AV, Drake JM, Lamberti-Pasculli M. Cerebrospinal fluid shunt infection: a prospective study of risk factors. Journal of neurosurgery. 2001;94(2):195-201. [12] Yakut N, Soysal A, Kepenekli Kadayifci E, Dalgic N, Yilmaz Ciftdogan D, Karaaslan A, et al. Ventriculoperitoneal shunt infections and re-infections in children: a multicentre retrospective study. British journal of neurosurgery. 2018;32(2):196-200. [13] CDC Epidemiology Glossary USA: Centers for Disease Control and Prevention; 2015 [updated Page last reviewed: January 21, 2015. Epidemiology Glossary]. Available from: https://www.cdc.gov/reproductivehealth/data_stats/glossary.html. [14] Kestle JR, Holubkov R, Douglas Cochrane D, Kulkarni AV, Limbrick DD, Jr., Luerssen TG, et al. A new Hydrocephalus Clinical Research Network protocol to reduce cerebrospinal fluid shunt infection. Journal of neurosurgery Pediatrics. 2016;17(4):391-6. [15] Turgut M, Alabaz D, Erbey F, Kocabas E, Erman T, Alhan E, et al. Cerebrospinal fluid shunt infections in children. Pediatric neurosurgery. 2005;41(3):131-6. [16] Ochieng N, Okechi H, Ferson S, Albright AL. Bacteria causing ventriculoperitoneal shunt infections in a Kenyan population. Journal of neurosurgery Pediatrics. 2015;15(2):150-5. [17] Spiegelman L, Asija R, Da Silva SL, Krieger MD, McComb JG. What is the risk of infecting a cerebrospinal fluid-diverting shunt with percutaneous tapping? Journal of neurosurgery Pediatrics. 2014;14(4):336-9. [18] Weiser MC, Shemesh S, Chen DD, Bronson MJ, Moucha CS. The Effect of Door Opening on Positive Pressure and Airflow in Operating Rooms. The Journal of the American Academy of Orthopaedic Surgeons. 2018;26(5):e105-e13. [19] Simmons S, Dale C, Jr., Holt J, Passey DG, Stibich M. Environmental effectiveness of pulsed-xenon light in the operating room. American journal of infection control. 2018;46(9):1003-8. [20] El Haddad L, Ghantoji SS, Stibich M, Fleming JB, Segal C, Ware KM, et al. Evaluation of a pulsed xenon ultraviolet disinfection system to decrease bacterial contamination in operating rooms. BMC infectious diseases. 2017;17(1):672.
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Figures:
Figure I: Epidemic Curve and Implementation of Control Measures 2
Outbreak concern Initial meeting and start of investigation
Formal audit initiated Inquiries to catheter manufacturer Airflow in rooms checked Non-CSF surgeries in neurosurgical OR limited Reduced traffic in ORs
Catheter brand changed Automatic door sensor disabled Masking pre-equipment opening 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
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Tables:
Table I Clinical Features Variable Median days from OR to symptoms
Results 10 (5-53)
Fever
4 (66.7)
Neurological symptoms
3 (50.0)
Abdominal symptoms
4 (66.7)
Shunt malfunction
4 (66.7)
Median CSF WBC
490 (3-1775)
Mortality within 30 days
0
Mortality > 30 days
1 (16.7)
* Data are presented as median (range) or number (%) of patients.
Table II Perioperative Risk Factors Cases* Neonate at surgery 2 (33.3) Esophageal/gastric/ 3 (50.0%) intestinal disease Premature birth 4 (66.7)
Controls* 1 (5.3) 4 (21.1) 8 (42.1)
Odds Ratio 9.00 (0.65 – 125.32) 3.75 (0.54-26.19) 5.00 (0.46-54.04)
P value 0.10 0.18 0.67
Age, median years
1.9
3.1
0.99 (0.86-1.15)
0.89
0 Operations in preceding 90 days
3 (50.0)
13 (68.4)
Reference
-
1 Operation in preceding 90 days
1 (16.7)
4 (21.1)
1.08 (0.09-13.5)
0.61
2 Operations in preceding 90 days
2 (33.3)
2 (10.5)
4.33 (0.42-44.43)
0.231
Elective Case Status
1 (20.0)
4 (21.1)
Reference
-
10
Urgent Case Status
3 (50.0)
8 (42.1)
1.50 (0.12-19.44)
0.51
Emergency Case Status
1 (20.0)
7 (36.8)
0.57 (0.03-11.85)
0.54
Use of intraoperative antibiotics
1 (16.7)
1 (5.3)
3.6 (0.19-38.34)
0.39
Use of an endoscope
0
3 (16)
-
-
Attending surgeon A
3 (50.0)
8 (42.1)
Reference
-
Attending surgeon B
3 (50.0)
3 (15.8)
2.67 (0.33-21.32)
0.94
Attending surgeon C Presence of a resident
0 5 (83.3)
8 (42.1) 16 (84.2)
1.00 (0.08-11.93)
1.00
Presence of a fellow
4 (66.7)
14 (73.7)
0.77 (0.11-5.61)
0.80
Shunt accessed post 2 (33.3) 1 (5.3) 5.33 surgery (0.34-82.83) Shunt not accessed 3 (50.0) 8 (42.1) post surgery * Data are presented as median (range) or number (%) of patients.
0.23 -
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