Effect of Hand Antisepsis Agent Selection and Population Characteristics on Surgical Site Infection Pathogens

Abstract

Background:

Selection of a pre-operative hand antisepsis agent has not been studied in relation to surgical site infection (SSI) culture data. In our hospital, we introduced an alcohol-based hand rub (ABR) in 2012 as an alternative to traditional aqueous surgical scrubs (TSS). It was the goal of this study to review any effect of this implementation on SSI pathogen characteristics. In addition, we sought to compare our SSI culture data with available National Healthcare Safety Network (NHSN) data. We hypothesized that SSI pathogens and resistant isolates are affected by surgical hand antisepsis technique.

Methods:

Data collected prospectively between 2007 and 2014 were retrospectively analyzed for two time periods at the Veterans Affairs Boston Healthcare System (VABHS): Before ABR implementation (TSS group) and after (ABR group). Pathogen distribution and pathogenic isolate resistance profiles were compared for TSS and ABR, and similar comparisons, along with procedure-associated SSI comparisons, were made between VABHS and NHSN. All VABHS data were interpreted and categorized according to NHSN definitions.

Results:

Compared with TSS (n = 4,051), ABR (n = 2,293) had a greater rate of Staphylococcus aureus (42.6% vs. 38.0%), Escherichia coli (12.8% vs. 9.9%), Pseudomonas aeruginosa (8.5% vs. 2.8%), and Enterobacter spp. (10.6% vs. 2.8%), and a lower rate of Klebsiella pneumoniae/K. oxytoca (4.3% vs. 8.5%) cultured from superficial and deep SSIs (p < 0.05). Of the S. aureus isolates, 35.0% and 44.4% were resistant to oxacillin/methicillin (MRSA) in ABR and TSS, respectively (p = 0.06). Looking at all SSIs, coagulase-negative staphylococci and K. pneumoniae/K. oxytoca at VABHS (4.0% and 10.4%, respectively) accounted for the biggest difference from NHSN (11.7% and 4.0%, respectively). Aside from MRSA, where there was no difference between VABHS and NHSN (42.9% vs. 43.7%, respectively; p = 0.87), statistically significant (p < 0.05) differences were observed among multi-drug-resistant K. pneumoniae/K. oxytoca (0% vs. 6.8%, respectively) and Escherichia coli (10.0% vs. 1.6%, respectively), as well as among extended-spectrum cephalosporin-resistant K. pneumoniae/K. oxytoca (4.8% vs. 13.2%, respectively) and Enterobacter (58.3% vs. 27.7%, respectively). VABHS had a greater proportion of SSIs in abdominal and vascular cases than did NHSN (48.6% vs. 22.5% and 13.2% vs. 1.5%, respectively). Overall, these differences were significant (p < 0.05).

Conclusions:

The TSS and ABR groups differed in the distribution of pathogens recovered. Those differences, along with SSI pathogen distribution, pathogenic isolate resistance profiles, and procedure-associated SSIs between VABHS and NHSN, warrant further investigation.

Surgical site infections (SSIs) are a well established cause of morbidity, death, and excess cost [1]. Even with advancements in our surveillance and prevention methods, recent increasing antibiotic resistance has compounded these effects [2 –4]. A recent review reported that in the U.S., more than 38% of SSIs are caused by pathogens resistant to standard antibiotic prophylaxis; this has been corroborated in coronary artery bypass graft and arthroplasty procedures [5,6]. Antibiotic prophylaxis at the time of surgery mitigates (although it does not completely eliminate) the consequences of breaches in aseptic technique, but pathogen resistance negates this benefit [5,7]. Therefore, alternative methods for protecting against the transfer of microoranisms from surgical staff to the patient (e.g., hand hygiene, double-gloving) remain pertinent.

Proper surgical hand antisepsis is intended to eliminate or reduce transient and resident hand flora, respectively [8]. Although the relation between reduced hand inocula and SSIs remains imperfectly characterized, infection risk presumably is reduced when microorganisms are combated by traditional aqueous surgical scrubs (TSS) or alcohol-based hand rubs (ABR). Although neither product type has shown superiority, as judged by lower SSI rates, the impact on SSI pathogen distribution and resistance profiles has not been studied [9 –12]. Chlorhexidine, for example, alters skin flora quantity and characteristics, and resistance has been reported, but its clinical relevance remains to be determined, as user concentrations exceed those used for in vitro testing [13 –18]. Furthermore, SSI pathogen characteristics have not been compared between the Federal and private sector populations. U.S. Veterans, as a population, are unique in age, gender, socioeconomic status, and co-morbidity profile [19,20]. Population differences are therefore possible, as several of their baseline characteristics are also proven SSI risk factors.

At our Veterans Affairs hospital, an ABR was implemented in 2012 as an option for surgical hand antisepsis. This event naturally created pre- and post-ABR groups and allowed comparisons in pathogen distribution and resistance profiles. Our second objective in this study was to compare data among veterans with that reported to the National Healthcare Safety Network (NHSN), the U.S. Centers for Disease Control and Prevention (CDC)'s nationwide healthcare-associated infection tracking system.

Patients and Methods

Study design

This was a retrospective cohort study using prospectively collected data. The study was approved and granted a waiver of consent by the Veterans Affairs Boston Healthcare System (VABHS) Institutional Review Board and the local VA Research and Development Committee.

Study population

Patients who were assessed in the VA Surgical Quality Improvement Program (VASQIP) database at VABHS from January 1, 2007 to December 31, 2009 (TSS group) and from January 1, 2013 to December 31, 2014 (ABR group) were identified. Contaminated, dirty, ophthalmic, and oral and maxillofacial surgery cases were excluded. Cases between January 1, 2010 and February 1, 2012 were excluded due to inconsistent ABR availability, whereas cases between February 1, 2012 and December 31, 2012 were excluded to account for a period of acclimation. Education was provided to all staff upon introduction of the ABR option.

Study database

The VASQIP has been described [21]. In brief, it analyzes risk-adjusted 30-day morbidity and mortality data in select VA patients undergoing major surgery. A nurse reviewer trained in clinical medicine and quality assurance tracks this information and uses standard CDC NHSN definitions of operative procedure category and SSIs to ensure data reliability. Using patient identifiers, VASQIP data were cross-referenced to Veterans Health Information System and Technology Architecture data to identify any corresponding microbiology information for all reported SSIs. Pathogens were categorized into three groups: TSS (superficial and deep incisional SSIs [SDSSIs] only), ABR (SDSSIs only), and overall VABHS (all SSIs). All TSS, ABR, and overall VABHS data were defined according to the NHSN definitions for resistance and surgical specialty as defined by 2009–2010 data published in 2013 [22].

Statistical analysis

Chi-square tests were used to compare the following: SSI pathogen distribution between TSS and ABR, SSI pathogen distribution between VABHS and NHSN, SSI surgical specialty distribution between VABHS and NHSN, and SSI pathogen resistance profiles between TSS and ABR and between VABHS and NHSN. P < 0.05 was accepted as meaning statistically significant. All data analyses were performed using SAS v. 9.2 (SAS Institute Inc., Cary, NC).

Results

The VA External Peer Review Program reported a Surgical Care Improvement Project (SCIP) compliance rate of 97%–100% throughout both study periods. Double-gloving was common among surgical and nursing staff.

TSS vs. ABR pathogens

The SDSSI rates for TSS (n = 4,051) and ABR (n = 2,293) were similar (1.8% and 1.5%, respectively; p = 0.31). There were 71 organisms recovered from the 74 SDSSIs in the TSS period and 47 organisms recovered from the 34 SDSSIs in the ABR period (Table 1). Culture data were not available for 20 patients (19 TSS, 1 ABR). The distribution of pathogens differed significantly (p < 0.05) between TSS and ABR, with respective rates of Staphylococcus aureus (38.0% vs. 42.6%), Escherichia coli (9.9% vs. 12.8%), Pseudomonas aeruginosa (2.8% vs. 8.5%), Enterobacter spp. (2.8% vs. 10.6%) and Klebsiella pneumoniae/K. oxytoca (8.5% vs. 4.3%) responsible for the greatest differences. Pathogens with similar rates of infection in the two periods were coagulase-negative staphylococci (1.4% vs. 2.1%) and Enterococcus faecalis (4.2% vs. 4.3%). Although not cultured during the ABR period, other TSS pathogens included Proteus spp. (2.8%), Enterococcus faecium (2.8%), Serratia spp. (2.8%), and Candida albicans (1.4%). An additional 16 TSS (22.5%) and 7 ABR (14.9%) organisms were cultured and categorized as “other.”

Table 1.

Distribution of Pathogens Recovered Before (TSS) and After (ABR) Alcohol-Based Hand Rub Implementation at VABHS

Pathogen	TSS 2007–2009 No. (%) of pathogens	ABR 2013–2014 No. (%) of pathogens
Staphylococcus aureus	27 (38.0)	20 (42.6)
Coagulase-negative staphylococci	1 (1.4)	1 (2.1)
Escherichia coli	7 (9.9)	6 (12.8)
Enterococcus faecalis	3 (4.2)	2 (4.3)
Pseudomonas aeruginosa	2 (2.8)	4 (8.5)
Enterobacter spp.	2 (2.8)	5 (10.6)
Klebsiella (pneumoniae/oxytoca)	6 (8.5)	2 (4.3)
Enterococcus spp.	0	0
Proteus spp.	2 (2.8)	0
Enterococcus faecium	2 (2.8)	0
Serratia spp.	2 (2.8)	0
Candida albicans	1 (1.4)	0
Acinetobacter baumannii	0	0
Other Candida spp. or NOS	0	0
Other	16 (22.5)	7 (14.9)
Total	71 (100)	47 (100)

The overall distribution was significantly different between groups (p < 0.05).

ABR = alcohol-based hand rub; TSS = traditional aqueous surgical scrub; VABHS = Veterans Affairs Boston Healthcare System; NOS = not otherwise specified.

VABHS vs. NHSN pathogens

Overall, 202 pathogens (95% bacteria, 5% fungi) were cultured from the 158 SSIs (2.5%) at VABHS (n = 6,344); culture data were not available for 24 patients (Table 2). Four pathogens accounted for more than 50% of all cultured organisms: S. aureus (27.7%), E. coli (9.9%), K. pneumoniae or K. oxytoca (10.4%), and E. faecalis (7.4%). Other VABHS pathogens included Enterobacter spp. (5.9%), coagulase-negative staphylococci (4.0%), P. aeruginosa (4.0%), C. albicans (3.0%), other Candida spp. (2.0%), E. faecium (2.0%), Serratia spp. (1.5%), Proteus spp. (1.5%), and Enterococcus spp. (1.0%). The remaining 14 organisms (19.8%) were characterized as “‘other.” There was a statistically significant difference in pathogen distribution between VABHS and NHSN (p < 0.05), with coagulase-negative staphylococci (4.0% vs. 11.7%, respectively) and K. pneumoniae/K. oxytoca (10.4% vs. 4.0%, respectively) accounting for the greatest differences.

Table 2.

Distribution of Pathogens Recovered at VABHS Compared with Those Reported to NHSN (Sievert et al. [22])

Pathogen	NHSN 2009–10 No. (%) of pathogens	VABHS 2007–14 No. (%) of pathogens
Staphylococcus aureus	6,415 (30.4)	56 (27.7)
Coagulase-negative staphylococci	2,477 (11.7)	8 (4.0)
Escherichia coli	1,981 (9.4)	20 (9.9)
Enterococcus faecalis	1,240 (5.9)	15 (7.4)
Pseudomonas aeruginosa	1,156 (5.5)	8 (4.0)
Enterobacter spp.	849 (4.0)	12 (5.9)
Klebsiella (pneumoniae/oxytoca)	844 (4.0)	21 (10.4)
Enterococcus spp.	685 (3.2)	2 (1.0)
Proteus spp.	667 (3.2)	3 (1.5)
Enterococcus faecium	517 (2.5)	4 (2.0)
Serratia spp.	385 (1.8)	3 (1.5)
Candida albicans	267 (1.3)	6 (3.0)
Acinetobacter baumannii	119 (0.6)	0
Other Candida spp. or NOS	96 (0.5)	4 (2.0)
Other	3,399 (16.1)	40 (19.8)
Total	21,100 (100)	202 (100)

The overall distribution was significantly different between groups (p < 0.05).

NHSN = National Healthcare Safety Network; VABHS = Veterans Affairs Boston Healthcare System; NOS = not otherwise specified.

VABHS vs. NHSN procedure-associated SSIs

There were 14 VABHS cases that could not be characterized by NHSN definitions. The overall procedure distribution (Table 3) was significantly different (p < 0.05), with the greatest differences noted in orthopedic (VABHS 6.9% vs. NHSN 40.5%), abdominal (VABHS 48.6% vs. NHSN 22.5%), vascular (VABHS 13.2% vs. NHSN 1.5%), and neck (VABHS 8.3% vs. NHSN 0.1%) cases. The VABHS did not report any neurologic surgery SSIs, and there were few SSIs related to obstetrics/gynecology (0.7% vs. NHSN 9.6%) and breast (0.7% vs. NHSN 0.4%) cases. No transplant surgery operations were performed at VABHS.

Table 3.

Distribution of Procedure-Associated Surgical Site Infections at VABHS Compared with Those Reported to NHSN (Sievert et al. [22])

Type of surgery	NHSN 2009–10 No. (%) of SSIs	VABHS 2007–14 No. (%) of SSIs
Orthopedic^a	6,486 (40.5)	10 (6.9)
Abdominal^b	3,598 (22.5)	70 (48.6)
Cardiac^c	3,508 (21.9)	25 (17.4)
Obstetrics and gynecology^d	1,543 (9.6)	1 (0.7)
Neurologic^e	386 (2.4)	0
Vascular^f	245 (1.5)	19 (13.2)
Transplant^g	160 (1.0)	0
Breast^h	64 (0.4)	1 (0.7)
Neckⁱ	14 (0.1)	12 (8.3)
Other^j	15 (0.1)	6 (4.2)
Total	16,019 (100)	144 (100)

The overall distribution was significantly different between groups (p < 0.05).

Open reduction of fracture, hip prosthesis, knee prosthesis, limb amputation, spinal fusion, refusion of spine, or laminectomy.

Appendectomy, herniorrhaphy, or bile duct, liver, pancreatic, gallbladder, colon, gastric, small-bowel, spleen, abdominal, or rectal surgery.

Cardiac surgery, coronary artery bypass graft with chest incision with or without donor incision, pacemaker surgery, or thoracic surgery.

Cesarean section, abdominal hysterectomy, ovarian surgery, or vaginal hysterectomy.

Craniotomy or ventricular shunt.

Abdominal aortic aneurysm repair, shunt for dialysis, carotid endarterectomy, or peripheral vascular bypass surgery.

Heart transplant, kidney transplant, or liver transplant.

Breast surgery.

Neck surgery and thyroid and/or parathyroid surgery.

Prostate surgery or kidney surgery.

NHSN = National Healthcare Safety Network; VABHS = Veterans Affairs Boston Healthcare System.

Pathogen resistance

Antimicrobial resistance, as defined by NHSN, was identified in 43 VABHS isolates (21.3%) (Table 4). The most common organisms with antibiotic resistance were extended-spectrum cephalosporin (ESC)-resistant Enterobacter spp. (58.3%), oxacillin-methicillin (OX/METH)-resistant S. aureus (MRSA; 42.9%), and fluoroquinolone-resistant E. coli (25.0%). These compared with NHSN rates of 27.7%, 43.7%, and 25.3%, respectively. The remaining organisms showing a great difference between VABHS and NHSN were vancomycin-resistant E. faecium (VABHS 25.0% vs. NHSN 62.3%), aminoglycoside-resistant P. aeruginosa (12.5% vs. 6.0%), ESC-resistant E. coli (10.0% vs. 10.9%), multi-drug-resistant (MDR) E. coli (10.0% vs. 1.6%) and ESC K. pneumoniae/K. oxytoca (4.8% vs. 13.2%). All isolate resistance profiles at VABHS differed significantly from those of NHSN (p < 0.05) with the exception of OX/METH-resistant S. aureus (p = 0.87). Furthermore, several resistant isolates reported by NHSN were not found among VABHS pathogens. Too few cases of resistance existed among the TSS (n = 17) and ABR (n = 12) groups to compare statistically with the exception of OX/METH-resistant S. aureus isolates (TSS 12 [44.4%] vs. ABR 7 [35.0%]; p = 0.06).

Table 4.

Resistance of Pathogens to Select Antimicrobial Agents at VABHS Compared with NHSN (Sievert et al. [22])

Pathogen isolated, antimicrobial given	NHSN 2009–10 No. (%) of resistance	VABHS 2007–2014 No. (%) of resistance
Staphylococcus aureus	2,755 (43.7)	24 (42.9)
OX/METH
Enterococcus faecium	317 (62.3)	1 (25.0)
VAN
Enterococcus faecalis	74 (6.2)	0
VAN
Klebsiella (pneumoniae/oxytoca)
ESC4	94 (13.2)	1 (4.8)
Carbapenems	46 (7.9)	0
MDR1	42 (6.8)	0
Escherichia coli
ESC4	177 (10.9)	2 (10.0)
FQ3	475 (25.3)	5 (25.0)
Carbapenems	27 (2.0)	0
MDR1	22 (1.6)	2 (10.0)
Enterobacter spp.
ESC4	226 (27.7)	7 (58.3)
Carbapenems	14 (2.4)	0
MDR1	11 (1.7)	0
Pseudomonas aeruginosa
AMINOS	40 (6.0)	1 (12.5)
ESC2	112 (10.2)	0
FQ2	188 (16.9)	0
Carbapenems	96 (11.0)	0
PIP/PIPTAZ	56 (6.8)	0
MDR2	56 (5.3)	0
Acinetobacter baumannii
Carbapenems	38 (37.3)	0
MDR3	50 (43.9)	0

The distribution was significantly different between groups for each pathogen (p < 0.05) except Staphylococcus aureus (p = 0.87).

AMINOS = aminoglycosides (amikacin, gentamicin, tobramycin); carbapenems = imipenem or meropenem; ESC2 = extended-spectrum cephalosporin (cefepime, ceftazidime); ESC4 = (ESC2 plus cefotaxime or ceftriaxone); FQ2 = fluoroquinolone (ciprofloxacin, levofloxacin); FQ3 = FQ2 plus moxifloxacin; MDR1 = pathogens tests rated as “I” (intermediate) or “R” (resistant) to at least one drug in three of the five following classes: ESC4, FQ3, aminoglycosides, carbapenems, and piperacillin or piperacillin-tazobactam; MDR2 = substitute ESC2, FQ2 in MDR1; MDR3 = MDR2 plus ampicillin-sulbactam; NHSN = National Healthcare Safety Network; OX/METH = oxacillin-methicillin; PIP = piperacillin, PIPTAZ = piperacillin-tazobactam; VABHS = Veterans Affairs Boston Healthcare System; VAN = vancomycin.

Discussion

Over time, and with the introduction of an ABR for surgical hand antisepsis at our institution, we have shown changes in the distribution of SDSSI pathogens. We have further demonstrated differences between nationally reported data and our overall SSI pathogen distribution and the frequency of resistant isolates. With an estimated 60% of SSIs deemed preventable [1], these data are valuable to guide surgical anti-microbial prophylaxis, infection control measures, and initial antimicrobial therapy.

Compared with the TSS period, the proportion of S. aureus, E. coli, P. aeruginosa, and Enterobacter spp. in SDSSIs increased in the ABR period, whereas the proportion of K. pneumoniae/K. oxytoca decreased. Previous studies have not found a change in isolated pathogens between ABR and TSS [10,23], and any difference may be attributed to trends over time [24 –27] or perhaps to the microbiome of the hospital or clinical setting [28,29] rather than the hand antisepsis agent. The true value of using one agent more than another also may be underestimated, as approximately 10% of ABR users and 18% of TSS users at our facility apply the product more quickly than the recommended duration (unpublished quality improvement survey data). The possibility thus exists that incorrect product application affects pathogen selection and susceptibility.

Although SCIP compliance at our instituation was 97%–100% during our study period, antibiotic selection based both on the procedure being conducted and its correlation to local microbiology data should be investigated. Thus, ESC resistance was noted for 10 pathogens (5.0%) in the VABHS group. A study of spinal surgery evaluated resistance to cefazolin specifically and noted its presence in almost two-thirds of their gram-negative infections [30]. The results of this study are not supportive of changing current surgical antibiotic prophylaxis protocols but suggest the necessity for tailoring prophylaxis on the basis of local microbiology and antibiograms [21,31]. With regard to procedure type, the results herein provide the ability for our institution to target those to which the highest proportion of SSIs are attributed, namely abdominal, cardiac, and vascular procedures.

The VA patient population may be implicated in differences noted between our local institution and private sector data. Compared with the private sector, VA patients historically have greater age-adjusted mortality rates [32] and a larger number of co-morbidities on average compared with a Medicare cohort [33].

This study has several limitations, including its retrospective nature, the inability to control for changes in clinical practice over time, unknown user compliance with manufacturer-recommended product application, double gloving variability among staff, surgical hand antisepsis product selection at the time of surgery by all surgical personnel, and missing culture results. Because users were not randomized prospectively to a product type (e.g., TSS or ABR), it is not possible to identify which users in the ABR period chose to use the newly introduced ABR product versus which continued to use the TSS or utilized both.

Conclusion

The distribution changes of SSI pathogens between our two cohorts may be, in part, attributable to the addition of an ABR for use in performing surgical hand antisepsis. However, as differences also were noted between the overall local VA institution and NHSN data, we speculate that time, environment, changes in practice or patient population, or regional differences in resistant pathogens also were implicated. The SSI pathogen and resistance profile data are vital to an individual institution's evaluation and the tailoring of prophylactic antibiotics or empiric treatment in the event of an SSI. Future efforts should randomize and prospectively track surgical hand antisepsis product use while standardizing surgical antibiotic prophylaxis, double-gloving, and empiric treatment guidelines at an institution-specific level.

Footnotes

Author Disclosure Statement

The opinions expressed are those of the authors and do not necessarily reflect those of the US Department of Veterans Affairs.

BSO, QC, and KW have no competing financial interests. KMFI has received research funds to his institution from Merck, Sanofi, and Dr. Reddy's Laboratories, and he has been a research consultant for Irrimax.

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