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Journal of Hospital Infection 86 (2014) 24e33

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Journal of Hospital Infection

journal homepage: www.elsevierhealth.com/journals/jhin

Clinical and economic burden of surgical site infection (SSI) and predicted financial consequences of elimination of SSI from an English hospital

P.J. Jenks a,*, M. Laurent b, S. McQuarry c, R. Watkins b

a Departments of Microbiology and Infection Prevention and Control, Derriford Hospital, Plymouth, UK b ICNet International, Stroud, UK c Department of Finance, Derriford Hospital, Plymouth, UK

A R T I C L E I N F O

Article history: Received 10 June 2013 Accepted 26 September 2013 Available online 16 October 2013

Keywords: Attributable cost Healthcare-associated infection Length of stay Margin (profitability) Opportunity cost Surgical site infection

* Corresponding author. Address: Departme mouth Hospitals NHS Trust, Derriford Hospital Tel.: þ44 (0) 1752 439010; fax: þ44 (0) 1752

E-mail address: [email protected] (P.J.

0195-6701/$ e see front matter ª 2013 The http://dx.doi.org/10.1016/j.jhin.2013.09.012

S U M M A R Y

Background: Although surgical site infections (SSIs) are known to be associated with increased length of stay (LOS) and additional cost, their impact on the profitability of surgical procedures is unknown. Aim: To determine the clinical and economic burden of SSI over a two-year period and to predict the financial consequences of their elimination. Methods: SSI surveillance and Patient Level Information and Costing System (PLICS) datasets for patients who underwent major surgical procedures at Plymouth Hospitals NHS Trust between April 2010 and March 2012 were consolidated. The main outcome measures were the attributable postoperative length of stay (LOS), cost, and impact on the margin differential (profitability) of SSI. A secondary outcome was the predicted financial consequence of eliminating all SSIs. Findings: The median additional LOS attributable to SSI was 10 days [95% confidence in- terval (CI): 7e13 days] and a total of 4694 bed-days were lost over the two-year period. The median additional cost attributable to SSI was £5,239 (95% CI: 4,622e6,719) and the aggregate extra cost over the study period was £2,491,424. After calculating the oppor- tunity cost of eliminating all SSIs that had occurred in the two-year period, the combined overall predicted financial benefit of doing so would have been only £694,007. For seven surgical categories, the hospital would have been financially worse off if it had success- fully eliminated all SSIs. Conclusion: SSI causes significant clinical and economic burden. Nevertheless the current system of reimbursement provided a financial disincentive to their reduction. ª 2013 The Healthcare Infection Society. Published by Elsevier Ltd. All rights reserved.

nt of Microbiology, Ply- , Plymouth PL6 8DH, UK. 517725. Jenks).

Healthcare Infection Society.

Introduction

In the most recent point prevalence survey of inpatients in England, surgical site infection (SSI) was again the third most frequently occurring healthcare-associated infection (HCAI), causing 15.7% of reported infections.1 As well as resulting in substantial morbidity and mortality to patients who have undergone surgical procedures, SSI contributes to the burden

Published by Elsevier Ltd. All rights reserved.

P.J. Jenks et al. / Journal of Hospital Infection 86 (2014) 24e33 25

on providers of healthcare services by prolonging the duration of hospital stay and increasing costs.2e8 Comprehensive, evidence-based guidelines exist for the prevention of SSI and many carefully conducted studies have successfully reduced rates of wound sepsis by a combination of effective interven- tion and feedback of data on infection rates to surgical teams.7,9e13 Despite the success in some areas of HCAI pre- vention in England, most notably the fall in incidence of MRSA bacteraemia and Clostridium difficile, a similar reduction in SSI rates has not occurred.1,14 Few hospitals in England have the resources to perform comprehensive surveillance of sur- gical procedures and recent studies have confirmed that SSIs are significantly underestimated in the national surveillance programme facilitated by Public Health England (formerly the English Health Protection Agency).7,15,16 In 2009, concerns that there was inadequate information for English hospitals on the adverse effects of SSI in defined categories of surgical pro- cedures were raised by the Public Accounts Committee who, having reviewed the national SSI surveillance system, concluded that the true scale of SSIs in England was not un- derstood because of a ‘lack of decent data’.17

A critical step in convincing organizations to allocate scarce resources to infection control programmes is to demonstrate that these interventions will not only reduce the rate of infection, but will also result in savings that exceed the cost of preventive strategies.18,19 A better un- derstanding of the financial burden of SSI would help justify decisions on the economic benefit of greater investment in evidence-based interventions to prevent them. An effective SSI prevention programme should also be able to demon- strate a valuable return on investment through ongoing de- livery of quantifiable health benefits by releasing

Table I

Surgical site infection (SSI) and return of post-discharge questionnaire

Surgical category No. of procedures

No. (%) of PDQs returned

No. (%) during a

Cardiac 1672 970 (58) 25 Vascular 401 176 (44) 5 Limb amputation 291 102 (35) 3 Hip replacement 980 588 (60) 6 Knee replacement 970 543 (56) 0 Reduction long bone fracture

1503 631 (42) 6

Repair neck of femur 598 305 (51) 1 Cranial 896 278 (31) 2 Spinal 1827 713 (39) 2 Abdominal hysterectomy

402 273 (68) 3

Caesarean section 1837 1745 (95) 16 Breast 1016 569 (56) 3 Bile duct, liver, pancreatic

222 124 (56) 9

Cholecystectomy 46 23 (50) 1 Gastric 228 121 (53) 4 Large bowel 673 337 (50) 41 Small bowel 259 117 (45) 15 Multiple intra-abdominal 385 193 (50) 17 Multiple other procedures 94 47 (50) 3 All procedures 14,300 7854 (55) 162

hospital resources for alternative use and beds for new admissions.18e20 The additional cost associated with SSI has not been fully elucidated due to inconsistencies in study design and variation in methods of cost calculation.18,19,21 In general, previous studies have allocated hospital costs using the additional length of stay (LOS) associated with SSI, a method that may introduce bias and therefore be inaccurate.5e8,19e22 Despite these problems, a recent review comparing studies of magnitude of costs due to SSI estimated that the healthcare cost for a patient with SSI is likely to be approximately twice that of one without.23 This contrasts with the latest total attributable hospital cost due to SSI estimated by the National Institute for Health and Clinical Excellence (NICE) of £469 per infection.9

A dedicated team at Plymouth Hospitals NHS Trust has conducted surveillance of SSI, including for infections developing after discharge from hospital, with feedback to surgeons for all major surgical procedures since January 2009. In April 2010, the hospital introduced a Patient Level Information and Costing System (PLICS) that combines data from a range of administrative, clinical and financial systems to allocate cost to individual patient episodes, and allowing linkage of financial and clinical outcomes. In the present study, we sought to quantify the clinical and economic burden of SSI through analysis of PLICS data for patients who underwent surgical site surveillance at our hospital between April 2010 and March 2012. We aimed to obtain a measure of the attributable cost of SSI and also the margin (profitability) differential between patients with and without SSI for different surgical categories. In addition, we sought to pre- dict the financial consequences of the elimination of all SSIs that occurred over the study period.

s (PDQs) by surgical category

of SSIs dmission

No. (%) of SSIs on readmission

No. (%) of SSIs post discharge

Total SSIs (overall SSI rate)

(1.5) 18 (1.1) 137 (8.2) 180 (10.8) (1.2) 7 (1.8) 16 (4.0) 28 (7.0) (1.0) 4 (1.4) 6 (2.1) 13 (4.5) (0.6) 5 (0.5) 5 (0.5) 16 (1.6)

6 (0.6) 25 (2.6) 31 (3.2) (0.4) 13 (0.9) 12 (0.8) 31 (2.1)

(0.2) 6 (1.0) 7 (1.2) 14 (2.3) (0.2) 7 (0.8) 0 9 (1.0) (0.1) 9 (0.5) 7 (0.4) 18 (1.0) (0.7) 2 (0.5) 9 (2.2) 14 (3.5)

(0.9) 9 (0.5) 114 (6.2) 139 (7.6) (0.3) 11 (1.1) 35 (3.4) 49 (4.8) (4.1) 1 (0.5) 11 (5.0) 21 (9.5)

(2.2) 2 (4.4) 3 (6.5) 6 (13.0) (1.8) 2 (0.9) 3 (1.3) 9 (4.0) (6.1) 12 (1.8) 33 (4.9) 86 (12.8) (5.8) 1 (0.4) 8 (3.1) 24 (9.3) (4.4) 3 (0.8) 18 (4.7) 38 (9.9) (3.2) 2 (2.1) 2 (2.1) 7 (7.4) (1.1) 120 (0.8) 451 (3.2) 733 (5.1)

P.J. Jenks et al. / Journal of Hospital Infection 86 (2014) 24e3326

Methods

Setting, study population and SSI surveillance

The study was performed at Derriford Hospital, a 1200-bed university hospital in England that is part of Plymouth Hospitals NHS Trust and provides specialist services to the south west peninsula, including cardiac, liver, upper gastrointestinal and neurosurgery. Between April 2010 and March 2012, 13,854 emergency and 58,203 elective surgical operations were per- formed, of which 36,611 were day-case procedures. During this period, prospective surveillance of SSI for all major surgical categories involving incision of the skin (listed in Table I) was performed using the Surgical Site Infection Surveillance Service (SSISS) protocol established by Public Health England (formerly the English Health Protection Agency).24 Patients who under- went coronary artery bypass graft and/or valve surgery were combined in a single cardiac surgery category. Those who had multiple intra-abdominal or multiple other surgical procedures were consolidated under these named categories (Table I). Standard data collection for surgical inpatients was performed as previously described by a dedicated surveillance team of healthcare assistants that had been trained to recognize the signs and symptoms of SSI.25 An automated surveillance soft- ware and data collection and storage system, ICNet SSI Monitor (version 6.2.3, ICNet International Ltd, Stroud, UK), that interfaced with the hospital patient administration and microbiology systems, was used to prospectively collect sur- veillance data and also to identify readmissions to the hospital. Post-discharge surveillance was performed using a question- naire modified from that described by Wilson et al. which pa- tients were asked to return using a reply paid envelope 28 days following discharge.7 When necessary, additional information was obtained from the primary care team by telephone inter- view. The presence of a surgical wound infection was deter- mined using the SSISS definitions, which are modified from those used by the US Centers for Disease Control.24,26 For SSIs, the date of onset, site, type (superficial, deep or organ space) and microbial pathogens involved were recorded. Organ space infection was included in deep infection in the present study. A patient record (episode) was defined as a surgical procedure with postoperative follow-up, including readmission, termi- nated by another surgical procedure or lapse of 12 months. The incidence or rate of SSI during admission, on readmission or following discharge from hospital was defined as the number of SSIs per 100 operations for each surgical category. Outcome and economic analysis was limited to SSIs occurring during admission or on readmission, with the latter aggregated with those of the original admission to form a single patient episode.

Cost and outcome data and definitions

Income, cost and outcome data for each individual patient episode was extracted from the hospital PLICS, which uses the Allocate Speciality and Procedure Pricing System (SAPPS) costing model (Allocate Software, London, UK) based on the national reference costs published annually by the Department of Health (http://www.dh.gov.uk/health/category/policy- areas/nhs/resources-for-managers/nhs-costing/) and using published clinical costing standards.27 Each patient was allo- cated a Healthcare Resource Group (HRG) code using an

amalgamation of the International Classification of Diseases V.10 (ICD-10) and Office of Population Censuses and Surveys Classification of Surgical Operations and Procedures V.4.5 (OPCS-4.5).28,29 Individual patient income was derived from locally or nationally agreed HRG-specific tariff. Additional remuneration was allocated for high-cost medical devices not included within tariff. Episodes for patients whose stay exceeded the nationally defined expected length of stay (LOS) on critical care areas also received additional reimbursement on a per diem basis.27 All individual patient costs were fully absorbed from the hospital’s accounting and activity systems, and therefore included all non-duplicated costs associated with staff, diagnostic and other activities, consumables and overheads attributable to each individual episode. Patient identifiable costs, such as diagnostic investigations, consum- ables and any applied financial penalties (for example, for readmission to hospital), were attributed directly to individual episodes. Overhead and staffing costs were derived as a func- tion of the main cost driver as outlined in national clinical costing standards (for example, ward costs used LOS as the main cost driver and were apportioned using time of bed oc- cupancy and bed rate).27

Outcome data, including postoperative LOS and readmission indicators, were also allocated by the PLICS to individual pa- tient episodes. Postoperative LOS was defined as the period of inpatient stay between the day of operation until the day of discharge, reoperation or death. Case mortality data were gathered retrospectively from deaths registered with the Per- sonal Demographics Service (www.connectingforhealth.nhs. uk) and used to generate KaplaneMeier curves, with survival analysed up to 90 days following the surgical procedure. The log-rank chi-square test was used to determine whether there was a difference in survival between non-SSI and SSI patients.30

P � 0.05 was considered significant.

Data and statistical analysis

Surgical site surveillance and PLICS data were imported from ICNet SSI Monitor into the MySQL relational database system (Oracle Corporation UK Ltd, Reading, UK) and the datasets consolidated using the common patient identifier and date of admission. As part of the consolidated dataset, the postoperative LOS, income and cost associated with any linked readmissions were aggregated with those of the original admission to form a single patient episode.

A retrospective matched cohort analysis was performed in order to obtain postoperative LOS and aggregate cost attributable to individual SSI episodes. Individual SSI cases were matched to a minimum of eight non-SSI episodes on the basis of a combination of surgical category, HRG code, age and the NNIS system risk index.31 Median postoperative LOS and aggregate cost for SSI and matched non-SSI cohorts were calculated for each surgical category using R, which is open- source software for statistical computing, analysis and graphics (available at http://www.r-project.org/).32,33 The postoperative LOS and cost attributable to SSI patient epi- sodes were derived from the difference between the post- operative LOS and cost for each SSI and the benchmark values for the matching cohort of non-SSI cases in each sur- gical category. Data are reported for each surgical category as the aggregated total and median values with 95% confi- dence interval (CI). Statistical analysis was performed using

P.J. Jenks et al. / Journal of Hospital Infection 86 (2014) 24e33 27

the ManneWhitney U-test. P � 0.05 was considered significant.

To assess the impact of SSIs on profitability, the mean value of the difference between cost and revenue for each of these groups in individual surgical categories was calculated. The category-specific opportunity cost was derived by assuming a zero rate of SSI and calculating the predicted financial margin available to the hospital if it chose to use released bed-days to perform the maximum possible addi- tional procedures based on the median total (i.e. preopera- tive and postoperative) non-SSI LOS for that category. The overall financial impact of eliminating all SSIs was calculated by aggregating the opportunity cost and the savings made from eliminating all SSIs (the gross margin of the SSI episodes of each surgical category).

Results

Surgical site infections

During the two-year period of surveillance, 14,870 surgical episodes were followed. For 197 episodes, it was not possible to consolidate SSI surveillance and PLICS data using patient identifiers and dates of admission, and these were excluded from further analysis. A further 371 non-SSI episodes relating to private or Ministry of Defence patients were excluded as cost and outcome data on these non-NHS episodes were not

Table II

Additional attributable postoperative length of stay (LOS)a due to sur mission by surgical category

Surgical category No. of SSIs Total LOS attributa to SSI (days)

Cardiac 43 1159 Vascular 12 231 Limb amputation 7 83 Hip replacement 11 252 Knee replacement 6 67 Reduction long bone fracture 19 335 Repair neck of femur 7 161 Cranial 9 58 Spinal 11 238 Abdominal hysterectomy 5 86 Caesarean section 25 142 Breast 14 70 Bile duct, liver, pancreatic 10 132 Cholecystectomy 3 35 Gastric 6 171 Large bowel 53 731 Small bowel 16 259 Multiple intra-abdominal

20 385

Multiple other procedures

5 99

All categories 282 4694 a LOS aggregated for original admission and linked readmissions. b P < 0.05. c Insufficient episodes to generate confidence interval (CI).

collected by the hospital PLICS. Finally, after a further two episodes without an allocated HRG code had been excluded, 14,300 episodes were included for further analysis.

The number and rate of SSIs and return of post-discharge questionnaires by surgical category are shown in Table I. Of the 282 SSIs identified during admission and readmission, 98 (34.8%) were deep or organ space and 184 (65.2%) were su- perficial infections. Post-discharge follow-up was performed on 7854 (55%) patients and a further 451 (3.2%) infected wounds were found, of which 48 (10.6%) were deep or organ space and 403 (89.4%) superficial infections. A significant microbiological pathogen was grown from 389 (53%) wounds, and although Staphylococcus aureus was the frequently found isolate, responsible for 33.2% infections, meticillin-resistant S. aureus (MRSA) was rare, both relative to other micro- organisms and in absolute terms. Coagulase-negative staphy- lococci were an important cause of infection in cardiac surgery and surgery involving prosthetic material.

Length of stay, readmission to hospital and mortality

The median postoperative LOS for patients with and without SSI, and additional attributable LOS due to SSI by surgical category derived from the matched cohort analysis, are shown in Table II. The median additional LOS attributable to SSI for all surgical categories over the two-year period was 10 days (95% CI: 7e13 days). The median postoperative LOS of patients who developed a superficial or deep or organ space SSI was

gical site infection (SSI) identified during admission and on read-

ble Median postoperative LOS (95% CI)

Median attributable LOS (95% CI) of SSI

Non-SSI SSI

7 (6e7) 29 (27e36)b 23 (19e30) 6 (6e7) 17 (8e32)b 10 (5e22) 6 (4e7) 16a,b 10c

6 (6e6) 22 (8e63)b 17 (1e57) 6 (6e6) 14a,b 7c

3 (3e4) 18 (6e34)b 5 (0e32) 10 (9e10) 31b,c 19c

5 (5e6) 13 (2e28) 1 (e3 to 17) 1 (1e1) 16 (7e29)b 13 (6e27) 4 (3e4) 17b,c 14c

2 (2e2) 7 (5e10)b 4 (2e7) 1 (1e1) 4 (3e9)a 3 (1e4) 8 (7e8) 22 (15e30)b 12 (4e24) 5 (3e7) 10b,c 8c

8 (7e9) 41b,c 29c

8 (8e9) 19 (14e25)b 11 (5e13) 7 (6e8) 21 (13e33)b 12 (6e26)

11 (10e11) 19 (14e33)b 7 (2e20)

20 (11e23) 36c 20c

5 (5e5) 19 (17e21)b 10 (7e13)

Table III

Additional attributable costa due to surgical site infection (SSI) by surgical category

Category Total cost attributable

to SSIs

No. of SSIs Median cost (95% CI) Median cost attributable to SSI (95% CI)

Non-SSI SSI

Cardiac £722,537 43 £11,606 (11,459e11,849) £22,236 (19,719e26,598)b £11,003 (8,517e15,395) Vascular £96,106 12 £7,314 (6,591e7,909) £10,251 (7,797e15,014)b £2,480 (e757 to 9,209) Limb amputation £36,764 7 £5,051 (4,337e5,721) £7,945c £6,799c

Hip replacement £84,105 11 £7,438 (7,319e7,616) £15,114 (7,971e24,812)b £3,214 (657e17,040) Knee replacement £30,928 6 £6,917 (6,738e6,924) £9,528b £2,356c

Reduction long bone fracture

£174,816 19 £4,495 (4,310e4,693) £7,775 (5,453e16,183)b £4,982 (284e11,873)

Repair neck of femur £79,840 7 £5,786 (5,476e6,001) £18,448b,c £12,104c

Cranial £83,559 9 £7,693 (7,249e7,930) £14,155 (8,803e37,467)b £2,662 (5e20,297) Spinal £135,251 11 £4,029 (3,946e4,112) £13,380 (10,629e24,975)b £7,076 (3,391e17,945) Abdominal hysterectomy

£26,629 5 £3,733 (3,586e3,886) £9,510b,c £5,983c

Caesarean section £97,021 25 £3,572 (3,491e3,634) £7,467 (4,655e9,455)b £3,716 (894e4,905) Breast £52,647 14 £2,893 (2,793e2,991) £4,835 (3,665e10,655)b £1,469 (1,123e4,058) Bile duct, liver, pancreatic

£70,030 10 £9,121 (8,579e9,748) £14,808 (10,728e24,643)b £2,838 (e141 to 14,218)

Cholecystectomy £19,469 3 £4,500 (2,859e5,662) £9,052b,c £6,236c

Gastric £133,034 6 £9,159 (7,115e11,867) £34,509b,c £21,493c

Large bowel £328,860 53 £6,770 (6,328e7,031) £12,951 (9,790e14,508)b £4,928 (4,020e7,503) Small bowel £111,587 16 £5,391 (4,698e6,310) £10,466 (5,229e17,957)b £6,198 (e424 to 9,254) Multiple intra-abdominal

£121,707 20 £10,937 (10,289e11,879) £14,104 (9,154e22,736) £1,495 (e3,121 to 11,712)

Multiple other procedures

£83,533 5 £14,850 (11,066e19,413) £29,548b,c £9,696c

All categories £2,491,424 282 £5,837 (5,743e5,925) £12,928 (11,191e14,311)b £5,239 (4,622e6,719) a Cost aggregated for original admission and linked readmissions. b P < 0.05. c Insufficient episodes to generate confidence interval (CI).

P.J. Jenks et al. / Journal of Hospital Infection 86 (2014) 24e3328

significantly increased to 17 days (95% CI: 13e18 days) and 24 days (95% CI: 21e29 days) respectively compared with 5 days (95% CI: 5e5 days) for those who did not develop an infection (P < 0.01). The median additional postoperative LOS attribut- able to superficial SSIs and deep or organ space SSIs was 8 days (95% CI: 7e11.5 days) and 15 days (95% CI: 11e22 days) respectively. Over the two-year period, the aggregate addi- tional LOS attributable due to SSIs was 4694 days (equivalent to 6.4 beds per day), with a range of 35 extra days for cholecys- tectomy to 1159 days for cardiac surgery (Table II).

The diagnosis of SSI was made during an episode of read- mission to hospital in 120 patients (Table I). The proportion of all patients who were subsequently readmitted to hospital was significantly higher for those who developed an SSI during their initial admission than those that did not (24.7% vs 7.9%, P < 0.001). Patients who underwent hip replacement, bile duct, liver or pancreatic surgery and large bowel surgery, and who developed an SSI during their initial admission, were signifi- cantly more likely to be readmitted than uninfected patients. When considering all patients who developed an SSI at any time following surgery, including following discharge from hospital, these were also more likely to be readmitted to hospital than those who did not (25.4% vs 7.9%, P < 0.001). Patients who un- derwent cardiac, vascular, hip replacement, reduction of long bone fracture, repair neck of femur, spinal surgery, lower segment caesarean section, breast and large bowel surgery and

who developed an SSI at any time following surgery, including following discharge from hospital, were significantly more likely to be readmitted than uninfected patients.

During the study period there were 490 deaths in the non-SSI and 21 deaths in the SSI group (data not shown). There was no significant difference in mortality rate between SSI and non-SSI patients in any of the surgical categories followed.

Economic evaluation

The additional attributable cost due to SSI by surgical category is shown in Table III. The median additional cost attributable to SSI for all surgical categories over the two-year period was £5,239 (95% CI: 4,622e6,719). The median cost of patients who developed a superficial or deep or organ space SSI was significantly higher at £11,020 (9,510e12,462) and £17,242 (14,368e19,719) respectively compared with £5,837 (5,743e5,925) for those who did not develop an infection (P < 0.01). The median additional cost attributable to super- ficial SSIs and deep or organ space SSIs was £4,656 (2,988e5,487) and £6,690 (5,713e8,969) respectively. Over the two-year period, the aggregate additional cost attributable to SSIs was £2,491,424, with a range of £19,469 for cholecystec- tomy to £722,537 for cardiac surgery (Table III).

For all surgical categories, w11% of the additional cost attributable to SSI was related to operating theatre costs, 24%

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Figure 1. Breakdown of costs of non-surgical site infection (SSI) (light grey bars) and SSI episodes (dark grey bars) for all surgical categories.

P.J. Jenks et al. / Journal of Hospital Infection 86 (2014) 24e33 29

to stay on the general ward and a further 10% was incurred by stay on critical care areas (Figure 1). Medical and other staff accounted for 18% and 2% respectively of SSI-related costs; diagnostics, wound dressings, antibiotics and other therapies accounted for a further 12%. The impact of the development of an SSI on cost categories varied for different surgical pro- cedures (data not shown). As expected, ward and staffing costs associated with SSI episodes increased for all surgical cat- egories and was related to the longer LOS of these patients. Critical care cost was particularly high for SSI episodes in car- diac, cranial, gastric and bile liver and pancreatic surgery due to longer initial patient stay in these areas or return to critical care following wound debridement or other surgical interven- tion for the management of SSI. The increase in pharmacy services and other drug costs for SSI episodes was largely accounted for by use of antibiotics and was particularly marked in cardiac, orthopaedic, spinal and complex intra-abdominal surgery where prolonged courses of antimicrobial therapy were frequently used to treat wound infections. The cost of prosthetics and implants was higher in patients with SSIs who had undergone reduction of long bone fracture, repair of neck of femur, and cranial and breast surgery, and reflects increased use of, or replacement of, prosthetic material in patients in these categories with SSI. The cost associated with use of blood products was particularly increased in SSI episodes in cardiac, vascular, hip replacement, repair of neck of femur, gastric and bile, liver and pancreatic surgery.

The impact of SSI on profitability by surgical category is shown in Table IV. The mean income received per patient episode for each surgical category is also shown and was higher for SSI compared with non-SSI patients for all categories of surgery other than limb amputation. With the exception of bile, liver and pancreatic surgery and cardiac surgery, which made profits of £30,528 and £3,569,139 respectively, the hos- pital made an aggregate loss on all categories of surgery for non-SSI patient episodes. The overall loss for the two-year period for non-infected patients for the categories covered by surveillance was £6,994,982, with a mean loss of £499 per episode. The hospital continued to receive income for patients who developed an SSI and paradoxically made a net profit of £882 for cholecystectomy and £13,472 for small bowel surgery patients with SSIs. For all the other surgical categories, the development of an SSI resulted in a higher mean loss per pa- tient episode, with the largest impact on patients undergoing gastric surgery, with a loss per patient episode of £16,967 (compared with a loss of £3,068 per non-SSI patient). When considering all surgical categories combined, the hospital made a mean loss of £3,843 per SSI patient episode. The overall loss for the two-year period for SSI patients was £1,083,726, giving a combined loss for all surgical procedures covered by the surveillance programme of £8,078,708.

The category-specific opportunity costs and the predicted overall financial impact of eliminating all SSIs are shown in Table V. Since the hospital made a loss on all surgical categories

P.J. Jenks et al. / Journal of Hospital Infection 86 (2014) 24e3330

except for bile, liver and pancreatic surgery and cardiac sur- gery, these were the only categories with a positive opportu- nity cost. However, because the hospital continued to receive income for SSI episode, the overall predicted financial benefit of eliminating all SSIs was less than the cost attributable to SSI for all surgical categories. Despite this, there was still a financial incentive to have eliminated all SSIs and doing so would have generated a profit in 12 of the 19 surgical cat- egories. For example, for cardiac surgery, eliminating all SSIs, which had an attributable cost of £722,537 (Table III), would have released an additional 1159 beds, allowing an extra 144 procedures to have been performed with an opportunity cost of £315,504, which, when combined with the gross margin (sav- ings) associated with the SSI episodes (£49,708), would have resulted in an additional profit of £365,212 for the hospital over the two years. Despite ten of the surgical categories having a negative opportunity cost, the impact of the savings associated with eliminating SSIs would still have been sufficient to generate a positive overall financial impact. An example was vascular surgery, where despite the opportunity cost of �£19,012 that would have been generated by performing an additional eight non-SSI procedures, the £62,496 gross margin that would have been generated from eliminating SSIs would have resulted in an additional profit of £43,484. This compares with the attributable cost of SSI in vascular surgery of £96,106. However, for hip surgery, reduction of long bone fracture, spinal surgery, abdominal hysterectomy, breast surgery, chole- cystectomy and small bowel surgery, the savings made from eliminating all SSIs would not have been enough to have given an overall positive financial impact. For example, for hip sur- gery, eliminating SSIs that had an attributable cost of SSI of £84,105 would have resulted in the ability to perform an additional six procedures at a loss of £81,396. However, the

Table IV

Income received and margin for patient episodes without and with sur

Surgical category Non-SSI

No. Mean income Mean margina

Cardiac 1629 £16,178 £2,191 Vascular 389 £9,041 �£679 Limb amputation 284 £7,067 �£250 Hip replacement 969 £6,526 �£1,938 Knee replacement 964 £6,520 �£953 Reduction long bone fracture 1484 £5,497 �£65 Repair neck of femur 591 £6,587 �£268 Cranial 887 £10,200 �£143 Spinal 1816 £5,070 �£1,150 Abdominal hysterectomy 397 £3,343 �£1,007 Caesarean section 1812 £3,394 �£535 Breast 1002 £2,540 �£741 Bile duct, liver, pancreatic 212 £10,192 £144 Cholecystectomy 43 £4,740 �£475 Gastric 222 £7,699 �£3,068 Large bowel 620 £8,748 �£674 Small bowel 243 £7,437 �£515 Multiple intra-abdominal 365 £9,911 �£2,732 Multiple other procedures 89 £11,964 �£7,098 All categories 14,018 £7,191 �£499 a Mean value of difference between cost and revenue for individual ca b Aggregate value of difference between cost and revenue for all case

£76,472 gross margin generated from preventing all SSIs would have been insufficient to compensate this, resulting in an overall loss of £4,924 for this category.

Discussion

This is the first study to combine surgical site surveillance infection data with individual patient-level income and costing information to give a comprehensive analysis of the clinical and economic impact of SSI on a hospital. By defining opportunity costs, this is also the first study to indicate that there may be perverse incentives in not preventing at least some SSIs. The overall incidence of SSI during the initial inpatient episode or on readmission was 2.0%, and following discharge from hospital was 3.2%. Although the most significant microbiological path- ogen causing SSI was S. aureus, rates of infection with MRSA were low, reflecting the fall in incidence of MRSA bacteraemia both in our hospital and nationally.1,14 The median LOS of infected patients in individual surgical categories increased approximately three- to four-fold and, over the two years, a total of 4694 bed-days were lost due to SSI (equivalent to 6.4 beds per day). Patients who developed an SSI were approxi- mately three times more likely to be readmitted to hospital and the cost of their combined inpatient stay was higher than that of non-infected patients, with a total attributable SSI cost of £2,491,424 over the study period. The LOS on general and critical care wards was an important determinant of the overall cost of SSI episodes, but theatre and medical staffing costs were also major contributors. For SSI in certain surgical cat- egories, specific high costs, for example linked to increased use of antibiotics and prosthetics and implants, were identified. Whereas surveillance was targeted on the more complex and hence more costly surgical procedures, it is notable that the

gical site infection (SSI) by surgical category

SSI

Gross margin No. Mean income Mean margin Gross marginb

£3,569,139 43 £27,889 �£1,156 �£49,708 �£264,131 12 £10,766 �£5,208 �£62,496 �£71,000 7 £6,719 �£2,159 �£15,113 �£1,877,922 11 £10,067 �£6,952 �£76,472 �£918,692 6 £6,910 �£5,053 �£30,318 �£96,460 19 £8,015 �£6,645 �£126,255 �£158,388 7 £11,265 �£6,006 �£42,042 �£126,841 9 £19,427 �£706 �£6,354 �£2,088,400 11 £9,249 �£10,936 �£120,296 �£399,779 5 £8,556 �£1,167 �£5,835 �£969,420 25 £5,100 �£2,546 �£63,650 �£742,482 14 £5,242 �£2,231 �£31,234 £30,528 10 £15,870 �£1,856 �£18,560

�£20,425 3 £9,534 £294 £882 �£681,096 6 £15,504 �£16,966 �£101,796 �£417,880 53 £10,736 �£3,690 �£195,570 �£125,145 16 £13,681 £842 £13,472 �£997,180 20 £13,052 �£5,084 �£101,680 �£631,722 5 £22,034 �£10,127 �£50,635 �£6,994 982 282 £13,186 �£3,843 �£1,083,726 ses within a surgical category. s within a surgical category.

Table V

Opportunity cost and overall financial impact of eliminating all surgical site infections (SSIs) by surgical category

Surgical category Total LOS attributable to SSI

Mean total non-SSI LOS

No. of additional proceduresa

Mean non-SSI margin

Opportunity costb

Gross SSI margin

Overall financial impactc

Cardiac 1159 8 144 £2,191 £315,504 �£49,708 £365,212 Vascular 231 8 28 �£679 �£19,012 �£62,496 £43,484 Limb amputation 83 9 9 �£250 �£2,250 �£15,113 £12,863 Hip replacement 252 6 42 �£1,938 �£81,396 �£76,472 �£4,924 Knee replacement 67 6 11 �£953 �£10,483 �£30,318 £19,835 Reduction long bone fracture

335 6.5 51 �£65 �£3,315 �£126,255 �£122,940

Repair neck of femur 161 12 13 �£268 �£3,484 �£42,042 £38,558 Cranial 58 6 9 �£143 �£1,287 �£6,354 £5,067 Spinal 238 1 238 �£1,150 �£273,700 �£120,296 �£153,404 Abdominal hysterectomy

86 4 21 �£1,007 �£21,147 �£5,835 �£15,312

Caesarean section 142 3 47 �£535 �£25,145 �£63,650 £38,505 Breast 70 1 69 �£741 �£51,129 �£31,234 �£19,895 Bile duct, liver, pancreatic

132 9 14 £144 £2,016 �£18,560 £20,576

Cholecystectomy 35 7 5 �£475 �£2,375 £882 �£3,257 Gastric 171 9 18 �£3,068 �£55,224 �£101,796 £46,572 Large bowel 731 9 81 �£674 �£54,594 �£195,570 £140,976 Small bowel 259 8 32 �£515 �£16,480 £13,472 �£29,952 Multiple intra- abdominal

385 12 32 �£2,732 �£87,424 �£101,680 £14,256

Multiple other procedures

99 22 4 �£7,098 �£28,392 £50,635 £22,243

All categories 4694 6 781 �£499 �£389,719 �£1,083,726 £694,007 LOS, length of stay. a No. of additional procedures ¼ (total LOS attributable to SSI) � (median total non-SSI LOS). b Opportunity cost ¼ (no. of additional procedures) � (mean non-SSI margin). c Overall financial impact ¼ (opportunity) � (gross SSI margin).

P.J. Jenks et al. / Journal of Hospital Infection 86 (2014) 24e33 31

hospital lost almost £7 million on surgical procedures not complicated by SSI and that only two categories generated a profit. Although the development of SSI generally resulted in a greater financial loss per patient episode, this was mitigated by the hospital continuing to receive income for episodes complicated by SSI. This resulted in the paradoxical situation in which patients who developed SSI following cholecystectomy and small bowel surgery generated a profit for the hospital, whereas those that did not resulted in a loss. Furthermore, after calculating the opportunity cost of eliminating all SSIs that occurred in the two-year period, we found that the overall predicted financial benefit of eliminating all SSIs was less than the aggregate cost attributable to SSI for each surgical cat- egory. The combined overall predicted financial benefit of preventing all SSIs for all surgical categories would only have been £694,007 compared with the aggregate attributable cost of SSI of £2,491,424. Strikingly, for seven surgical categories, the hospital would have been financially worse off if had it successfully eliminated all SSIs.

Only a few recent studies have examined the clinical and economic impact of SSI on English hospitals. A survey of hos- pitals participating in the national surveillance scheme be- tween October 1997 and June 2001 found that the additional LOS due to SSI for nine surgical categories ranged from 3.3 days for abdominal hysterectomy to 21.0 days for limb amputation.6

Although the additional cost attributable to SSI was similar in most surgical categories, this was higher in our study for car- diac surgery (£11,003 vs £3,894) and abdominal hysterectomy (£5,983 vs £959). A review of infection data from University College London Hospital NHS Trust between 2000 and 2004 reported the mean increased cost associated with SSI to be £4,018, which, accounting for inflation, is a similar value to the median cost attributable to SSI found in our study.7 One other study, which included costs incurred by primary care following discharge from hospital, found the additional cost of treating a colorectal SSI to be £10,523.8 No other studies have examined the impact of SSI on profitability or have estimated the po- tential financial impact of their elimination.

Since few hospitals in England perform comprehensive continuous surveillance of surgical procedures, a strength of this study is that we were able to define the incidence of SSI for the majority of surgical procedures using consistently applied definitions and robust surveillance systems.7,15,16 In addition, we were able to use PLICS to measure income and cost over the full cycle of individual patient episodes and compare this with outcome, in this case the development of SSI. Whereas previ- ous studies have based their analysis on modelling techniques that estimate the specialty-specific cost per bed-day and then allocated this to SSI and non-SSI episodes by multiplying by LOS, we were able to obtain an accurate financial measure of the

P.J. Jenks et al. / Journal of Hospital Infection 86 (2014) 24e3332

impact of infection at the individual patient level.2,3,5,6,8

Because PLICS combines cost and income data from a range of administrative, clinical and financial systems, we were also able to build a picture of the various costs associated with each hospital episode, including staffing, consumables, drugs, di- agnostics and overheads. A further strength was that we were able to determine the margin (profitability) differential be- tween patients with and without infection, but otherwise having a similar case mix, and use this to model the potential financial impact that eliminating all SSIs would have had on our hospital.

The main weakness of our study is that it considers data from a single hospital in England. Although comparison with other centres would be revealing, very few would have access to a similar breadth of SSI surveillance data and be able to interface this with costing data from a system such as PLICS.7,15,16 A number of factors suggest that our findings are likely to be representative of other hospitals in England. Although published data on SSI rates for a number of cat- egories, such as gastric and bile, liver and pancreatic surgery, are limited, the overall and category-specific rates of SSI in this study are broadly similar to those reported else- where.6e8,13,31,34 Similarly, patient income for surgical pro- cedures was derived from an agreed HRG-specific tariff system that would apply to other hospitals in England. To counter this, the introduction of feedback of infection rates and the intro- duction of other interventions, such as MRSA screening in car- diac surgery, has led to a fall in the incidence of SSI at our hospital, and this could potentially limit comparison with other hospitals and have biased the predicted financial benefits of further reduction.25 Another limitation is that patients read- mitted to other hospitals were not included in our analysis. The number of episodes involved was small and unlikely to have significantly affected the overall findings of the study. Finally, up to 15% of the financial burden of SSI is thought to be borne by the community, and we did not consider the additional costs to primary care services of SSIs occurring in hospital or of those infections that developed following discharge from hospital.8

Our study does not therefore account for the financial impact of SSI on the community healthcare sector, or to patients and their carers.

Determination of the incidence as well as the clinical and financial burden of HCAIs is of critical importance for patients, providers and commissioners who must make rational and informed decisions about patient care and allocation of re- sources. There are currently no national surveillance systems to determine the number of common HCAIs, including SSI, and, despite evidence that surveillance of wound infections can be cost-effective in the NHS environment, few hospitals have dedicated surveillance and feedback programmes.7,15,16 In addition, there is limited appreciation of the economic burden of SSIs, making it difficult to assess the scale of potential sav- ings to hospitals if cost-effective preventive programmes are instituted and maintained.

Our study has highlighted a number of issues with the way our hospital is currently reimbursed for surgical procedures and on whether preventive programmes would be cost-effective. Although only high-risk, expensive surgical procedures were included in the surveillance programme, the hospital suffered financial loss for the majority of categories, even in the absence of SSI. Whereas across the hospital this is balanced by other profit-making categories of surgery, these results raise

the question as to whether the losses could be reduced by implementation of efficiencies and/or review of the national tariff for these procedures. During the study period, a number of financial penalties, for example for readmission, were applied to the hospital. Despite these penalties and the sig- nificant additional attributable cost of SSI, the fact that the hospital continued to receive income for SSI episodes meant that the impact of infection on profitability was less than anticipated. The presence of a paradoxical financial disincen- tive for SSI reduction was confirmed when the opportunity cost of eliminating all SSIs was calculated and the financial benefit to the hospital was found to be less than the aggregate attributable cost of SSI over the same period for each surgical category. Indeed, the hospital would have been financially worse off if it had eliminated all SSIs in seven of the 19 surgical categories. A recent US study has reported a similar phenom- enon, with the occurrence of post-surgical complications associated with a higher contribution margin for certain pa- tients, resulting in the potential for near-term adverse finan- cial implications for reducing post-surgical complication.35

While such a system is clearly undesirable, introducing finan- cial penalties, or not including HCAIs in tariff, is controversial and may have unintentional consequences, including a reluc- tance to record and share results openly. The policy change by Medicare to deny payment for what were considered to be preventable infections appears to have influenced the report- ing of SSI by institutions in order to minimize financial loss.36e38

Rather than using a remuneration process that disincentivizes improvements in clinical practice or imposing disproportionate target penalties, developing a system based on financial re- wards, perhaps similar to the Commissioning for Quality and Innovation (CQUIN) system, would be more likely to be pro- ductive and be better received by clinicians. Accurate local surveillance and costing data could be used to both inform appropriate financial incentives and guide decisions about the economic value of introducing or expanding preventive interventions.

In conclusion, SSIs cause significant clinical and economic burden. The current system of reimbursement at our hospital provides a financial disincentive to reducing SSI. Further studies are required to determine whether this applies to other hospitals within the NHS.

Acknowledgements

We thank M. Hollow, C. Haill, G. Parker and S. Reid who were contributors to this manuscript through collection of SSI and outcome data.

Conflict of interest statement M.L. and R.W. are employees of ICNet International, a company that markets management, surveillance and reporting software for healthcare-associated infections.

Funding sources None.

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