Abstract
Surgical site infections (SSI) in open Hepatopancreatobiliary (HPB) surgery are common complications. They worsen patients’ outcomes and prolong hospital stays. Their economic significance in the German diagnosis related groups (DRG) system is mostly unknown. To investigate their economic importance, we evaluated all cases for SSIs as well as clinical and financial parameters undergoing surgery in our centre from 2015 and 2016. Subsequently, we carried out a cost‐revenue calculation by assessing our billing data and the cost matrix of the InEK (German Institute for the Payment System in Hospitals). A total of 13.5% of the patients developed a superficial, 9% a deep incisional, and 2.4% of the patients an organ space SSI. Compared with Patients without SSI, Patients with SSI had more comorbidities, were older, and their average length of stay was extended by 19 days (P < .001). The financial loss per SSI‐case was €‐7035.65 despite increased reimbursement, which resulted in a calculated total loss for the hospital of €‐802 064.62 in 2015 and 2016. Surgical site infections are common complications of open HPB surgery, which lead to a significant increase in the cost per case. Further prevention strategies need to be developed. Besides, an adjustment of revenues must be demanded.
Keywords: biliary tract surgical procedures (D001662), costs and cost analysis (D003365), length of stay (D007902), liver (D008099), surgical wound infection (D013530)
1. INTRODUCTION
Hepatopancreatobiliary (HPB) surgery includes surgery of the liver, bile ducts, and pancreas. These operations range from resections of the smallest liver lesions to complex hepatic and pancreatic resections lasting hours. The possible complications are as heterogeneous as the operations themselves. These complications range from bile duct stenosis and leaks, fluid collections, anastomotic leakage, bleeding, and liver failure to surgical site infections (SSI). 1 These SSIs are classified according to the centers for disease control and prevention (CDC) classification into superficial, deep incisional, and organ space SSIs. 2
With 18.4% in Europe in 2016 3 and 21.8% in the USA in 2014, 4 SSIs account for a considerable proportion of hospital‐acquired infections. In a recently published guideline of SSI treatment, the WHO underlined the importance of their prevention . 5 However, the evidence of the measures proposed is consistently weak. The frequency of SSIs varies greatly and depends on the author and the particular surgical specialty studied. In HPB‐surgery SSI rates of 25.1% after pancreatoduodenectomy 6 and 23.2% after hepatic and pancreatic resections have been reported. 7 The genesis of SSIs is not yet clearly understood. Much research has examined the influence of various extrinsic and intrinsic factors on the genesis of SSIs, 8 but in many cases, this cannot explain the occurrence of SSIs. It is undisputed that SSIs lead to prolonged hospitalisation and readmission, 9 re‐operations, and increased costs of treatment. 10 However, the resulting values for the health care system are difficult to assess. In addition to the costs for hospitals resulting from more extended inpatient stays and operations without adequate reimbursement, further economic damages arise from prolonged incapacity to work and outpatient wound care costs. Systematic analyses of the additional expenses caused by wound infections are rare and show massive fluctuations depending on the underlying calculation model, indication area, and author. When interpreting these data, the country of data collection should also be taken into account, as significant differences can exist, particularly in reimbursement. However, all authors describe that an SSI leads to a financial loss despite an additional refund. 11 , 12 In the strict German diagnosis related groups (DRG) system, Graf et al showed in a matched case‐control study in thoracic surgery that the occurrence of an SSI compared to the control population leads to a deficit of €‐12 482 versus a gain of €484 despite additional revenue. Wolters et al showed an increase in the debt per treatment case from €1128 to €5471 in patients after cystectomy. German data on the economic relevance of SSIs in HPB surgery are entirely lacking.
Therefore, we aimed to analyse the relevance of SSI in HPB surgery at a German university hospital and to examine the economic consequences in the context of the German DRG system.
2. MATERIALS AND METHODS
2.1. Study design
In this retrospective study, we analysed 431 patients who underwent open HPB‐surgery in 2015 and 2016 at the University Medical Center Regensburg (UKR) for the primary endpoint, occurrence of SSI. These were mostly complex hepatic resections, highly complex operations on the bile ducts and pancreas resections, and liver transplants. The case‐mix‐index of the examined cases was seven, which underlines the complexity of the treatments.
2.2. Collection of variables
All variables were determined by studying patient records. Besides socio‐demographic information such as height, weight, body mass index, and age, previous illnesses were recorded as well as personal risk scores such as American Society of Anaesthesiologists (ASA) classification and wound contamination class. All measured variables are listed in Tables 1 and 2. Target variable SSI was recorded by evaluating the standardised wound documentation sheets of the nursing documentation and by evaluating physicians letters and medical documentation. During the inpatient stay, the SSIs were classified as superficial, deep incisional, and organ space SSI according to the depth of infection following the centers for disease control and prevention (CDC) guidelines.
TABLE 1.
Patient characteristics (n = 431)
| Variable | No SSI (n = 323) | SSI (n = 108) | P value | |||
|---|---|---|---|---|---|---|
| Age | <50 | 79 | (85.9%) | 13 | (14.1%) | .006 |
| ≥50 | 243 | (71.9%) | 95 | (28.1%) | ||
| Gender | Male | 180 | (69.5%) | 79 | (30.5%) | .001 |
| Female | 143 | (83.1%) | 29 | (16.9%) | ||
| ASA score | 1 | 20 | (87%) | 3 | (13%) | <.001 |
| 2 | 124 | (82.7%) | 26 | (17.3%) | ||
| 3 | 148 | (70.8%) | 61 | (29.2%) | ||
| 4 | 15 | (55.6%) | 12 | (44.4%) | ||
| 5 | 2 | (50%) | 2 | (50%) | ||
| Diabetes | No | 260 | (76.9%) | 78 | (23.1%) | .070 |
| Yes | 63 | (67.7%) | 30 | (32.3%) | ||
| Malignancy | No | 118 | (74.2%) | 41 | (25.8%) | .790 |
| Yes | 205 | 75.4%) | 67 | (24.6%) | ||
| Anaemia | No | 125 | (83.9%) | 24 | (16.1%) | .020 |
| Yes | 198 | (70.2%) | 84 | (29.8%) | ||
| CAD | No | 290 | (77.1%) | 86 | (22.9%) | .006 |
| Yes | 33 | (60%) | 22 | (40%) | ||
| COPD | No | 308 | (75.9%) | 98 | (24.1%) | .760 |
| Yes | 15 | (60%) | 10 | (40%) | ||
| Smoker | No | 268 | (74.7%) | 91 | (25.3%) | .756 |
| Yes | 55 | (76.4%) | 17 | (23.6%) | ||
| Alcohol | No | 289 | (75.9%) | 92 | (24.1%) | .228 |
| Yes | 34 | (68%) | 16 | (32%) | ||
| Immobility | No | 283 | (77.7%) | 81 | (22.3%) | .002 |
| Yes | 40 | (59.7%) | 27 | (40.3%) | ||
| Chronic kidney disease | No | 297 | (76.3%) | 92 | (23.7%) | .040 |
| Yes | 26 | (61.9%) | 16 | (38.1%) | ||
| Liver cirrhosis | No | 282 | (77%) | 84 | (23%) | .017 |
| Yes | 41 | (63.1%) | 24 | (36.9%) | ||
| Body mass index [kg/m2] | Mean | 25.8 | 26.7 | .098 | ||
| SD | 5.54 | 5.28 | ||||
| Anti‐coagulation | No | 265 | (77.7%) | 76 | (22.3%) | .003 |
| Yes | 57 | (64%) | 32 | (36%) | ||
TABLE 2.
Perioperative characteristics
| Variable | SSI No (%) | SSI Yes (%) | P value | |||
|---|---|---|---|---|---|---|
| Emergency procedure | No | 296 | (76.1%) | 93 | (23.9%) | .093 |
| Yes | 27 | (64.3%) | 15 | (35.7%) | ||
| Contamination class | Clean‐cont. | 284 | (76.1%) | 21.5 | (23.9%) | .194 |
| Contaminated | 30 | (66.7%) | 29.5 | (33.3%) | ||
| Dirty‐Infected | 9 | (69.2%) | 16.7 | (30.8%) | ||
| Incision | Median | 168 | (78.5%) | 46 | (21.5%) | .117 |
| Transversal | 39 | (79.6%) | 10 | (20.4%) | ||
| L‐formed | 103 | (70.5%) | 43 | (29.5%) | ||
| Subcostal | 12 | (57.1%) | 9 | (42.9%) | ||
| Packing | No | 300 | (77.7%) | 86 | (22.3%) | .000 |
| Yes | 23 | (51.1%) | 22 | (48.9%) | ||
| Preoperative biliary drainage | No | 283 | (75.9%) | 90 | (24.1%) | .55 |
| PTCD | 19 | (67.9%) | 9 | (32.1%) | ||
| ERCP | 6 | (60%) | 4 | (40%) | ||
| ERCP + Stent | 15 | (75%) | 5 | (25%) | ||
| Duration of operation (min) | Mean | 241 | 266 | .113 | ||
| SD | 108 | 128 | ||||
2.3. Statistical analysis
Categorical variables are presented as absolute and relative frequencies, and continuous variables either as mean (standard deviation) or as median (first quartile, third quartile), depending on the underlying distribution. Normality was assessed using the Shapiro–Wilk test. Nominally scaled variables were compared using the Chi‐squared test of independence, ordinal, and skewed variables were compared using the Kruskal–Wallis test, and normally distributed variables were compared by using an analysis of variance (ANOVA). All P‐values less than .05 were considered statistically significant. Statistical analyses were performed by using IBM SPSS statistics 25.
2.4. Analysis of the cost/income statement
Our controlling department provided data about the length of stay, respective DRG, and reimbursement per case. The costs per case were calculated using the cost matrix of the InEK and compared to the compensation per case. In order not to overestimate the effect, we have chosen a conservative calculation model. Since not every patient with SSI required a re‐operation, and some patients without SSI required one, we did not include the calculated surgery costs of the initial DRG in the calculation of the additional costs. We underestimated the actual costs at best.
3. RESULTS
3.1. Frequency of SSIs
A total of 108 (25.1%) patients developed a surgical site infection. Superficial SSIs occurred in 58 (13.5%), deep incisional SSIs in 39 (9%), and organ space SSIs were the least frequent in 11 (2.4%) cases (Table 3). The interventions were heterogeneously distributed over the operations of HPB surgery.
TABLE 3.
Surgical Site Infections in HPB‐surgery
| Overall HPB‐procedures (n = 431) | Hepatic procedures (n = 289) | Pancreatic procedures (n = 79) | Biliary procedures (n = 63) | ||||||
|---|---|---|---|---|---|---|---|---|---|
| No SSI | 323 | (74.9%) | 211 | (73.0%) | 64 | (81.0%) | 48 | (76.2%) | P = .337 |
| SSI | 108 | (25.1%) | 78 | (27.0%) | 15 | (19.0%) | 15 | (23.8%) | |
| Incisional SSI | 58 | (13.5%) | 39 | (13.5%) | 9 | (11.4%) | 10 | (13.5%) | |
| Deep incisional SSI | 39 | (9.0%) | 29 | (10.0%) | 5 | (6.3%) | 5 | (7.9%) | |
| Organ Space SSI | 11 | (2.6%) | 10 | (3.5%) | 1 | (1.3%) | 0 | (2.6%) | |
Most of the operations investigated were hepatic resections. These patients also showed the highest probability of occurrence of SSIs. Of the 289 patients, 78 (27%) developed SSI. In 79 pancreatic operations, SSIs occurred in 15 (19%) patients, and in 63 biliary procedures, 15 patients developed an SSI (24%). The statistical analysis showed no significant difference between the three indications (P = .523).
Incisional and deep incisional SSIs were detected in 17.4% of median, 18.4% of transverse, 27.5% of L‐shaped, and 42.9% of subcostal incisions (P = .117).
The cohort also includes 13 patients who underwent hemihepatectomy or left‐lateral liver resection for living donor liver transplantation. In contrast to the other hemihepatectomy‐patients, none of them developed an SSI (P = .010).
3.2. Patient‐ and perioperative characteristics
As shown in Table 1, SSIs occurred more frequently in patients aged over 50 years (28.1% / 14.1%, P = .006) and in males (30.5%/ 16.9%, P = .001). As the American Society of Anaesthesiologists (ASA) score increased, so did the rate of SSI (P < .001). As a further expression of multimorbidity, SSIs occurred more frequently in immobile patients (40.3%/ 22.3%, P = .002), patients with coronary heart disease (40%/ 22.9%, P = .006), and chronic kidney disease (38.1% / 23.7%, P = .040). Similarly, more patients with liver cirrhosis (36.9%/ 23%, P = .017) and postoperative anaemia (29.8%/ 16.1%, P = .020) developed SSIs. After intraabdominal packing during initial surgery, SSI occurred more often than without (48.9%/ 22.3%, P < .001). Other examined, patient‐centred (Table 1) as well as procedural characteristics (Table 2) showed no statistically significant impact for the development of a SSI.
3.3. Length of hospital stay
As a basis for further economic studies, we determined the median length of hospital stay (LOS) with and without SSI. The median LOS of all patients with HPB surgery was 17 (11, 30) days. Patients without SSI stayed 15 (10, 24) days while patients with superficial stayed 24 (17, 37), with deep incisional 40 (29, 56) with organ space SSI 50 (34, 74) days. The occurrence of an SSI prolonged the median hospital stays up to 34 days (P < .001) (Figure 1). Since other serious complications naturally occur in HPB surgery and can, in principle, influence the LOS, we only analysed those patients who did not develop any other complications in further analysis (n = 321). Here the median LOS was 14 (10, 20) days without, 20 (15, 28)) days with superficial and 36.5 (29, 42) days with deep incisional SSI. Superficial SSIs, therefore, seem to prolong the LOS about 6 days, deep incisional SSIs about 22.5 days.
FIGURE 1.
The median length of stay of patients in hpb‐surgery. Patients without SSI remained 15 (10, 24) days in the hospital, patients with superficial SSI 24 (17, 37), with deep incisional SSI 40 (29, 56), and with organ space infection 50 (34, 74) days. Error bars represent 95% CI
3.4. Economic aspects of wound infections in HPB surgery
The economic analysis of all patients revealed that patients stayed in the hospital, on average, 1.1 days longer than the average LOS specified in the respective DRG. Therefore, the revenue‐loss calculation results in a deficit of €‐681 per patient. If a wound infection was present, the deficit per patient increased to €‐7.303. Since the patients also had other complications such as bile leakage, hematomas, or fluid retentions, we also analysed only those patients who did not show any further complications. In this 253 Patients containing group, we calculated a deficit per patient of €‐116. Here, the average length of stay deviates only a few hours from the average LOS calculated in the DRG. In the case of an SSI (n = 54), we recorded a deficit of €‐5.676. All economic aspects are shown in Table 4.
TABLE 4.
Cost−/ reimbursement calculation of SSI in HPB‐surgery
| Overall | Without other complications | |||||
|---|---|---|---|---|---|---|
| No SSI | SSI | P‐value a | No SSI | SSI | P‐value a | |
| Calculated mean costs per case | €21 663 | €45 646 | <.001 | €17 694 | €27 477 | <.001 |
| Mean reimburse‐ment per case | €20 982 | €38 343 | <.001 | €17 579 | €21 800 | <.001 |
| Mean profit / loss | €‐681 | €‐7303 | <.001 | €‐116 | €‐5676 | <.001 |
| Overall profit loss | €‐212 353 | €‐781 369 | €‐29 232 | €‐306 524 | ||
| Number of cases | 349 | 114 | 253 | 54 | ||
Mann–Whitney U test was used.
4. DISCUSSION
HPB surgery represents a heterogeneous field of surgery from simple cholecystectomy to highly complex, multi‐stage oncological liver resections. To investigate the economic aspects of HPB surgery, we developed a cost‐profit model based on the German DRG system. Calculations based on this cost‐profit model, which allow us also to depict costs of highly complex cases, show that in a centre of the highest level of care, cost coverage cannot be achieved. In our cohort with a casemix index of 7, treatments are complicated and lead to prolonged hospital stays. The median LOS of all patients without SSI in our collective was 17 days. With this, the patients already exceeded the average LOS based on DRG regulations by 1 day, which meant an average deficit of ‐ €681 per patient. Due to SSIs, the median LOS increased dramatically up to 34 days, which was reflected in the economic analysis. Since inpatient care is organised differently in other health care systems than in Germany, data on LOS are only comparable to a limited extent. For example, other authors found only an extension of the LOS after pancreatoduodenectomy from 7 to 8 days for superficial and 11 days for deep incisional SSIs. 13 The average LOS calculated in the DRG for comparable pancreatic surgery in Germany is 11 days. As already mentioned above, an increase in the LOS is only reimbursed in additional charges once the DGR‐specific upper limit of stay has been exceeded, but this is far from covering the additional costs.
The median prolongation of LOS of 19 days in case of SSI results in financial losses, which are not adequately reimbursed by the German DRG system. The €5676 additional costs per incisional SSI determined in our study show that also in HPB surgery, SSI represents a considerable economic burden for care providers, especially since the cost calculation we made is a cautious estimation. In our cohort, it resulted in a calculated total loss of ‐€781 369 in patients with SSI. Already Wolters et al showed additional costs of €5628 per patient with SSI in a German urological cohort. 14 Graf et al showed additional charges of €12 482 in cardiac surgery patients who developed deep sternal SSI. We assume that, especially in a hospital of the highest level of care, such as ours, the costs are significantly higher due to the substantially larger maintenance of material, equipment, and personnel. Within the DRGs, the treatments performed are very heterogeneous; however, interventions of varying degrees and risks are reimbursed by the same amount. Typically, this is compensated if a hospital performs a mixture of many “easy” and few “complex” procedures summarised under one DRG. If a hospital like ours and many other university hospitals and large tertiary referral centres are highly specialised and perform almost only “complex” procedures of one DRG, this leads to a severe underfinancing of these “expert” centres. The cost analysis within Germany cannot, of course, be transferred to other health care systems without restrictions. Badia et al were able to show in their review of comprehensive data on the costs of SSI in various indication areas that SSI in these systems also represent an economic burden for the service providers, as there is no total cost‐covering reimbursement. 15 It is necessary to demand that the costs of SSIs have to be more clearly reflected within the DRG system. These costs also have to be compensated by the insurance companies using additional charges if necessary. The analysis does not consider the economic follow‐up costs of SSIs due to prolonged follow‐up treatment, incapacity to work, and in some cases, the need for long‐term care and the socio‐economic importance for patients. In the worst‐case, an SSI can significantly worsen the oncological outcome of the patient.
Therefore, it must be the aim of all surgical disciplines to develop strategies to reduce the number of SSIs. Extrinsic factors appear to be easier to influence than patient‐centred ones. Nevertheless, the comparison of living liver donors with comparable patients gives indications of a more significant influence of intrinsic variables on the genesis of SSIs (SSI 0% / 32%, P < .001). As one of these strategies, we are currently investigating the benefit of epicutaneous negative pressure wound therapy in postoperative wound treatment for the prevention of SSI in HPB surgery intending to reduce the SSI rate by economically reasonable means. The findings of the present study have been used intensively for study planning and the subsequent economic evaluation of these and other preventive measures. In addition to further efforts to reduce wound infections, however, full cost coverage by the health insurance funds must also be demanded. Otherwise, the hospitals could be increasingly forced in the economic interest to discharge patients with wounds that heal secondarily and thus shift the costs to the outpatient sector. This practice would certainly be to the detriment of patients and would lead to a significant increase in the price of the overall treatment for the health insurance funds. The current system penalises hospitals that primarily treat particularly ill patients and allows cost‐covering work only for hospitals that carry out risk‐stratified patient selection.
ACKNOWLEDGEMENTS
Open access funding enabled and organized byProjekt DEAL.
CONFLICT OF INTEREST
The authors declare no conflicts of interest.
Brennfleck FW, Bachmeier T, Simet W, et al. Surgical Site Infections and their economic significance in hepatopancreatobiliary surgery: A retrospective incidence, cost, and reimbursement analysis in a German centre of the highest level of care. Int Wound J. 2021;18:17–23. 10.1111/iwj.13511
The study was performed at the Department of Surgery, University Medical Centre Regensburg, Franz‐Josef‐Strauß‐Allee 11, 93053 Regensburg, Germany.
[Correction added on 6 November 2020, after first online publication: Projekt Deal funding statement has been added.]
DATA AVAILABILITY STATEMENT
The data that support the findings of this study are available on request from the corresponding author. The data are not publicly available due to privacy or ethical restrictions.
REFERENCES
- 1. Andres A, Toso C, Moldovan B, et al. Complications of elective liver resections in a center with low mortality: a simple score to predict morbidity. Arch Surg. 2011;146(11):1246‐1252. [DOI] [PubMed] [Google Scholar]
- 2. Garner JS, Jarvis WR, Emori TG, Horan TC, Hughes JM. CDC definitions for nosocomial infections, 1988. Am J Infect Control. 1988;16(3):128‐140. [DOI] [PubMed] [Google Scholar]
- 3. Kärki T, Plachouras D, Cassini A, Suetens C. Burden of healthcare‐associated infections in European acute care hospitals. Wien Med Wochenschr. 2019;169(Suppl 1):3‐5. [DOI] [PubMed] [Google Scholar]
- 4. Magill SS, Edwards JR, Bamberg W, et al. Multistate point‐prevalence survey of health care–associated infections. N Engl J Med. 2014;370(13):1198‐1208. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 5. World Health Organization . Global Guidelines for the Prevention of Surgical Site Infection. Geneva, Switzerland: World Health Organization; 2016. [Google Scholar]
- 6. Zimmerman AM, Roye DG, Charpentier KP. A comparison of outcomes between open, laparoscopic and robotic pancreaticoduodenectomy. HPB (Oxford). 2018;20(4):364‐369. [DOI] [PubMed] [Google Scholar]
- 7. Nakahira S, Shimizu J, Miyamoto A, et al. Proposal for a sub‐classification of hepato‐biliary‐pancreatic operations for surgical site infection surveillance following assessment of results of prospective multicenter data. J Hepatobiliary Pancreat Sci. 2013;20(5):504‐511. [DOI] [PubMed] [Google Scholar]
- 8. Isik O, Kaya E, Sarkut P, Dundar HZ. Factors affecting surgical site infection rates in hepatobiliary surgery. Surg Infect (Larchmt). 2015;16(3):281‐286. [DOI] [PubMed] [Google Scholar]
- 9. Merkow RP, Ju MH, Chung JW, et al. Underlying reasons associated with hospital readmission following surgery in the United States. Jama. 2015;313(5):483‐495. [DOI] [PubMed] [Google Scholar]
- 10. Graf K, Ott E, Vonberg R‐P, et al. Surgical site infections–economic consequences for the health care system. Langenbecks Arch Surg. 2011;396(4):453‐459. [DOI] [PubMed] [Google Scholar]
- 11. Ohno M, Shimada Y, Satoh M, Kojima Y, Sakamoto K, Hori S. Evaluation of economic burden of colonic surgical site infection at a Japanese hospital. J Hosp Infect. 2018;99(1):31‐35. [DOI] [PubMed] [Google Scholar]
- 12. Roy S, Patkar A, Daskiran M, Levine R, Hinoul P, Nigam S. Clinical and economic burden of surgical site infection in hysterectomy. Surg Infect (Larchmt). 2014;15(3):266‐273. [DOI] [PubMed] [Google Scholar]
- 13. Fadayomi AB, Kasumova GG, Tabatabaie O, et al. Unique predictors and economic burden of superficial and deep/organ space surgical site infections following pancreatectomy. HPB (Oxford). 2018;20(7):658‐668. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 14. Wolters M, Oelke M, Lutze B, et al. Deep surgical site infections after open radical cystectomy and urinary diversion significantly increase hospitalisation time and Total treatment costs. Urol Int. 2017;98(3):268‐273. [DOI] [PubMed] [Google Scholar]
- 15. Badia JM, Casey AL, Petrosillo N, Hudson PM, Mitchell SA, Crosby C. Impact of surgical site infection on healthcare costs and patient outcomes: a systematic review in six European countries. J Hosp Infect. 2017;96(1):1‐15. [DOI] [PubMed] [Google Scholar]
Associated Data
This section collects any data citations, data availability statements, or supplementary materials included in this article.
Data Availability Statement
The data that support the findings of this study are available on request from the corresponding author. The data are not publicly available due to privacy or ethical restrictions.