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Arch Orthop Trauma Surg

DOI 10.1007/s00402-016-2600-z

TRAUMA SURGERY

Bacterial reduction and shift with NPWT after surgical


debridements: a retrospective cohort study
Thorsten Jentzsch1 Georg Osterhoff1 Pawel Zwolak1 Burkhardt Seifert2

Valentin Neuhaus1 Hans-Peter Simmen1 Gerrolt N. Jukema1

Received: 3 May 2016


Springer-Verlag Berlin Heidelberg 2016

Abstract bacterial load and led to a shift away from Gram-positive


Background Surgical debridement, negative-pressure bacteria, facultative anaerobic bacteria, and S. aureus, as
wound therapy (NPWT) and antibiotics are used for the well as questionably toward CoNS and Pseudomonas spp.
treatment of open wounds. However, it remains unclear in this patient cohort. High rates of wound closure were
whether this treatment regimen is successful in the reduc- achieved in a relatively short time with low revision rates.
tion and shift of the bacterial load. Whether each modality played a role for these findings
Methods After debridement in the operating room, NPWT, remains unknown.
and antibiotic treatment, primary and secondary consecu-
tive microbiological samples of 115 patients with 120 open Keywords Bacterial reduction  Bacterial shift  Negative-
wounds with bacterial or yeast growth in C1 swab or tissue pressure wound therapy (NPWT)  Vacuum-assisted
microbiological sample(s) were compared for bacterial closure (VAC)  Gram-staining  Oxygen use
growth, Gram staining and oxygen use at a level one
trauma center in 2011.
Results Secondary samples had significantly less bacterial Introduction
growth (32 vs. 89%, p \ .001, OR 17), Gram-positive
bacteria (56 vs. 78%, p = .013), facultative anaerobic Surgical debridement and negative-pressure wound therapy
bacteria (64 vs. 85%, p = .011) and Staphylococcus aureus (NPWT) are common treatment modalities for the acute
(10 vs. 46%, p = .002). They also tended to include rela- and chronic open wound management [13]. The latter
tively more Coagulase-negative Staphylococci (CoNS) (44 effectively drains wound exudate and hematoma through a
vs. 18%) and Pseudomonas species (spp.) (31 vs. 7%). sterile wound dressing, which consists of black poly-
Most (98%) wounds were successfully closed within urethane ether (PUE) or white polyvinyl alcohol (PVA)
11 days, while wound revision was needed in 4%. foam, a semi-occlusive foil and negative pressure, usually
Conclusions The treatment regimen of combined use of between 50 and 125 mm Hg [4, 5]. It also provides the
repetitive debridement, irrigation and NPWT in an oper- benefit of continuous wound contraction, tissue granula-
ating room with antibiotics significantly reduced the tion, improved perifocal blood supply, and cost-effective-
ness because dressing changes are not needed daily [69].
Therefore, together with surgical debridement and antibi-
& Thorsten Jentzsch otics, it is an effective adjunct treatment modality against
thorsten.jentzsch@gmail.com; thorsten.jentzsch@usz.ch contaminated and/or infected wounds [1012].
1
The influence of NPWT on the reduction of bacterial
Division of Trauma Surgery, Department of Surgery,
loads within an open wound cavity is an important con-
University Hospital Zurich, University of Zurich,
Ramistrasse 100, 8091 Zurich, Switzerland tributor to effective treatment. It has been subject to debate
2 since its suggestion in 1997, and, ultimately, requires more
Department of Biostatistics, Epidemiology, Biostatistics and
Prevention Institute, University of Zurich, Zurich, studies to clarify the remaining uncertainties [3, 1320].
Switzerland Some studies have reported no reduction of the bacterial

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Arch Orthop Trauma Surg

load [13, 14, 18], while others found a bacterial shift following surgeries before final wound closure. They were
[14, 15], or a reduction of the bacterial load [16, 17]. obtained after surgical debridement and before NPWT
However, aside from the limited number of these studies application. Samples were usually incubated for 10 days
[3, 1320], they not only show discrepancies regarding the before final results were documented. Furthermore, the
location of NPWT application, antibiotic treatment, but management of infected and traumatic wounds followed a
were also based on in vitro experiments [13], in vivo ani- different standardized algorithm at our hospital. Microbi-
mal models [15], topical application [17], or included a ological samples were always acquired immediately in
rather small sample size [14, 16]. infected wounds, whereas traumatic wounds were first
Early administration of antibiotics for open wounds is treated with local debridement, irrigation and NPWT for
one of the most important factors in open wound treatment 12 days before the wound status in the second look was
[21]. A recent meta-analysis of randomized controlled tri- used for the decision on microbiological sampling. This
als about patients with open fractures has reported a 59% approach proved beneficial because it avoided over-inter-
lower risk of infection with antibiotics compared to pla- preting contaminated wounds as infected ones. The stan-
cebo [22]. It is common knowledge that antibiotics, usually dardized treatment protocol involved serial surgical
a first-generation cephalosporin, should be administered as debridements in the sterile operating room, usually within
soon as possible and may be continued for 24 h [23]. 15 days. Care was taken to rigorously debride all tissues
Surgical debridement is another very important factor in that could have possibly been infected, but without com-
open wound treatment. It is always the goal to fully debride promising neurovascular structures. After local debride-
and irrigate all contaminated and necrotic tissue with sal- ment and irrigation, provisional wound closure was
ine. The exact time frame remains unknown and the his- performed using NPWT with V.A.C GranuFoamTM
toric 6-h rule does apply anymore, but debridement should (PUE) or V.A.C. WhiteFoam (PVA) dressing [Kinetic
be done as soon as tolerable for a patients condition Concepts Inc. (KCI), San Antonio, TX, USA] and their
[2428]. Bone viability can be evaluated by capacity to corresponding semi-occlusive drapes and T.R.A.C PadsTM
bleed and muscle viability by the 4 Cs, color, contractility, about every 3 days until wound closure. The reasons for
consistency, and capacity to bleed [23, 29, 30]. different foam use were mostly subjective personal pref-
The goal of the present study was to investigate the erence of a surgeon. During surgeries, the irrigation regi-
changes of the bacterial load and a bacterial community men consisted of isotonic saline volume for all wounds
shift in a large clinical cohort of mainly trauma patients, with added pulse lavage in severely contaminated open
who received a treatment regimen of surgical debridement, traumatic wounds. Postoperatively, negative pressure,
NPWT in a sterile operating room, and antibiotics. usually around 125 mm Hg, was applied. Secondary
wound closure was carried out after sufficient granulation
tissue was visible without clinical signs of necrosis or
Materials and methods infection after at least two rounds of surgical debridements.
Overall, antibiotic use was heterogeneous. An intra-
The present study investigated 261 consecutive patients venous broad-spectrum antibiotic, most commonly amox-
with 280 open wounds treated with surgical debridement icillin/clavulanic acid, was usually given to high-risk
and NPWT at a single-level one trauma center (Department patients, e.g., open fractures, and suspected or confirmed
of Trauma Surgery, University Hospital of Zurich, infections, usually for at least 3 days. Wound infection was
Switzerland) in 2011 and is an ancillary to the retrospective defined as two or more positive microbiological samples
cohort study by Osterhoff et al. [4]. Out of the 261 patients from the wound, abscess formation with one or more
reported by Osterhoff et al. [4], 115 patients with 120 positive microbiological samples or wound drainage. In
wounds were eligible for our study due to a positive low-risk patients (e.g., fasciotomy due to compartment
microbiological sample. Therefore, none of the presented syndrome), a single shot of intravenous cefazolin was
results has been previously reported. Our study complied administered 30 min before surgery or oral antibiotics,
with the regulations of the cantonal ethical review board mostly amoxicillin/clavulanic acid, were given. Afterward,
(Zurich, Switzerland). antibiotics were changed according to antibacterial sensi-
The inclusion and exclusion criteria are given in tivity tests, usually in an interdisciplinary approach with an
Table 1. The flow chart in Fig. 1 depicts the number of infectiologist, particularly in difficult cases. The time per-
patients in this study as well as the measurements and iod for the antibiotic treatment varied in this group of
outcome variables. For further patient characteristics, such patients. Generally, trauma patients were mostly treated
as comorbidities, one may refer to the study by Osterhoff with amoxicillin/clavulanic acid for 57 days, while
et al. [4]. Microbiological samples were sterilely acquired patients with primary infections received this treatment
in all patients at the first or second surgery and one of the regimen for 1214 days or a combination of ciprofloxacin,

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Table 1 Inclusion and exclusion criteria


Inclusion criteria Exclusion criteria

NPWT between January and December 2011 Negative microbiological sample


Bacterial or yeast growth in C1 swab or tissue microbiological sample(s) Follow-up \1 year
NPWT negative-pressure wound therapy

Fig. 1 Flow chart of patient and study characteristics

rifampicin, and clindamycin for 24 weeks. This variation Data are presented as frequencies and percentages of
is attributable to the individual decision-making process, wounds. Primary and secondary microbiological samples
which combined the results of the secondary microbio- were compared using univariate logistic regression analysis
logical samples, laboratory analysis, and clinical with bacterial growth, Gram staining and oxygen use as
judgement. independent variables. Clustering within patients was
The microbiological sample was processed with a addressed with clustered robust standard errors. Risk
standardized semiquantitative technique with laminar flow stratification and comorbidities were compared between
hoods as described previously [31]. Samples were streaked patients with and without bacterial reduction, Gram stain-
on one-third of a 5% sheep blood Columbia agar plate ing, and oxygen use using Fishers exact test. p values less
(BioMerieux, Geneva, Switzerland). Using a disposable than .05 were considered statistically significant. Stata 13.1
sterile loop, two successive dilutions were obtained by (StataCorp., College Station, TX, USA) was used for sta-
further streaking the initial inoculum on the agar plates tistical analyses.
over the remaining two-thirds, using a new loop for each
streaking maneuver. The samples were then placed into
LuriaBertani broth (Sigma St. Louis, MO, USA) for Results
enrichment for 72 h. The plates were then incubated at
37 C for 48 h, after which they were assessed for colony The present study included 115 patients, 31 females and 84
growth. After 72 h, the liquid enrichment medium was males, with a median age of 47 (IQR 3564) (range 1688)
processed on agar plates identical to the agar plate method years and 120 open wounds. Main causes included a pri-
described above. Gram staining was performed for mor- mary infection (e.g., abscess, bursitis, postoperative surgi-
phologic analysis and classification. The bacterias oxygen cal site infection, spetic arthritis) in 52% (n = 62) and
use was evaluated with the catalase reactivity test. Several trauma in 46% (n = 55), whereof 18% (n = 21) were open
subcultures were specified by the RapID Staph Plus System fractures. The wounds were localized at the lower
(BioMerieux, Geneva, Switzerland). extremity in 51% (n = 61), the trunk, spine and pelvis in

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28% (n = 34), the upper extremity in 19% (n = 23), and Table 3 Gram-staining bacteria in primary (n = 107) and secondary
the abdomen in 2% (n = 2) with varying size. The mean (n = 39) microbiological samples [n (%)] with bacterial growth
time of NPWT until definite wound closure was 11 days Gram staining Primary Secondary p value
(10 days). The majority of wounds (98%) were suc-
- 15 (14%) 10 (26%)
cessfully closed. Two (2%) wounds were not closed
because one patient died due to an urosepsis in a metas- ? 83 (78%) 22 (56%) .013*

tasized breast cancer and one patient had an amputation of ; 9 (8%) 7 (18%)
a lower leg in an open (Gustilo IIIc) ankle fracture dislo- * Logistic regression analysis with clustered robust standard errors

cation. The hospital readmission rate was 18% due to No significant difference
various reasons. Furthermore, there were five cases (4%)
with delayed ([30 days) wound healing or a reinfection
requiring surgical revision. Staphylococci (CoNS), and Pseudomonas species (spp.)
Bacterial growth was significantly reduced in the sec- (mainly Pseudomonas aeruginosa), while newly acquired
ondary samples (32%) compared to the primary samples bacteria in secondary samples mainly revealed CoNS
(89%) (p \ .001) and the odds for bacterial growth were (Table 6). S. aureus was significantly reduced in the sec-
reduced by factor 17 [95% confidence interval (CI) 646] ondary samples (10%) compared to the primary samples
(Table 2). Of the 11% without bacterial growth in the (44%) and the odds for bacterial growth were reduced by
primary wounds, 82% were acute trauma patients, while factor 5 (95% CI 212) (p = .002). In the primary samples,
18% had an atraumatic infection. Regarding the positive two methicillin-resistant S. aureus (MRSA) were found.
secondary samples (n = 39), pre-existing bacteria were Although not significant, there was a tendency toward an
cultured again in 69% (n = 27) and newly acquired bac- increased percentage of Coagulase-negative Staphylococci
teria were detected in 31% (n = 12). Yeast growth was (CoNS) and Pseudomonas species (spp.) in the positive
observed in two secondary samples, whereof one patient, secondary samples (n = 39) than in the primary samples
who had bacterial growth in the primary sample, with (n = 107) (44 and 18 vs. 31 and 7%).
Candida glabrata was treated with anti-mycotics, while the Fifty-seven patients (48%) received an intravenous
other patient, who did not have bacterial growth in either antibiotic from the beginning of treatment and were,
sample, was interpreted as a contamination. therefore, perceived as high-risk patients. An influence of
Gram-positive bacteria was significantly reduced in the the perceived stratification into low- and high-risk patients
secondary samples (56%) compared to the primary samples on the results in the secondary wound cultures was not
(78%) and the odds for bacterial growth were reduced by found since no significant differences in bacterial reduction
factor 3 (95% CI 16) (p \ .013) (Table 3). Gram-negative were observed between perceived low- and high-risk
and -positive bacteria did not show significant reductions. patients.
Furthermore, if wounds with bacteria were not sterile, no With respect to the reported comorbidities by Osterhoff
change in Gram staining was slightly more common than a et al. [4], patients with bacterial reduction had significantly
change in Gram staining (Table 4). less peripheral vascular disease and immunosuppressive
Facultative anaerobic bacteria were much more common medication (p = 0.023 and p = 0.030, respectively). There
than bacteria with a different use of oxygen in primary and were no significant differences for smoking, alcohol and
secondary samples (Table 5). Their growth was signifi- drug abuse, diabetes, and immunodeficiency diseases.
cantly reduced from the primary (85%) to the secondary Furthermore, PUE foam was used in 58 patients, PVA
samples (64%) and the odds for bacterial growth were foam in three patients, and both foams in five patients.
reduced by factor 3 (95% CI 18) (p = .011). Since it was not documented which foam was used in 54
The primary samples and pre-existing secondary bac- patients, no analysis of different foams was performed.
teria mainly showed, among other more rare bacteria,
Staphylococcus (S.) aureus, Coagulase-negative
Discussion

Table 2 Bacterial growth in primary and secondary microbiological The present follow-up study on a cohort study [4] adds
samples [n (%)] of wounds (n = 120) information to the controversial literature [3, 1320] about
Primary Secondary p value bacterial colonization of open wounds treated with our
treatment regimen of surgical debridement and irrigation in
No bacterial growth 13 (11%) 81 (68%) \.001* a sterile operating room, NPWT and antibiotics by inves-
Bacterial growth 107 (89%) 39 (32%) tigating a large clinical cohort of mainly trauma patients
* Logistic regression analysis with clustered robust standard errors admitted to our level one trauma center. The applied

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Table 4 Bacterial shift


Primary samples ? Secondary samples Samples
according to Gram stain from
primary (n = 107) to secondary Bacterial growth Sterile 80 (75%)
microbiological samples [n (%)]
with bacterial growth Bacterial growth No change in Gram stain 17 (16%)
Bacterial growth Change in Gram stain 10 (9%)
Gram-negative Gram-positive 6 (60%)
Gram-positive Gram-negative 2 (20%)
Gram-negative and -positive Gram-negative or -positive 2 (20%)

Table 5 Oxygen use in primary


Oxygen use Primary samples Secondary samples p value
(n = 106*) and secondary
(n = 39) microbiological Anaerobic 7 (7%) 2 (5%)
samples [n (%)]
Facultative anaerobic 90 (85%) 25 (64%) .011*
Aerobic 6 (5%) 5 (13%)
Mix 3 (3%) 7 (18%)
* Logistic regression analysis with clustered robust standard errors

The oxygen use remained unknown in one primary sample

Table 6 Most commonly found specific bacteria in primary than control wounds with gauze dressings. Another study
(n = 107) and secondary (n = 39) bacteriological samples [n (%)] [16] also showed a reduction in the bacterial load in all
Bacteria Primary Secondary p value 21 patients, who were treated with NPWT. In contrast,
another study [14] did not find a quantitative reduction
Staphylococcus aureus 49 (46%) 6 (10%) .002* of the bacterial load despite favorable wound healing in

Pseudomonas species 7 (7%) 7 (18%) a well-designed prospective randomized trial of 54

Coagulase-negative Staphylococci 33 (31%) 17 (44%) patients, which is in line with other studies [18, 19]. A
* Logistic regression analysis with clustered robust standard errors theoretically possible explanation for these discrepancies

No significant difference may be found in the location of NPWT application,


which, in the present study, was exclusively performed
in a sterile operating room, including surgical debride-
treatment regimen effectively reduced the bacterial load ments with irrigation at every NPWT procedure, and
while keeping newly acquired bacteria to a minimum and concomitant antibiotic treatment. This raises the question
was associated with a bacterial community shift away from whether it may be more beneficial to perform NPWT
Gram-positive bacteria, facultative anaerobic bacteria, and changes in an operating room instead of at a patients
S. aureus. It proved to be effective after a relatively short bedside. This has been appealing because it safes time
time (mean of 11 days) with a high rate of wound closures and does not occupy the operating room. However, this
(98%) and a low revision rate (4%). cannot be proven by this study due to the retrospective
The use of NPWT for open wound management has design using a multimodal therapeutic approach.
been controversially discussed, but several studies have The presented treatment regimen was most effective
shown a clear benefit for patients [11, 12]. A multicenter, against Gram-positive bacteria because they reduced sig-
randomized controlled trial after diabetic foot amputation nificantly more often than the remaining bacteria. Addi-
showed that NPWT could lead to better and faster wound tionally, the relative proportion of Gram-negative bacteria
healing [11]. In a prospective casecontrol study [12] about in secondary samples was higher than in primary samples,
the management of diabetic foot ulcers, it was reported that which constitutes a common clinical problem. This shift
NPWT was more effective, safe, and satisfactory for may have been attributed to an increased resistance of
patients than conventional dressings. plasmid-containing Gram-negative bacteria with efflux
Previous studies [3, 32], who introduced the NPWT in pumps against antibiotics [33]. In a recent study [34],
a pig model in 1997, support a reduction of the bacterial NPWT with instillation was only associated with a bacte-
load with NPWT. Similarly, in a prospective randomized rial reduction at a short dwell time and when excluding
study [20] of a limited number patients (n = 23) with Gram-negative bacteria. This is an upcoming topic, where
open fractures, it was reported that only wounds treated bacterial reduction may much more depend on the type of
with NPWT were much less frequently colonized (8%) solution used.

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The facultative anaerobic bacteria, which, among others, negative intraoperative microbiological samples [35].
included S. aureus and CoNS were the most commonly However, other recent studies have pointed into a different
found subgroup and showed a significant reduction of their direction in revision arthroplasty, where prophylaxis of
bacterial load from primary to secondary samples. Fur- infection is very important. In these studies, diagnostic
thermore, anaerobic bacteria, such as Propionibacterium sensitivity of microbiological samples did not differ in case
spp. and Bacteroides spp., exclusively became sterile or of administration before or after sampling [36, 37]. In
changed into a different oxygen-using subgroup. Therefore, heavily contaminated wounds, it seems adequate to
the presented treatment regimen seems to provide enough administer antibiotics early, but one needs to remember
oxygen to be effective against anaerobic bacteria. Simi- that false-negative microbiological samples may arise. In
larly, another study [14] did not find a difference in the cases with ambiguous clinical courses, it may be helpful to
number of anaerobes in wounds treated with or without add broad-range polymerase chain reaction to the bacteri-
NPWT. ological analysis [38]. Third, our sample size included
In a thorough review article [10], diverse effects on different wound types with different aetiologies, varying
certain bacteria have been reported, ultimately suggesting sizes and various locations. Although chronic infections
that more studies are needed. In the present study, a ten- may have been underrepresented and several surgeons were
dency toward a relative bacterial shift from S. aureus involved, most patients were treated due to trauma or acute
toward CoNS and Pseudomonas spp. was observed. Simi- infections and the standard operating procedures were
larly, another study [3] reported a decrease in S. aureus. applicable to all surgeons because the study was carried out
Contrarily, a different study [14] showed an increase in S. at a level one trauma center. Fourth, the present study used
aureus and, together with another report [15], observed a PUE and PVA foams, which could not be presented in a
decrease in Pseudomonas spp. in their in vivo goat study. subgroup analysis due to frequent missing data, whereas a
A recent prospective study reported that bacterial loads previous study [14] exclusively used PUE foams. Fifth,
remained high in foams despite routine changes [18]. Of 68 although it is our impression that C3 tissue samples should
foams, 97% had C1 bacterial type and of 17 patients, 27% be the gold standard for regular wounds and additional
had an additional bacterial type. Although this is worri- three samples in case of suspecting low-grade infection, the
some, it does not necessarily indicate that these bacteria type and number of acquired samples were very hetero-
were in the wounds, i.e., surrounding tissue, as well. Dif- geneous, limiting generalizability. It should also be kept in
ferences to the results of our study may also be explained mind that Gram staining in tissue samples often has low
by the fact that surgical debridement, irrigation, and NPWT sensitivity and certain bacterias (e.g., Propionibacterium)
changes were performed in a rather sterile operating room, need long incubation periods (1014 days). One may also
potentially higher negative pressure in certain cases, more consider that one positive histological tissue is proof for
frequent foam changes every 12 days. infection, which was only done in some patients in this
Due to the retrospective design and multimodal treat- study. Despite these numerous limitations, the current
ment regimen with concomitant use of surgical debride- study adds interesting findings to the literature that can be
ment and NPWT application in an operating room as well taken into account during NPWT application and for the
as antibiotic treatment, this study has several limitations. design of randomized controlled trials, which are already
First, it is not possible to state which particular factor of the underway [39]. Further studies could compare NPWT
treatment regimen was associated with an outcome vari- changes under sterile conditions in an operating room to
able. However, the goal of the present study is to provide bedside changes of NPWT.
information about the bacterial reduction and shift in a
large patient cohort that was treated with a commonly used
treatment regimen. Although amoxicillin/clavulanic acid Conclusion
was the most commonly used antibiotic, heterogeneous
differences in antibiotic treatment represent an important The treatment regimen of combined use of repetitive sur-
possible confounder. In the clinical setting, this aspect gical debridement, irrigation and NPWT in a sterile oper-
constitutes an issue that is very hard to overcome due to the ating room in combination with antibiotic treatment
different preferences of physicians and the need to adapt significantly reduces the bacterial load and leads to a
the antibiotic therapy to the specific bacteria of each bacterial shift away from Gram-positive bacteria, faculta-
wound, but should be considered when planning future tive anaerobic bacteria, and S. aureus, as well as a ques-
trials or treatment algorithms in hospitals. Second, preop- tionable shift toward CoNS and Pseudomonas spp. High
erative antibiotic administration likely affects bacterial rates of wound closure were achieved in a relatively short
detection in microbiological samples. It is usually assumed time with low revision rates. Whether each modality
that preoperative antibiotic administration may entail false- played a role for these findings remains unknown.

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Arch Orthop Trauma Surg

Acknowledgements A similar version of this abstract (Bacterial without negative pressure in an in vitro wound model. Int Wound
Reduction and Community Shift with Negative-Pressure Wound J 7:283289
Therapy: The Relevance of Surgical Debridements in the Operating 14. Moues CM, Vos MC, van den Bemd GJ, Stijnen T, Hovius SE
Room) was presented as an oral presentation at the 16th European (2004) Bacterial load in relation to vacuum-assisted closure
Congress of Trauma and Emergency Surgery (ECTES) of the Euro- wound therapy: a prospective randomized trial. Wound Repair
pean Society for Trauma and Emergency Surgery (ESTES) in May Regen 12:1117
2015 in Amsterdam, The Netherlands. We would like to thank Dr. 15. Lalliss SJ, Stinner DJ, Waterman SM et al (2010) Negative
med. Florian P. Maurer for his advice as well as Dr. med. Matthias A. pressure wound therapy reduces pseudomonas wound contami-
Konig, Ms. Verena Wilzeck, and Ms. Carmen Kruger for their help nation more than Staphylococcus aureus. J Orthop Trauma
with data acquisition. 24:598602
16. Pinocy J, Albes JM, Wicke C, Ruck P, Ziemer G (2003) Treat-
Compliance with ethical standards ment of periprosthetic soft tissue infection of the groin following
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