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Flap Reconstruction for Deep Sternal

Wound Infections: Factors Influencing


Morbidity and Mortality
William Piwnica-Worms, BA, Saïd C. Azoury, MD, Geoffrey Kozak, MD,
Shelby Nathan, MS, John T. Stranix, MD, David Colen, MD, Sammy Othman, BA,
Prashanth Vallabhajosyula, MD, Joseph Serletti, MD, and Stephen Kovach, MD
GENERAL THORACIC

Division of Plastic Surgery, Department of Surgery, University of Pennsylvania, Philadelphia, Pennsylvania; and Division of
Cardiothoracic Surgery, Department of Surgery, University of Pennsylvania, Philadelphia, Pennsylvania

Background. Deep sternal wound infections (DSWI) mortality was 15.1%. End-stage renal disease (P [ .002),
often require flap reconstruction to obliterate dead space congestive heart failure (P [ .049), low albumin (P [
and provide healthy soft tissue coverage. A better un- .004), cardiopulmonary bypass time (P [ .0001), need for
derstanding of risk factors for complications after DSWI open chest (P [ .020), and high American Society of
flap reconstruction may improve operative management. Anesthesiologists Physical Status Classification (P [
Methods. A retrospective study (2007-2018) was con- .003) were associated with higher mortality. By multi-
ducted of all patients with DSWI after cardiothoracic variate analysis, multidrug resistance was predictive of
procedure referred to a single reconstructive surgeon for any postoperative complication (odds ratio [OR], 5.6; 95%
flap reconstruction. Patient and operative factors were confidence interval [CI], 1.3-23.2; P [ .018), VRAM was
reviewed, including procedure types and outcomes. Pre- predictive of SSI (OR, 9.6; 95% CI, 1.4-66.4; P [ .022), and
dictors of morbidity and mortality rates were analyzed. end-stage renal disease (OR, 8.57; 95% CI, 1.06-69.1; P [
Results. A total of 119 patients requiring flap recon- .044) was predictive of higher mortality.
struction for DSWI met inclusion criteria. Unilateral Conclusions. Pectoralis muscle flaps are the workhorse
(49.6%) or bilateral (40.3%) pectoralis muscle flaps were for complex sternal wound coverage, but complications
performed most frequently, followed by vertical rectus after flap reconstruction for DSWIs remain high. In
abdominis myocutaneous (VRAM) (4.2%), omental particular, end-stage renal disease, VRAM reconstruction,
(4.2%), and omental/pectoralis flap combination (1.7%). and multidrug-resistant infection may predict a compli-
Superficial surgical site infection (SSI) was the predomi- cated postoperative course in these patients.
nant postoperative complication (17.6%). Debridement/
revisional procedures were required in 19 patients (16%), (Ann Thorac Surg 2020;109:1584-90)
and flap failure occurred in 5 (4.2%). Overall 30-day Ó 2020 by The Society of Thoracic Surgeons

D eep sternal wound infection (DSWI) after a median


sternotomy is a serious complication, estimated to
occur in 1.5% to 2.5% of patients after open cardiac pro-
collaborative approach to d ebridement, followed by
muscle flap closure. The paradigm shift to early flap
coverage occurred after the early work of Jurkiewicz and
cedure.1-4 Whereas superficial wound infections are colleagues10 in 1980, which showed a significant reduc-
contained to the suprasternal skin, subcutaneous tissue, tion in mortality from as high as 40% to 8$ to 21% with the
and fascia, DSWI involves deeper structures, including use of a muscle flap.8,11-15
the sternum or mediastinum. DSWI portends significant Use of unilateral or bilateral pectoralis major flaps re-
morbidity and mortality, with mortality rates ranging mains the most common reconstruction performed due to
from 1.0% to 36%.5-9 Historically treated with the muscle’s proximity to the wound and versatility as a
debridement and open packing or with drains and anti- turnover or advancement flap.13,16 Vertical rectus
biotic lavage, this devastating complication is managed abdominis myocutaneous (VRAM), omental, or a combi-
more recently with consultation of plastic surgery for a nation of these remain viable alternatives, but surgical
decision making ultimately depends on past surgical
history, potential donor sites, and the dimension and
Accepted for publication Dec 4, 2019. tissue character of the defect remaining after
Presented at the Thirty-sixth Annual Meeting of the European Association debridement. Despite adoption of early d ebridement and
of Plastic Surgeons, Helsinki, Finland, May 23-24, 2019. flap reconstruction for management of DSWI, no stan-
Address correspondence to Dr Azoury, Division of Plastic Surgery, Uni-
dardized treatment exists, largely due to the variability in
versity of Pennsylvania Health System, 3400 Civic Center Blvd, Philadel- time to presentation, patient risk factors, and extent of the
phia, PA 19104; email: said.azoury@pennmedicine.upenn.edu. infection.

Ó 2020 by The Society of Thoracic Surgeons 0003-4975/$36.00


Published by Elsevier Inc. https://doi.org/10.1016/j.athoracsur.2019.12.014
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2020;109:1584-90 RECONSTRUCTION OF COMPLEX STERNAL WOUNDS

pectoralis major advancement flap, VRAM flap, omental


Abbreviations and Acronyms flap, or a combination of omental and pectoralis flap. The
ASA = American Society of size of DSWI defect (measured as the cross-sectional area
Anesthesiologists of the wound after d ebridement), operation length (mi-
CBT = cardiopulmonary bypass time nutes), and the number and type of drains placed were
CAD = coronary artery disease analyzed.
CHF = congestive heart failure Once consulted, the senior author reconstructive sur-
CI = confidence interval geon (S.K.), in collaboration with cardiothoracic surgery,
COPD = chronic obstructive pulmonary proceeds with operative therapy as soon as possible.
disease
Sternal hardware/wires are removed at the time of
DSWI = deep sternal wound infection
debridement before flap advancement. The reconstruc-
ESRD = end-stage renal disease
MDR = multidrug resistant tive and cardiothoracic surgeons choose not to reestablish

GENERAL THORACIC
MI = myocardial infarction sternal fixation with wires/hardware given the risk of
No. = number colonization to the prosthetic material. They prefer to
NPWT = negative pressure wound therapy primarily use pectoralis muscle flaps for defects where
OR = odds ratio the prosthetic aortic reconstruction does not need
SSI = surgical site infection coverage in the deeper mediastinum. Omental flaps are
VRAM = vertical rectus abdominis preferred if vascularized tissue needs to be used to shield
myocutaneous and cover prosthetic aortic grafts or if the sternum needs
to be reclosed (Figure 1). Successful reconstruction was
defined as complete resolution of the tissue defect with no
Common serious complications contributing to high further intervention necessary.
morbidity after DSWI flap reconstruction include super- Reoperations were divided into flap salvage or com-
ficial surgical site infection (SSI), dehiscence, hematoma, plete flap failure. Salvage was defined as d ebridement
and seroma.13 However, specific risk factors for post- and irrigation with preservation of the original flap, and
operative complications have not been clearly defined in complete failure was defined as partial d ebridement of
this population. A better understanding of these variables the original flap with advancement of an additional flap to
as they relate to the cardiac procedure, flap choice, spe- achieve adequate coverage for wound closure.
cific complications, and outcomes will aid plastic and Pearson c2 Fisher exact tests were used to analyze
cardiothoracic surgeons in management decisions sur- categorical variables, and the t test and Wilcoxon rank
rounding this frequently devastating complication. sum were used for continuous variables to assess for
significance between risk factors/flap choices and
morbidity and mortality. Multivariate analysis was per-
formed with a step-down logistic regression model to
Patients and Methods
assess the strongest independent predictive factors asso-
After approval from the University of Pennsylvania Insti- ciated with perioperative mortality. Results with a P of
tutional Review Board, a retrospective review (September less than .05 were considered to be statistically significant.
2007-August 2018) was performed of all patients referred Analyses were performed using Stata IC 11.0 software
to a single plastic surgeon for reconstruction of DSWI after (StataCorp, College Station, TX).
cardiothoracic procedures. Only patients aged older than
18 years at the time of procedure were included in the
Results
study. The study excluded patients with DSWI after a
noncardiac procedure, those with superficial chest wall During the study period (September 2007-August 2018),
infections managed with local tissue rearrangement/com- 16,340 median sternotomies with cardiopulmonary
plex closure (ie, no muscle flap), and patients with inade- bypass were performed by the cardiac services at the 2
quate follow-up, defined as lack of available major teaching hospitals of Penn Medicine. Overall, 119
documentation after discharge. patients met inclusion criteria for the study. Patient de-
Medical records were reviewed for patient de- mographics and presternotomy comorbidities are sum-
mographics and relevant risk factors. Variables and out- marized in Table 1.
comes related to the index cardiothoracic operation and The type and distribution of antecedent cardiac pro-
subsequent reconstructive procedure were analyzed. Pa- cedures are summarized in Table 2. Average cardiopul-
tient presentation was defined as delayed if the plastic monary bypass time (CBT) was 174  112 minutes.
surgery consult occurred more than 30 days after the Emergent cardiothoracic procedures was performed in 41
original cardiothoracic procedure.17 Flap reconstruction patients (34.5%). Redo sternotomy was performed in 24
was defined as delayed if the surgeon performed recon- patients (20.2%), and only 3 (2.5%) required a nonmidline
struction more than 20 days after the plastic surgery sternotomy. Unilateral internal mammary artery grafting
consult.17 Use of negative pressure wound therapy as a was performed in 60 patients (50.4%), and bilateral internal
bridge to reconstruction was reviewed. mammary artery grafting was performed in 3 (2.5%).
The type of reconstruction performed included unilat- Massive transfusions were required during the operation
eral pectoralis major advancement flap, bilateral in 7 patients (5.9%), and 18 (15.1%) required tracheostomy
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GENERAL THORACIC

Figure 1. Reconstructive algorithm for deep sternal wound infections. (VRAM, vertical rectus abdominus myocutaneous.)

placement postoperatively. Negative pressure wound to the DSWI. Both patients were bilateral lung transplant
therapy was used to bridge 15 patients (12.6%) to recon- recipients on immunosuppression with progressive
struction before the plastic surgery consultation. sepsis ultimately leading to multiorgan failure. Cause of
The average area of chest wall defects was 114  84 cm2. death in the remaining patients included multiorgan
Most patients received unilateral or bilateral pectoralis failure in 4, cerebrovascular accident in 3, congestive
major flap coverage, with the remaining flap choices heart failure (CHF) in 3, renal failure in 2, and necrotic
performed less frequently (Table 2). Evidence of pros- bowel, unrelated colonic perforation, aortic aneurysm
thetic aortic graft or valve infection was present in 10 rupture, and pulmonary infection in 1 patient each. The
patients (8.4%) at the time of reconstruction. On average, most common complications are summarized in Table 3.
debridement and flap reconstruction took 147  54 mi- By univariable analysis, younger age (52 vs 65 years,
nutes. Jackson-Pratt drains were most commonly used P ¼ .002), lower body mass index (24.7 vs 31.1 kg/m2, P ¼
(83%), and Blake (12%) or a combination of both (5%) .003), and no history of hypertension were associated with
were less commonly used. postoperative hematoma. Low preoperative albumin (2.2
Staphylococcus aureus (50%) was the most common vs 2.9 g/dL, P ¼ .013) was associated with hematoma. A
operative cultured microbe, followed by polymicrobial history of diabetes was associated with lower rate of
(12%), Staphylococcus epidermidis (10%), Pseudomonas aeru- postoperative seroma (P ¼ .01), and evidence of prosthetic
ginosa (8%), Serratia marcescens (8%), Proteus mirabilis (6%), aortic graft or valve infection was associated with higher
vancomycin-resistant enterococcus (3%), and Mycobacte- rate of seroma (P ¼ .024), end-stage renal disease (ESRD)
rium abscessus (3%). Of patients with multidrug-resistant (P ¼ .003), and need for open chest (P < .0001) were
(MDR) organisms, at least one of the studied complica- significantly associated with flap failure, and chronic
tions developed in 48%, compared with 13% in those with obstructive pulmonary disease (COPD) significantly
non-MDR organisms (P ¼ .004). MDR was associated with associated with dehiscence (P ¼ .043). There was no sig-
requiring reoperation (P ¼ .046) and hematoma (P ¼ .029). nificant association between the type of cardiothoracic
Polymicrobial infections were associated with flap failure procedure and postoperative complications (P > .1) or
(P ¼ .008), dehiscence (P ¼ .044), and seroma (P ¼ .003). death (P ¼ .827) (Table 4). Flap choice for reconstruction
There were no intraoperative deaths. Overall periop- was not associated with flap failure (P ¼ .089) or higher
erative 30-day all-cause mortality was 15.1% (n ¼ 18) mortality (P ¼ .624) (Table 4). Increasing severity of
(Table 3). Only 2 of these 18 deaths were directly related American Society of Anesthesiologists Physical Status
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Table 1. Patient Demographics Table 3. Morbidity and Mortality


Factors Overall (n ¼ 119) Outcome No. (%) (n ¼ 119)

Age, y 64.4  12.3 Mortality 18 (15.1)


Body mass index, kg/m2 30.6  6.5 Reoperation
Preoperative albumin, g/dL 2.85  0.80 Salvage 19 (16.0)
Smoking status New flap 5 (4.2)
Never 55 (46) Surgical site infection 21 (17.6)
Former 39 (33) Dehiscence 18 (15.1)
Current 24 (20) Hematoma 8 (6.7)
ASA Physical Status Classification Seroma 6 (5.0)
III 72 (61)

GENERAL THORACIC
No., number.
IV 42 (35)
V 1 (1)
Male sex 74 (62) confidence interval [CI], 1.06-69.1; P ¼ .044), and VRAM
Hypertension 93 (78) reconstruction was an independent predictor of SSI (OR,
MI/CAD 70 (59)
9.6; 95% CI, 1.4-66.4; P ¼ .022). MDR infection was an
independent predictor of developing any postoperative
Diabetes mellitus 60 (50)
complication (OR, 5.6; 95% CI, 1.3-23.2; P ¼ .018).
Insulin-dependent 31 (26)
Congestive heart failure 60 (50)
Chronic kidney disease 41 (34)
End-stage renal failure 18 (15) Comment
COPD 24 (20) The aim of this study was to provide additional insight
Chronic steroids 7 (6) into factors that contribute to the ultimate success of flap
Nonsteroid immunosuppressive agents 8 (7) reconstruction for DSWI after median sternotomy at a
high-volume center. Treatment algorithms based on the
Data are presented as mean  SD or number (%).
acuity and wound characteristics currently exist but do
ASA, American Society of Anesthesiologists; CAD, coronary artery dis- not take into account patient comorbidities.18 This high-
ease; COPD, chronic obstructive pulmonary disease; MI, myocardial
infarction. volume cardiothoracic experience offers a unique op-
portunity to examine the potential influence of many
Classification was significantly associated with higher different cardiac cases on outcomes after reconstruction.
mortality rates (P ¼ .003), as were increased CBT (P ¼ Interestingly, the type of cardiac procedure was not
.0001), need for open chest (P ¼ .020), CHF (P ¼ .049), significantly correlated with major flap complications or
ESRD (P ¼ .002), and low preoperative albumin (2.3 vs 2.9 higher mortality. One may expect a potentially more
g/dL, P ¼ .004) (Table 4). complicated course for patients undergoing more
By multivariable analysis, ESRD was an independent complicated initial cardiac operations (eg, aortic root
predictor of higher mortality (odds ratio [OR], 8.57; 95% repair) or heart/lung transplantation on immunosup-
pressive medications. Instead, the 2 cardiothoracic vari-
Table 2. Procedure Distribution ables associated with increased mortality in this
Procedure No. (%) (n ¼ 119) population were increased CBT and the need for open
chest management, 2 variables that increase mediastinal
Antecedent cardiothoracic procedure exposure to potential contamination and subsequent
CABG 48 (40.3) infection. Even at a high-volume center, the 15.1% mor-
CABG þ valve replacement 23 (19.3) tality reported in the above study is comparable to what
Valve replacement 18 (15.1) has been previously reported (Table 5).5,6,9,12,13,19-22
Aortic root 13 (10.9) This study found that VRAM reconstruction poses an
Lung or cardiac transplant 7 (5.9) increased risk of SSI in patients undergoing reconstruc-
Other 10 (8.4) tion. In fact, postoperative complications occurred in all 5
Internal mammary artery use patients who underwent VRAM flap reconstruction: 3
Unilateral 60 (50.4) were complicated by SSI, 1 required a salvage procedure
Bilateral 3 (2.5) for a dehiscence, and a hematoma developed in 1.
Flap choice for reconstruction Although pectoralis muscle flaps were used most
Unilateral pectoralis major 59 (49.6) commonly in our series, VRAM flaps were likely used in
Bilateral pectoralis major 48 (40.3) patients with more challenging reconstructions or more
Vertical rectus abdominis 5 (4.2) complicated prereconstructive procedure courses that
Omental 5 (4.2) were not well captured. Such reasons included prior
Combined pectoralis/omental 2 (1.7)
pectoralis flap failure, significant d ebridement that
rendered the pectoralis muscle less favorable for use, or
CABG, coronary artery bypass grafting; No., number. defects located at the inferior aspect of the sternum.
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Table 4. Variables Associated With Perioperative Mortality Rates pectoralis flap coverage (Figure 1).23,24 These in-
dications provide particularly unique challenges for the
Death Survival
Factors (n ¼ 18) (n ¼ 101) P plastic surgeon. Given the increased risk of SSI after
VRAM reconstruction, intraoperative sterile technique,
Patient copious irrigation, and ensuring adequate d ebridement
Age, y 63.6  10.8 64.6  12.7 .38 should be emphasized. Postoperative management may
Body mass index, kg/m2 31.3  7.4 30.5  6.4 .69 require more frequent wound checks with an emphasis
Preoperative albumin, g/dL 2.32  0.61 2.95  0.80 .004 on sterile dressings and short-interval follow-up
Hemoglobin A1c, % 8.24  3.1 8.06  2.4 .88 checks.
Smoking status .21 The literature supports an association between preex-
Never 50 46 isting renal dysfunction and death after cardiac proced-
Former 44 31 ures as well as development of sternal wound infection.25-
GENERAL THORACIC

Current 6 23
28
After flap reconstruction in these same patients,
ASA Physical Status .003 azotemia has been shown to be associated with higher
Classification rates of mortality, and ESRD has been described as an
III 33 68 independent predictor of death.8,29 In this series, ESRD
IV 61 32 again was found to be an independent risk factor for
V 6 0 higher mortality. Given that ESRD has been shown to be
Male sex 56 64 .50 strongly associated with development of DSWI, flap fail-
Hypertension 67 81 .17 ure, and higher mortality, it is evident that these patients
MI/CAD 56 60 .72 pose a particularly difficult problem to both the cardio-
Diabetes mellitus 61 49 .34 thoracic and plastic surgeons. Knowing the significant
Insulin-dependent 45 54 .60 risk of ESRD may allow for better preoperative coun-
Congestive heart failure 72 47 .05
seling and perioperative management.
Culture data also had a significant impact on the rate of
Chronic kidney disease 50 32 .32
complications after reconstruction. Similar to previous
End-stage renal failure 39 11 .002
reports, different microbes had no association with mor-
COPD 33 18 .14
tality rates.8 MDR infection was an independent risk
Chronic steroids 11 5 .31
factor for developing at least 1 of the studied complica-
Nonsteroid 11 6 .44
tions. The shift in management from antibiotics to
immunosuppressive agents
debridement and early flap coverage has decreased the
Cardiothoracic surgery
rate at which these particularly virulent organisms
Type of cardiothoracic procedure .83
develop within DSWI. For those who present after a delay
Emergent procedures 41 33 .51
in care to tertiary care centers, complication rates remain
Internal mammary artery use .11
high, and therefore, proper antibiotic stewardship is
None 33 9 important. Early consultation of the infectious disease
Unilateral 67 85 team is paramount in the treatment algorithm of this
Bilateral 0 5 particularly challenging subset of the studied population.
Redo sternotomy 33 18 .14 Other risk factors for postoperative complications
Non-midline sternotomy 6 2 .36 after sternal wound reconstruction include COPD,
Cardiopulmonary bypass 275  135 152  96 .0001 CHF, and low preoperative albumin. In general, COPD
time, min is a major risk factor for sternal dehiscence after me-
Required massive transfusion 11 5 .31 dian sternotomy.30-32 Studies have shown that the
Need for open chest 33 12 .02 increased chest diameter in patients with COPD leads
Required tracheostomy 22 13 .31 to elevated chest wall tension, particularly at the lower
Management of DSWI part of the sternum.33 Increased rates of dehiscence
Bridged with NPWT 11 12 .92 among women and patients with COPD needing flap
Late presentation 29 34 .73 reconstruction after DSWI highlight the necessity for
Delayed reconstruction 0 3 .47 particularly stout closures in these populations. Other
Prosthetic graft involvement 6 9 .63 studies have found CHF to be associated with any
Type of reconstruction .62 complication after reconstruction for DSWI and low
albumin to be associated with higher mortality.16,29
Data are presented as the mean  SD or percentage of patients. CHF decreases perfusion to the valuable flap tissue,
ASA, American Society of Anesthesiologists; CAD, coronary artery dis- putting these patients at risk of further complications.
ease; COPD, chronic obstructive pulmonary disease; DSWI, deep sternal Low albumin is a marker of poor nutritional status, and
wound infection; MI, myocardial infarction; NPWT, negative pressure
wound therapy. adequate nutritional support is necessary before and
after surgical procedures.
VRAM is sometimes preferred over pectoralis flaps Our study has several limitations, including its
for DSWI involving the lower sternum due to its retrospective design. The high mortality rate may also
superior coverage or for reoperation after failed be reflective of the tertiary referral status of the
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Table 5. Predictors of Morbidity and Mortality for Flap Reconstruction of Deep Sternal Would Infection After Median Sternotomy
Study
Authors, Design, Dates, Types of Morbidity and Outcome of
Journal, Year Cohort Size Flaps Used Mortality Interest Result

Cabbabe Retrospective, Bilateral pectoralis Dehiscence Predictors of Delayed


et al,19 Plast multicenter, major flaps (100%) (6.2%), morbidity and reconstruction associated
Reconstr single surgeon pressure sore mortality after with increased ventilator
Surg, 2009 1986-2008 (5.7%), immediate vs dependence, tracheotomy,
n ¼ 583 required skin delayed flap pressure sore, dehiscence,
graft (1.5%) reconstruction skin grafting, length of stay,
Mortality, 1.5% mortality
Patel et al,8 Retrospective, Bilateral pectoralis Seroma (1.6%), Predictors of ESRD, COPD, and mechanical
Plast single center, major (89.5%), hematoma morbidity and ventilation (per day) found

GENERAL THORACIC
Reconstr single surgeon unilateral (2.4%), SSI mortality to be independent
Surg, 2009 1997-2004 pectoralis major requiring following flap predictors of mortality
n ¼ 124 (9.7%), pectoralis debridement reconstruction
major and right (7.3%), flap
rectus abdominis failure (2.4%)
(0.8%) Mortality, 21%
Zahiri et al,16 Retrospective, Bilateral pectoralis Required Predictors of Diabetes mellitus, congestive
Ann Plast single center, advancement reoperation complications heart failure, and
Surg, 2012 multiple (20.8%), unilateral (18%), SSI after flap hypertension associated
surgeons pectoralis (17%), skin reconstruction with increased
1989-2010 advancement necrosis (4.7%), complications
n ¼ 106 (17.0%), bilateral flap necrosis
pectoralis turnover (3.8%),
(1.9%), unilateral dehiscence
pectoralis turnover (3.8%),
(23.6%), mixed hematoma
(turnover þ (2.8%)
advancement) Mortality, 2%
(29.2%), omental
(2.8%), latissimus
dorsi (0.9%), rectus
abdominis (0.9%),
other (2.8%)

COPD, chronic obstructive pulmonary disease; DSWI, deep sternal wound infection; ESRD, end-stage renal disease; SSI, surgical site infection.

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