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CARDIOVASCULAR

Benefit of Partial Right-Bilateral Internal Thoracic


Artery Harvesting in Patients at Risk of Sternal
Wound Complications
Jacob Zeitani, MD, Alfonso Penta de Peppo, MD, Ruggero De Paulis, MD,
Paolo Nardi, MD, Antonio Scafuri, MD, Saverio Nardella, MD, and Luigi Chiariello, MD
Division of Cardiac Surgery, Tor Vergata University, Rome, Italy, and Second University of Naples, Naples, Italy

Background. Excellent long-term patency of the inter- Results. Incidence of obesity, chronic obstructive pul-
nal thoracic artery (ITA) graft promotes use of bilateral monary disease, diabetes, and peripheral vascular dis-
ITA bypass grafting; sternal devascularization, however, ease was higher in study patients. Postoperative Doppler
increases the risk of wound complications. We hypothe- ultrasonography detected reversed systolic dominant
sized that restricting right ITA (RITA) harvesting to a flow pattern. Wound complications occurred in 2 of 78
short proximal skeletonized segment (3 to 5 cm) would (2.6%) patients, compared with 14 of 143 (9.8%) after
result in adequate residual blood supply to reduce that bilateral ITA (p 0.04) and 8 of 160 (5%) after single ITA
risk. grafting (p ns). Technique of bilateral ITA harvesting
Methods. Seventy-eight patients with numerous risk (partial right versus full length; odds ratio, 0.2; confi-
factors for wound complications underwent composite dence interval: 0.04 to 0.9) and diabetes mellitus (odds
double ITA grafting, utilizing the RITA segment anasto- ratio, 2.7; 95% confidence interval: 1.1 to 6.3) were inde-
mosed to the left skeletonized ITA and to the obtuse pendent predictors of wound complications in the entire
marginal branch in Y fashion. Blood flow in the distal series.
RITA was assessed by parasternal transthoracic Doppler Conclusions. Substantial residual blood supply is de-
ultrasonography. Comparisons were made with prospec- tectable after partial RITA harvesting and may prevent
tively collected data of patients undergoing pedicled wound complications in high-risk patients.
single (n 160) or skeletonized bilateral ITA grafting (n (Ann Thorac Surg 2006;81:139 44)
143) during the same period. 2006 by The Society of Thoracic Surgeons

E vidence of better long-term patency of internal tho-


racic artery (ITA) grafts, compared with vein grafts
[1], promotes the use of arterial grafts for myocardial
patients, we proposed a method of partial right BITA
harvesting and composite arterial graft fashioning [18],
which seems to offer substantial residual blood flow to
revascularization. Despite availability of various arterial the middle and distal portions of the right hemisternum.
conduits, the ITA remains the ideal arterial graft [2], and The aim of this study was to assess the extent and pattern
several investigations appear to confirm the benefit of of that residual blood flow and the occurrence of wound
bilateral ITA (BITA) over single ITA (SITA) grafting for complications in selected patients.
myocardial revascularization [35]. Bilateral harvesting
implies, however, extensive devascularization of the ster-
num and increases the risk of postoperative tissue isch- Material and Methods
emia, leading to wound infection and dehiscence [6], in One thousand three hundred patients underwent iso-
particular in patients with additional risk factors of lated myocardial revascularization at our institution from
wound complications as diabetes mellitus, obesity, January 2002 to December 2004; of those, 78 patients
chronic obstructive pulmonary disease, or peripheral requiring revascularization of the left anterior descend-
arteriopathy [710]. As a consequence, although the tech- ing artery and of at least one large proximal obtuse
nique of skeletonization of the ITA may limit the extent of marginal branch, presenting two or more risk factors of
devascularization of the sternum and reduce the risk of sternal wound complications (obesity, diabetes mellitus,
complications [1117], BITA harvesting is frequently chronic obstructive pulmonary disease, peripheral vas-
avoided in patients with multiple risk factors. To main- cular disease, depressed left ventricular function), under-
tain the benefit of receiving two ITAs in those high-risk went BITA bypass grafting by using the method of partial
right ITA (RITA) harvesting and assembling the compos-
Accepted for publication June 8, 2005. ite graft in Y fashion. Ethical Review Board approval
Address correspondence to Dr Zeitani, Division of Cardiac Surgery, Tor
(December 10, 2001) and individual patient informed
Vergata University, Via Oxford 85, Rome 00133, Italy; e-mail: consent for surgical and additional radiologic procedures
zeitani@hotmail.com. were obtained.

2006 by The Society of Thoracic Surgeons 0003-4975/06/$32.00


Published by Elsevier Inc doi:10.1016/j.athoracsur.2005.06.025
140 ZEITANI ET AL Ann Thorac Surg
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PARTIAL RIGHT ITA HARVESTING 2006;81:139 44

Table 1. Data of Patients Who Received Skeletonized and second obtuse marginal branches. The sternum was
Bilateral Internal Thoracic Arteries (BITAs) or Pedicled reapproximated at the end of the procedure by using a
Single Internal Thoracic Artery (SITA) single stainless steal wire (A&E Medical Corporation,
Partial Right Full-Length Farmingdale, New Jersey) for each 10 kg of body weight.
BITAs BITAs SITA The fascia, subcutaneous layers and skin were closed
(n 78) (n 143) (n 160) with running absorbable sutures.
Sex (male/female) 56/22a 127/16 144/16
Ultrasonography and Radiography
Age (years) 69.5 5.7a 58.5 9.9c 62.2 8.5
NYHA class IIIIV 40 (51%)a 29 (20%) 23 (14%) To assess the preoperative blood flow in the distal RITA
Diabetes mellitus 40 (51%)a 43 (30%) 36 (22%) and the postoperative residual flow in the residual distal
COPD 40 (51%)a 20 (14%)c 6 (3.7%) RITA, a transthoracic color Doppler ultrasound scan
Peripheral vascular 20 (26%)a 16 (11%) 15 (9.3%) (Sonos 5500 and 7.5 MHz transducer; Hewlett Packard,
disease Andover, Massachusetts) was performed with intercostal
LVEF 50% 40 (51%)a 37 (26%) 39 (24%) approach at the fourth to fifth right parasternal space,
Obesity (body mass 20 (26%)b 15 (10%)c 37 (23%) obtaining two-dimensional images and pulsed Doppler
index 30 kg/m2) signals preoperatively and from the fourth to sixth post-
Reoperation for bleeding 2 (2.7%) 4 (2.8%) 3 (1.9%) operative day.
Bypass grafts 3.0 0.7 3.1 0.7 3.1 0.8 In 10 patients, an anteroposterior chest radiograph was
Distal ITA anastomoses 2.7 0.6a 2.1 0.6c 1.0 0.5 obtained in the operating room with portable equipment,
Cardiopulmonary bypass 81 28 82 27 85 26 protected by sterile drapes, after injection of 30 mL of
time (min) iodine solution through an 18G cannula inserted into the
Aortic crossclamp time 53 16c 54 18c 49 15 still unclipped end of the undissected distal RITA, to
(min)
visualize the residual vascular supply to the right hemis-
Sternal wound 2 (2.6%)b 14 (9.8%) 8 (5%)
complications ternum (the distal RITA and corresponding intercostal
Deep 0 (0%) 6 (4.2%)c 1 (0.6%) branches). On the fourth postoperative day, a multislice
Superficial 2 (2.6%) 8 (5.6%) 7 (4.4%) computed tomography (CT) scan was performed in the
same patients after injection of iodine solution in a
a
p 0.05 versus full-length BITA and SITA. b
p 0.05 versus peripheral vein, visualizing the distal RITA, veins, and
full-length BITA. c
p 0.05 versus SITA.
the corresponding intercostal branches.
COPD chronic obstructive pulmonary disease; LVEF left ventric-
ular ejection fraction; NYHA New York Heart Association.

Surgical Technique
Surgery was performed after skin preparation with pov-
idone-iodine solution and antibiotic administration (1 g
intravenous ceftizoxime) before incision; antibiotic pro-
phylaxis was continued for 48 hours postoperatively. The
partial right BITA harvesting technique and the method
of composite arterial graft fashioning have been de-
scribed previously [18]. Briefly, the left parasternal endo-
thoracic fascia is incised longitudinally, and the left ITA
(LITA) with the adjoining veins are visualized. The artery
is then harvested in a scheletonized fashion for the full
sternal length, by using titanium clips and scissors to
dissect collateral branches. Similarly, a proximal RITA
segment is dissected in a skeletonized fashion, from its
origin to the second or third intercostal space (3 to 5 cm)
Then, the free ends of the residual artery are clipped with
titanium clips, the segment is removed and anastomosed
as a free graft end-to-side to the in-situ LITA, in a
Y-graft configuration, approximately at the level where it
crosses the left pericardial border when distended to-
ward the left anterior descending artery. The RITA seg-
ment is anastomosed to the first obtuse marginal branch Fig 1. Postoperative multislice computed tomography scan of a pa-
and the in-situ LITA to the left anterior descending tient after harvesting of the proximal segment of the right internal
artery. In 45 patients the LITA was also sequentially thoracic artery, showing the residual artery (arrow), vein, and corre-
anastomosed to a diagonal branch, and in 7 patients the sponding intercostal branches (roman numerals indicate intercostal
RITA segment was sequentially anastomosed the first spaces).
Ann Thorac Surg ZEITANI ET AL 141

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2006;81:139 44 PARTIAL RIGHT ITA HARVESTING

Wound complications were observed during hospital- Table 2. Predictors of Sternal Wound Complications
ization or detected by physical examination at the outpa-
Univariate
tient clinic during the first 2 postoperative months of Analysis Multivariate Analysis
follow-up; they included instability of the sternum, with-
out evidence of tissue infection, or sternal wound infec- Odds
tion, according to the guidelines for prevention of surgi- Risk Factor p Value Ratio 95% CL p Value
cal site infection of the Hospital Infection Control Diabetes mellitus 0.04 2.7 1.16.3 0.02
Practices Committee [19]. In particular, superficial infec- Type of BITA harvesting 0.04 0.2 0.040.9 0.03
tion was defined as wound erythema and purulent dis- (partial right versus
charge involving the skin and the subcutaneous layers full length)
without involvement of sternal or mediastinal tissues; COPD 0.46
deep infection was diagnosed in case of one of the Obesity 0.80
following: visual evidence of mediastinitis, isolation of an
BITA bilateral internal thoracic artery; CL confidence limits;
organism from culture of mediastinal tissue or fluid, or COPD chronic obstructive pulmonary disease.
fever or instability of the sternum associated with puru-
lent drainage from the mediastinum. Patients character-
istics and occurrence of sternal wound complications graphs after direct injection of iodine solution in the
were compared with the prospectively collected data of residual distal RITA showed the artery and the corre-
143 consecutive patients undergoing isolated bypass sponding intercostal branches from the fourth to fifth
grafting with skeletonized BITAs during the same period, intercostal spaces; that residual vascular supply was also
and of 160 patients submitted to pedicled SITA grafting well identified at postoperative CT scanning (Fig 1).
on the same dates (2 days before or after). The decision Aortic cross-clamp time was about 5 minutes longer
for the number of ITAs and the method of harvesting was during BITA than SITA bypass grafting; among BITA
taken by one of the four attending surgeons involved in patients, an average of 2.7 distal ITA anastomoses were
the series. Patients undergoing off-pump bypass or con- performed with the composite Y grafting procedure, a
comitant procedures were excluded. number significantly higher than with in situ BITAs
(Table 1). The postoperative Doppler analysis detected
Statistical Analysis systolic dominant inverted flow in the distal RITA.
Comparisons of variables were performed by the un- Mediastinitis did not occur. Analysis of the entire
paired Students t test, 2 or Fishers exact test, as series of 381 patients showed that the rate of wound
appropriate. Influence of variables on wound complica- complications was higher among patients with diabetes
tions was assessed by univariate analysis; factors poten- mellitus (12 of 107, 10%, versus 12 of 250, 4.6%; p 0.04);
tially affecting sternal wound complications included age, incidence of deep infection or dehiscence was also higher
sex, III to IV New York Heart Association functional class, in diabetic patients (5 of 114, 4.2%, versus 2 of 260, 0.8%;
echocardiographic left ventricular ejection fraction lower p 0.02). Wound complications were less frequently
than 50%, diabetes mellitus, obesity (body mass index observed after partial right than after full-length BITA
30 kg/m2), chronic obstructive pulmonary disease, pe- harvesting (2.6% versus 9.8%, p 0.03). Instability of the
ripheral vascular disease, type of ITA harvesting (single sternum without evidence of tissue infection occurred in
in pedicled fashion, skeletonized full-length bilateral, 2 patients (1.4%) in the full-length BITA group; deep
skeletonized partial right bilateral), and time of cardio- wound infection was diagnosed in 4 more patients (2.8%)
pulmonary bypass. Factors with a probability (p) value in that group, in 1 patient (0.6%) in the SITA group, and
less than 0.1 were then included in a stepwise logistic in no patient in the partial right BITA group. Incidence of
regression prediction model. Variables are presented as deep wound complications was higher in the full-length
mean 1 SD. A p value less than 0.05 was considered than in the partial right BITA group, although at low
statistically significant. Statistical analysis was done by statistical power (4.2% versus 0%, p 0.06); nevertheless,
SPSS statistical software package (SPSS, Chicago, comparisons with patients receiving a SITA demon-
Illinois). strated a significantly higher rate of deep wound prob-
lems after full-length but not after partial right BITA
harvesting (4.2% versus 0.6%, p 0.03, and 0% versus
Results 0.6%, p not significant; Table 1). A multivariate analysis
Patients undergoing partial right BITA harvesting were in the entire series was then performed, showing that
older and presented more risk factors of wound compli- both diabetes and technique of BITA (partial versus
cations than patients undergoing SITA or full-length full-length RITA) harvesting were independent predic-
BITA harvesting (Table 1). The preoperative transtho- tors of wound complications (Table 2).
racic color Doppler ultrasonography detected antegrade All patients with deep wound complications under-
flow in the distal RITA with the normal pattern of a went reoperation for debridement of necrotic and devas-
peripheral artery. A shorter operative time was required cularized tissue and direct closure of the sternum, fascia,
for dissection of the proximal segment than for dissection and superficial layers, associated with intravenous anti-
of the full sternal length of the RITA (5.7 0.7 versus 19.8 biogram-guided antibiotic therapy in patients with pos-
2.6 minutes, p 0.001). Intraoperative chest radio- itive cultures or wide-spectrum antibiotic prophylaxis in
142 ZEITANI ET AL Ann Thorac Surg
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PARTIAL RIGHT ITA HARVESTING 2006;81:139 44

aseptic sternal dehiscence. They experienced complete sidual blood supply, and therefore wound healing, in
wound healing. Patients with superficial wound compli- those high-risk patients.
cations were also treated by surgical debridement, pri- We hypothesized that a proximally limited dissection
mary closure of wound dehiscence and antibiotic treat- of the RITA would leave a residual vascular supply to the
ment, as described previously [20]; one procedure failed right hemisternum through the distal RITA, promoting
and was crossed over to conventional topical treatment more efficient wound healing, in particular in patients
until secondary wound healing. presenting with numerous risk factors for complications.
Although use of the distal arterial segment would result
in residual antegrade perfusion to the chest wall, the
Comment proximal ITA segment was preferred as it presents a
Different surgical strategies have been developed during larger diameter, which facilitates fashioning of the com-
the last decade to achieve the optimal myocardial revas- posite graft. Interestingly, postoperative Doppler analy-
cularization for each patient. It is now well documented sis of blood flow in the distal RITA, which could now be
that the ITA graft compares favorably with other con- considered as the terminal branch of the right superior
duits, owing to the relatively large vessel diameter and epigastric artery, showed inverted systolic dominant flow
the physiologic properties of the arterial wall, which pattern, as previously reported [18]. Connections to the
provide for high flow and long-term patency [1, 2]. Use of lower intercostal branches and to the inferior epigastric
BITAs has been recently reported to improve survival artery appear to provide, therefore, for a persistent blood
and freedom from recurrent angina [35] but, at the same supply to the middle and distal portions of the right
time, to cause extensive devascularization of the ster- hemisternum that should be advantageous to promote
num, increasing the risk of wound infection and dehis- wound healing. Indeed, owing to the inclusion criteria,
cence [6]. That risk appears to increase seriously in patients selected for the described technique presented
patients with additional known risk factors as diabetes several potential risk factors of wound complications; yet,
mellitus or chronic obstructive pulmonary disease [710]. sternal wound problems rarely occurred in these pa-
Recently, for example, Molina and colleagues [10] re- tients, showing a significantly lower rate of wound com-
plications all together when compared with control BITA
ported an high incidence of wound infection in obese
graft patients. Also, fewer deep wound complications
patients, with a high mortality rate, and questioned
were observed in the former group, but at a low statistical
whether BITA harvesting should be performed in these
power, possibly as result of the several inclusion criteria
patients. Unlike pedicled ITA harvesting, the technique
selecting a homogeneous but relatively small group of
of skeletonization reduces the extent of devascularization
coronary patients for the partial right BITA harvesting
of the chest wall, leaving veins, muscle and surrounding
procedure; nevertheless, occurrence of deep complica-
endothoracic tissue in place and is, therefore, potentially
tions after full-length, but not partial right, BITA harvest-
associated with fewer postoperative wound complica-
ing compared unfavorably with single ITA harvesting,
tions: indeed, occurrence of sternal wound infection
thus enhancing the clinical significance of these observa-
appears consistently low after routine use of bilateral
tions in that subset of complications and underlining the
skeletonized ITAs [1517]. For example, the 2.8% rate of overall benefit of the proposed technique in preventing
deeper wound infection in the present series is similar to wound problems. Findings were confirmed by a multi-
the recently reported rates of 1.7% by Matsa and associ- variate analysis of the potential risk factors in the entire
ates (13), 2.2% by Pevni and colleagues [21], or 2.4% by series of 381 patients, still showing that type of BITA
Sauvage and coworkers [22]. Other recently published harvesting (partial versus full-length RITA) and diabetes
investigations in patients with diabetes also report a very mellitus were independent predictors of wound
moderate prevalence of wound problems after BITA complications.
skeletonization, with deep sternal infection rates from It has to be noted that the observed rate of 4.2% of deep
1.3% to 4% [11, 13, 23]. wound complications after full-length BITA skeletoniza-
Previous observations at our institution [14] also sug- tion appears relatively high when compared with preva-
gest a lower rate of wound infections after skeletoniza- lence of deep sternal infection, the more frequently
tion of BITAs than after harvesting both arteries in a reported wound problem, in the literature; that may
pedicled fashion; indeed, skeletonization may preserve a account for the statistical significance of that figure in the
number of sternal and intercostal branches arising as a present study. It should be considered, however, that
common trunk from the ITA [24], maintaining some postoperative sternal instability without evidence of in-
collateral flow to the sternum. Also, implantation of fection is potentially related, as sternal infection, to the
bilateral in-situ ITAs has the advantage of maintaining extent of sternal devascularization and therefore to the
two separate blood supplies to the myocardium, avoiding technique of harvesting, thus validating our definition of
additional anastomoses to fashion a composite graft. deep wound complication that was anyhow adopted for
Nonetheless, we also found that the risk of wound all observations in the series.
complications seemed to increase greatly in patients with Feasibility of the described composite Y grafting pro-
several risk factors for wound infection; the present study cedure requires a favorable coronary anatomy, with a
suggests that the proposed method of partial right BITA large and proximally located obtuse marginal branch; in
harvesting and skeletonization may further improve re- that case, a rather short proximal segment of the RITA
Ann Thorac Surg ZEITANI ET AL 143

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2006;81:139 44 PARTIAL RIGHT ITA HARVESTING

appears adequate, as part of the composite Y graft, to grafting: effects on mortality and event-free survival.
reach the first and sometimes the second marginal J Thorac Cardiovasc Surg 2004;127:1408 15.
5. Lytle BW, Blackstone EH, Loop FD, et al. Two internal
branches. Otherwise, should further sternal devascular- thoracic artery grafts are better than one. J Thorac Cardio-
ization be required to harvest a longer segment, other vasc Surg 1999;117:85572.
arterial grafts, as the radial artery, may replace the RITA 6. Seyfer AE, Shriver CD, Miller TR, Graeber GM. Sternal
as second conduits to reach the circumflex territory, blood flow after median sternotomy and mobilization of the
internal mammary arteries. Surgery 1988;104:899 904.
accomplishing complete arterial revascularization of the 7. Kouchoukos NT, Wareing TH, Murphy SF, Pelate C, Mar-
left ventricle with, one hopes, a good patency rate. In our shall WG. Risks of bilateral internal mammary artery bypass
technique, the proposed length of the RITA segment may grafting. Ann Thorac Surg 1990;49:210 9.
vary from 3 to 5 cm, depending on the number and 8. Ridderstolpe L, Gill H, Granfeldt H, Ahlfeldt H, Rutberg H.
Superficial and deep sternal wound complications: inci-
location of the marginal branches needing revasculariza- dence, risk factors and mortality. Eur J Cardiothorac Surg
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early and late mortality, morbidity and cost of care. Ann
ommended before RITA harvesting. Furthermore, the Thorac Surg 1990;49:179 87.
proposed composite Y-graft technique provides the pos- 10. Molina JE, Lew RS, Hyland KJ. Postoperative sternal dehis-
sibility of sequential grafting of the LITA to the left cence in obese patients: incidence and prevention. Ann
anterior descending artery and diagonal branches; con- Thorac Surg 2004;78:9127.
11. Peterson MD, Borger MA, Rao V, Peniston CM, Feindel CM.
sequently, more arterial distal anastomoses per patient Skeletonization of bilateral internal thoracic artery grafts
were performed with that technique than with bilateral lowers the risk of sternal infection in patients with diabetes.
in-situ ITA grafting. J Thorac Cardiovasc Surg 2003;126:1314 9.
In conclusion, the proposed method of BITA grafting, 12. Parish MA, Asai T, Grossi EH, et al. The effects of different
techniques of internal mammary artery harvesting on ster-
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distal sternal tissues, appears to prevent wound compli- 13. Matsa M, Paz Y, Gurevitch J, et al. Bilateral skeletonized
cations in selected patients at high risk of this complica- internal thoracic artery grafts in patients with diabetes.
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14. De Paulis R, de Notaris S, Scaffa R, et al. The effect of
more grafts by means of the two ITAs at acceptable risk. bilateral internal thoracic artery harvesting on superficial
and deep sternal infection: the role of skeletonization. J Tho-
Limitations of the Study rac Cardiovasc Surg 2005;129:536 43.
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