sternoclavicular joint infection: a comparison of two surgical approaches

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Sternoclavicular Joint Infection: A Comparison of Two Surgical Approaches Varun Puri, MD, Bryan F. Meyers, MD, Daniel Kreisel, MD, PhD, G. Alexander Patterson, MD, Traves D. Crabtree, MD, Richard J. Battafarano, MD, PhD, and Alexander S. Krupnick, MD Division of Cardiothoracic Surgery, Washington University, St. Louis, Missouri Background. This study compares conventional open debridement with the recently proposed flap closure technique for sternoclavicular joint infection. Methods. This is a retrospective review of patients undergoing surgery for sternoclavicular joint infection during the last 7 years. Results. Twenty patients underwent 35 operations for sternoclavicular joint infection from 2002 to 2009. The debridement and open wound procedure (10 of 20 pa- tients, 50%) involved debridement of the clavicle, manu- brium, and first rib and open wound care. The joint resection and flap closure procedure (10 of 20 patients, 50%) involved partial resection of the clavicle, manu- brium, and first rib, with immediate (9 of 10) or early (1 of 10) wound closure with pectoralis major advancement flap. The two groups were comparable in comorbidities, duration of symptoms, radiologic findings, and microbi- ologic results. Despite an approach of planned reopera- tion for wound care, the open group had fewer mean procedures performed per patient (1.6 0.7 versus 1.9 1.6), owing to fewer unplanned procedures (0 versus 0.8 procedures/patient) than the flap group. The incidence of wound complications (hematoma, seroma) was lower in open patients (0 of 10 versus 5 of 10). The median length of hospitalization was shorter in the open group (5.5 versus 10.5 days), but all open patients (10 of 10; 100%) required prolonged wound care compared with 2 of 10 (20%) in the flap group. The only hospital mortality occurred in the flap group. Eventual wound healing was satisfactory in all survivors. Conclusions. For sternoclavicular joint infection, a sin- gle-stage resection and muscle advancement flap leads to a higher incidence of complications. Debridement with open wound care provides satisfactory outcomes with minimal perioperative complications but requires pro- longed wound care. (Ann Thorac Surg 2011;91:257– 62) © 2011 by The Society of Thoracic Surgeons S eptic arthritis of the sternoclavicular joint (SCJ) is an unusual problem with a low worldwide incidence [1]. Therapeutic options range from antibiotic therapy with or without joint aspiration to radical resection of the joint with flap reconstruction. Thoracic surgeons are often involved in the care of patients referred for surgical therapy because of the proximity of major vessels to the joint and the relatively frequent involvement of the first or even the second ribs in the process. During the last decade there have been several publications describing the successful use of joint resection and primary or early flap closure for SCJ infection (SCJI) [2– 4]. Our group has used both the more conservative approach of wide de- bridement and open wound care as well as the more recently adopted approach of joint resection and primary flap closure. To determine whether clinical outcomes from the two approaches were comparable, we reviewed our recent experience with SCJIs. Patients and Methods Data Acquisition We queried a prospectively maintained institutional car- diothoracic surgical database with the following key phrases: sternoclavicular infection, sternoclavicular sep- tic arthritis, clavicular infection/osteomyelitis. All the cases were from a single institution. The study was reviewed by the institutional review board and ex- empted. Patient records from 2002 through 2009 were reviewed. Case records were individually reviewed, and only patients with SCJ septic arthritis were included. Patients who had SCJI as a result of an infected median sternotomy were excluded. Operative mortality included those patients who died within the first 30 days after the operation and those who died later but during the same hospitalization. Follow-up was obtained through outpa- tient clinic visits and correspondence with local physi- cians. Active wound care for more than 2 weeks was defined as prolonged wound care. Statistical Analysis Data were analyzed using Stata software (StataCorp, College Station, TX). Comparison analyses were per- formed using Student’s t test with unequal variances for mean values, Mann-Whitney test for median values, and Accepted for publication July 21, 2010. Address correspondence to Dr Puri, Cardiothoracic Surgery, 3108 Queeny Tower, Barnes Jewish Hospital, One Barnes Jewish Hospital Plaza, St. Louis, MO 63110; e-mail: [email protected]. © 2011 by The Society of Thoracic Surgeons 0003-4975/$36.00 Published by Elsevier Inc doi:10.1016/j.athoracsur.2010.07.112 GENERAL THORACIC

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Page 1: Sternoclavicular Joint Infection: A Comparison of Two Surgical Approaches

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ternoclavicular Joint Infection: A Comparison ofwo Surgical Approaches

arun Puri, MD, Bryan F. Meyers, MD, Daniel Kreisel, MD, PhD,. Alexander Patterson, MD, Traves D. Crabtree, MD, Richard J. Battafarano, MD, PhD,

nd Alexander S. Krupnick, MD

ivision of Cardiothoracic Surgery, Washington University, St. Louis, Missouri

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Background. This study compares conventional openebridement with the recently proposed flap closure

echnique for sternoclavicular joint infection.Methods. This is a retrospective review of patients

ndergoing surgery for sternoclavicular joint infectionuring the last 7 years.Results. Twenty patients underwent 35 operations for

ternoclavicular joint infection from 2002 to 2009. Theebridement and open wound procedure (10 of 20 pa-

ients, 50%) involved debridement of the clavicle, manu-rium, and first rib and open wound care. The jointesection and flap closure procedure (10 of 20 patients,0%) involved partial resection of the clavicle, manu-rium, and first rib, with immediate (9 of 10) or early (1 of0) wound closure with pectoralis major advancementap. The two groups were comparable in comorbidities,uration of symptoms, radiologic findings, and microbi-logic results. Despite an approach of planned reopera-

ion for wound care, the open group had fewer mean

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ower, Barnes Jewish Hospital, One Barnes Jewish Hospital Plaza, St.ouis, MO 63110; e-mail: [email protected].

2011 by The Society of Thoracic Surgeonsublished by Elsevier Inc

rocedures performed per patient (1.6 � 0.7 versus 1.9 �.6), owing to fewer unplanned procedures (0 versus 0.8rocedures/patient) than the flap group. The incidence ofound complications (hematoma, seroma) was lower in

pen patients (0 of 10 versus 5 of 10). The median lengthf hospitalization was shorter in the open group (5.5ersus 10.5 days), but all open patients (10 of 10; 100%)equired prolonged wound care compared with 2 of 1020%) in the flap group. The only hospital mortalityccurred in the flap group. Eventual wound healing wasatisfactory in all survivors.

Conclusions. For sternoclavicular joint infection, a sin-le-stage resection and muscle advancement flap leads tohigher incidence of complications. Debridement with

pen wound care provides satisfactory outcomes withinimal perioperative complications but requires pro-

onged wound care.(Ann Thorac Surg 2011;91:257–62)

© 2011 by The Society of Thoracic Surgeons

eptic arthritis of the sternoclavicular joint (SCJ) is anunusual problem with a low worldwide incidence

1]. Therapeutic options range from antibiotic therapyith or without joint aspiration to radical resection of the

oint with flap reconstruction. Thoracic surgeons areften involved in the care of patients referred for surgicalherapy because of the proximity of major vessels to theoint and the relatively frequent involvement of the firstr even the second ribs in the process. During the lastecade there have been several publications describing

he successful use of joint resection and primary or earlyap closure for SCJ infection (SCJI) [2–4]. Our group hassed both the more conservative approach of wide de-ridement and open wound care as well as the moreecently adopted approach of joint resection and primaryap closure. To determine whether clinical outcomes

rom the two approaches were comparable, we reviewedur recent experience with SCJIs.

ccepted for publication July 21, 2010.

ddress correspondence to Dr Puri, Cardiothoracic Surgery, 3108 Queeny

atients and Methods

ata Acquisitione queried a prospectively maintained institutional car-

iothoracic surgical database with the following keyhrases: sternoclavicular infection, sternoclavicular sep-

ic arthritis, clavicular infection/osteomyelitis. All theases were from a single institution. The study waseviewed by the institutional review board and ex-mpted. Patient records from 2002 through 2009 wereeviewed. Case records were individually reviewed, andnly patients with SCJ septic arthritis were included.atients who had SCJI as a result of an infected medianternotomy were excluded. Operative mortality includedhose patients who died within the first 30 days after theperation and those who died later but during the sameospitalization. Follow-up was obtained through outpa-

ient clinic visits and correspondence with local physi-ians. Active wound care for more than 2 weeks wasefined as prolonged wound care.

tatistical Analysisata were analyzed using Stata software (StataCorp,ollege Station, TX). Comparison analyses were per-

ormed using Student’s t test with unequal variances for

ean values, Mann-Whitney test for median values, and

0003-4975/$36.00doi:10.1016/j.athoracsur.2010.07.112

Page 2: Sternoclavicular Joint Infection: A Comparison of Two Surgical Approaches

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258 PURI ET AL Ann Thorac SurgSTERNOCLAVICULAR JOINT INFECTION 2011;91:257–62

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2 test with Fisher’s exact test for proportions. A proba-ility value of 0.05 or less was considered significant.

urgical Techniqueor patients undergoing the open wound procedure, aockey-stick incision was made directly over the in-olved SCJ. The sternal and clavicular heads of theternocleidomastoid were sectioned. The head of thelavicle and the lateral part of the manubrium sterni wereesected en bloc or separately. The medial end of the firstib was generally débrided with rongeurs. The subcla-ian vein was protected and pleural entry avoided ifossible. The surrounding infected soft tissues wereharply débrided to healthy margins. If at the end of thenitial operation, it was believed that more debridementould be necessary, patients were brought back to theperating room for planned second-look procedures. Theesulting defects (Fig 1) were managed with saline-oaked gauze packing initially and generally converted toegative-pressure wound therapy (NPWT) within a feways. Most patients required prolonged wound care (�2eeks).For patients undergoing the flap procedure a similar

ockey-stick incision was used. The clavicle was dividedateral to the phlegmon with a Gigli saw. A segment of

anubrium adjacent to the SCJ was divided with aternal saw. This maintained a minimum of 50% of theanubrium intact, preserving the stability of the con-

ralateral upper thoracic cage. The medial end of the first

ig 1. The resulting defect after resection of the right sternoclavicu-

iar joint. The medial end of the first rib has been débrided.

ib was also divided and removed en bloc with the SCJpecimen. The SCJ was then dissected away from thenderlying inflammatory mass and anatomic structuresnd removed. Further debridement of the clavicle oranubrium could be performed at this time if the mar-

ins of debridement did not yet appear healthy. A partialectoralis major advancement flap was next mobilizednd inset to cover the soft tissue defect (Fig 2). One drainas placed under the flap, and another was placed

uperficial to the muscle. The drains were removed whenhe cumulative output of the two drains was less than 60

L/day and the drainage appeared nonpurulent. Antibi-tic use was individualized on the basis of culture results.

esults

wenty patients (10 women, 10 men) with a mean age of6.5 years underwent a total of 35 operations for SCJIrom 2002 to 2009. Pain (17 of 20 patients; 85%) andwelling (19 of 20 patients; 95%) were the main present-ng symptoms. A minority of patients (7 of 20 patients;5%) had documented fever before admission. Two ofwenty (10%) patients were taking immunosuppressive

edications, and another 7 of 20 patients (35%) wereiabetic. Thirteen of twenty patients (65%) had a discern-

ble focus of infection away from the SCJ: urinary tract

ig 2. A partial pectoralis major advancement flap has been used torovide coverage for the wound after joint resection.

nfection, 3 of 20 patients (15%); intravenous drug abuse–

Page 3: Sternoclavicular Joint Infection: A Comparison of Two Surgical Approaches

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259Ann Thorac Surg PURI ET AL2011;91:257–62 STERNOCLAVICULAR JOINT INFECTION

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elated bacteremia, 3 of 20 patients (15%); line sepsis, 2 of0 patients (10%); others, 5 of 20 patients (25%). Theatients had been symptomatic for a median of 2 weeksefore presentation.All patients underwent computed tomography or mag-

etic resonance imaging scans to document the presencend extent of infection. Representative images are shownFigs 3,4). Intraoperative microbiologic cultures yieldedrowth in samples obtained from the majority of patients16 of 20 patients; 80%). The organisms identified werexacillin-sensitive Staphylococcus aureus, 7 of 20 patients35%); methicillin-resistant S aureus, 6 of 20 patients30%); and streptococcus, 3 of 20 patients (15%).

The debridement and open wound procedure waserformed in 10 of 20 patients (50%), and the jointesection and flap closure procedure in 10 of 20 patients50%). The two groups were comparable in comorbidi-ies, duration of symptoms, computed tomography and

agnetic resonance imaging findings, and microbiologicesults (Table 1).

Despite an approach of planned reoperation for woundare, the open group had fewer procedures performeder patient as a result of fewer unplanned procedures peratient (Table 2). The open group also had a trend towardshorter hospital stay (Table 2).The incidence of wound complications (hematoma,

eroma) was lower in open patients, but all open patients10 of 10 patients; 100%) required prolonged wound careompared with 2 of 10 patients (20%) in the flap group.here were five significant wound complications in theap group (hematoma, 2 patients; flap dehiscence with

nfection, 2 patients; seroma, 1 patient) All these patientsequired wound reexploration. The 2 patients in the flaproup who required prolonged wound care had theirounds opened at unplanned repeat procedures. Thenly hospital mortality occurred in the flap group but wasttributable to unrelated causes. Eventual wound healingas satisfactory in all survivors. The patients in the openroup required wound care for a median of 12 weeks.

ig 3. Computed tomography scan showing left sternoclavicularoint infection. The changes are of predominant inflammation with

aarly bone erosion.

omment

he true incidence of SCJI is not known, but it is likely toe low, as reported in a review published in 2004 sum-arizing a total of 180 cases in the literature [1]. Simi-

arly, the fraction of patients requiring an operation forCJI is unclear. In the review by Ross and Shamsuddin

1], 102 of 174 patients (58%) underwent an operation, buthis is likely to be an overestimate when applied to theeneral population as it is more likely that patientsndergoing an operation are reported in the literature.thers have recommended that drainage using needle

spiration combined with antibiotics could be sufficientreatment in early disease [5].

Pain, swelling, and fever are the most common pre-enting complaints [1–4, 6]. In the review by Ross andhamsuddin [1], the most common risk factor was intra-enous drug use (21%), followed by infection at a distantite (15%), diabetes mellitus (13%), trauma (12%), andnfected central venous access (9%). Similarly, a variety ofredisposing conditions were present in our patients.Patients with an SCJ swelling may not have clear-cut

ystemic evidence of infection. Imaging with computedomography or magnetic resonance imaging scans isenerally warranted. Johnson and colleagues [7] notedhat although there was overlap with both SCJI andegeneration, the imaging findings that were signifi-antly associated with infection included joint distensionf 10 mm or greater, joint capsule distension extendingore than 5 mm over the clavicle and sternum, and

djacent bone marrow edema. Imaging findings of ero-ions, cortical irregularity, hyperemia, and enhancementere seen in both groups, although they were more

ommon with infection [7].Fifteen percent of our patients had an infection related

o intravenous drug abuse. The SCJ is more frequently

ig 4. Computed tomography scan showing left sternoclavicularoint infection. The image shows predominant bone lysis with littleoft tissue phlegmon. A contralateral pneumonia and effusion arelso seen.

nd disproportionately involved in septic processes in

Page 4: Sternoclavicular Joint Infection: A Comparison of Two Surgical Approaches

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260 PURI ET AL Ann Thorac SurgSTERNOCLAVICULAR JOINT INFECTION 2011;91:257–62

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his population. It is postulated that seeding occurs fromropagation of infection through the wall of the subcla-ian vein into the overlying SCJ, after injection of con-aminated narcotics into an upper extremity [8]. Also,ntravenous drug users might accidentally inject the SCJ,hile attempting to access the vessels of the head andeck for drug abuse [9]. The possibility of retained needle

ragments and resultant risk of a needlestick injury isuite real, and the surgeon must not bluntly dissect anbscess in an intravenous drug user with a gloved finger10, 11].

When faced with surgical management of SCJI, ourpproach is to resect the joint. A similar strategy has beendvocated in recent surgical literature [2–4]. When theiagnosis is indeterminate, an initial approach of incisionnd drainage with biopsy is justified. Once joint resectionnd debridement have been performed, the choice isetween immediate or early wound closure with a mus-le flap versus managing an open wound and allowingertiary closure. Burkhart and associates [4] managed 6 ofheir 20 patients with open wound care. Ten of ourwenty patients were managed with open wounds andequired an average of 1.6 procedures per patient, in-luding planned reoperations for debridement. The ob-

able 1. Baseline Patient Characteristicsa

ariable Al

ge (y) 56Mbesityedian duration of infection (wk)

ymptomsPain 1FeverSwelling 1

T/MRI positive 1adiologic severity of infection (5-point scale) (median)ulture positive 1RSA

Values are numbers with percentages in parentheses, mean � standard

T � computed tomography; DM � diabetes mellitus; MRI � mureus.

able 2. Operative Outcomes

ariable All (n � 20

umber of procedures/patienta 1.75 � 1.2umber of unplanned procedures/patienta 0.45 � 0.9ny complications 8/20 (40%)ound complications 5/20 (25%)

rocedure-related transfusions 2/20 (10%)edian hospital stay (days) 7 (2–55

rolonged wound care 12/20 (60%)

Values are mean � standard deviation.

ious disadvantage of this approach is the need forrolonged wound care. The use NPWT has mitigated theuisance value of the same to some degree. Also, ifdditional procedures are required for debridement, theatients already expect them as they have been appro-riately counseled about wound management. Exposedubclavian vessels in the bed of the wound are more of aheoretic concern as thick inflamed surrounding tissuenvariably covers them. In general, our patients did wellith the open wound approach.The use of NPWT has simplified the care of openounds in thoracic surgical patients. Through tissueechanical deformation, NPWT increases arteriolar di-

atation, blood flow, and tissue oxygenation in surgicalounds. It also reduces edema and the bacterial biobur-en and allows better tissue granulation and healing [12].e generally use NPWT within a few days after the

nitial debridement when no further operative debride-ent is planned, and the sponges are changed three

imes a week. The subclavian vessels are generally notxposed in the bed of the wound. Patients typicallyolerate this therapy well with support from home healthervices.

The use of flap closure of the defect has been success-

20)Open Wound Group

(n � 10)Flap Group

(n � 10) p Value

14.8 60.8 � 12.1 52.2 � 16.5 0.2%) 2 (20%) 4 (40%) 0.63%) 1 (10%) 1 (10%) 152) 2 (1–5) 2.5 (1–52) 0.39

%) 7 (70%) 10 (100%) 0.2%) 3 (30%) 4 (40%) 1%) 10 (100%) 9 (90%) 1%) 9 (90%) 8 (80%) 1

3.5 3.5 1%) 9 (90%) 7 (70%) 0.58%) 3 (30%) 3 (30%) 1

ation, or median with range in parentheses.

tic resonance imaging; MRSA � methicillin-resistant Staphylococcus

Open Wound Group(n � 10)

Flap Group(n � 10) p Value

1.6 � 0.7 1.9 � 1.6 0.590.1 � 0.3 0.8 � 1.3 0.13

1/10 (10%) 7/10 (70%) 0.020/10 (0%) 5/10 (50%) 0.030/10 (0%) 2/10 (20%) 0.47

5.5 (2–35) 10.5 (3–55) 0.1210/10 (100%) 2/10 (20%) 0.001

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Page 5: Sternoclavicular Joint Infection: A Comparison of Two Surgical Approaches

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ully used in the literature [2–4]. We used this approachrimarily at the time of joint resection in 10 of our 20atients but encountered a higher incidence of localroblems, including bleeding requiring reexploration inpatient, transfusion in 2 patients, and wound infection

r flap skin dehiscence in 2 patients. It is possible that themall number of patients in our series is a confoundingactor or that technical issues with the operation mayave led to some of these complications. Our goal haseen to perform an equivalent debridement in both thepen and flap groups as inadequate debridement isound to require repeat procedures in either group. Songnd coworkers [2] performed primary flap closure in 6atients, of which 5 had been previously treated with

ncision and drainage. This may lead to a lower load ofnfected tissue at the time of their joint resection and flaplosure. Similarly, Burkhart and colleagues [4] performedelayed closure in the majority of their patients (12 of 20atients) and thus likely had a lower load of infection in

he tissues at the time of flap closure. A strategy ofelayed closure with a flap may thus lead to better results

han primary flap closure.One of the obvious advantages of early or primary flap

losure is that no wound care is needed and patients mayroceed to discharge. This, however, may not be aignificant issue in a patient with numerous other problemshat necessitate continued hospitalization. With our reviewf our own data we are now more likely to perform jointesection and open wound care than primary flap closure inatients with SCJI. This is especially true in patients withther critical problems and when there is any doubt aboutomplete eradication of infection after our initial debride-ent. We are also more likely to consider delayed flap

losure of wounds after an initial period of open woundare.

In conclusion, for SCJI, a single-stage resection anduscle advancement flap leads to a higher incidence of

omplications in our hands. Debridement with open

ound care provides satisfactory outcomes with minimal

herapy is associated with equivalent long-term success

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2011 by The Society of Thoracic Surgeonsublished by Elsevier Inc

erioperative complications but requires prolongedound care.

eferences

1. Ross JJ, Shamsuddin H. Sternoclavicular septic arthritis:review of 180 cases. Medicine (Baltimore) 2004;83:139–48.

2. Song HK, Guy TS, Kaiser LR, Shrager JB. Current presenta-tion and optimal surgical management of sternoclavicularjoint infections. Ann Thorac Surg 2002;73:427–31.

3. Carlos GN, Kesler KA, Coleman JJ, Broderick L, TurrentineMW, Brown JW. Aggressive surgical management of sterno-clavicular joint infections. J Thorac Cardiovasc Surg 1997;113:242–7.

4. Burkhart HM, Deschamps C, Allen MS, Nichols FC 3rd,Miller DL, Pairolero PC. Surgical management of sternocla-vicular joint infections. J Thorac Cardiovasc Surg 2003;125:945–9.

5. El Ibrahimi A, Daoudi A, Boujraf S, Elmrini A, Boutayeb F.Sternoclavicular septic arthritis in a previously healthy pa-tient: a case report and review of the literature. Int J InfectDis 2009;13:e119–21.

6. Mikroulis DA, Verettas DA, Xarchas KC, Lawal LA, KazakosKJ, Bougioukas GJ. Sternoclavicular joint septic arthritis andmediastinitis. A case report and review of the literature.Arch Orthop Trauma Surg 2008;128:185–7.

7. Johnson MC, Jacobson JA, Fessell DP, Kim SM, Brandon C,Caoili E. The sternoclavicular joint: can imaging differentiateinfection from degenerative change? Skeletal Radiol 2010;39:551–8.

8. George S, Wagner M. Septic arthritis of the sternoclavicularjoint. Clin Infect Dis 1995;21:1525–6.

9. Kay DJ, Mirza N. Diagnosis and management of complica-tions of self-injection injuries of the neck. Ear Nose Throat J1996;75:670–6.

0. Blumstein H, Roberts JR. Retained needle fragments anddigital dissection. N Engl J Med 1993;328:1426.

1. Hutchins KD, Williams W, Natarajan GA. Neck needleforeign bodies: an added risk for autopsy pathologists. ArchPathol Lab Med 2001;125:790–2.

2. Baillot R, Cloutier D, Montalin L, et al. Impact of deepsternal wound infection management with vacuum-assistedclosure therapy followed by sternal osteosynthesis: a 15-yearreview of 23,499 sternotomies. Eur J Cardiothorac Surg

2010;37:880–7.

NVITED COMMENTARY

uri and associates [1] provide a thorough review of theisk factors, cause, and pathologic consequences of thencommon but challenging problem of sternoclavicular

oint infection [1]. Resection of the joint and necroticissue is the most effective treatment when boney de-truction and significant local phlegmon is present. Pai-olero and colleagues [2] appropriately stated in hismportant contribution to the management of sternalnfections to “follow the same time-honored principles ofound healing elsewhere: the wound must be drained

dequately; all necrotic tissue, devascularized tissue, andoreign material must be removed; and all residual space

ust be obliterated” [2].The primary message of Puri and colleagues’ [1] work

s that resection of the sternoclavicular joint and debride-ent of the wound followed by negative pressure wound

nd fewer complications compared with resection andebridement, and immediate pectoralis muscle flap cov-rage of the wound. Although the limited number ofatients in this series does not allow us to definitivelyccept their contention that immediate pectoralis muscleap coverage is inferior to open management with heal-

ng by “secondary intention.” the results do enlighten uso the use of the “alternative” open approach withegative pressure wound therapy.Other issues regarding the use of the partial pectoralisuscle flap advancement are important to this topic.

upport for primary muscle flap use to cover the brachio-ephalic vasculature after resection is not commonlyarranted. Although such coverage is an important con-

ideration after manubrial clavicular resection for pri-ary malignant lesions or when mediastinal tracheos-

omy is required after laryngopharyngectomy, it does not

0003-4975/$36.00doi:10.1016/j.athoracsur.2010.08.059