urgical Management of Invasive Pulmonaryungal Infection in Hematology Patients
anjay Theodore, MCh, Matthew Liava’a, MBChB, Phillip Antippa, FRACS,ochelle Wynne, PhD, Andrew Grigg, FRACP, Monica Slavin, FRACP, and
ames Tatoulis, MD, FRACSepartments of Cardiothoracic Surgery and Haematology, and Victorian Infectious Diseases Service, The Royal Melbourne
ospital, University of Melbourne, Parkville, Victoria, Australia
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Background. The purpose of this study was to analyzeur institutional results with pulmonary resection ineutropenic patients with hematologic malignancies anduspected invasive pulmonary fungal infections.
Methods. We performed a retrospective medical recordeview of 25 immunocompromised patients with hema-ologic malignancies who underwent pulmonary resec-ion between 2000 and 2007. We analyzed preoperativeiagnostic technique, degree of pulmonary resection, andostoperative morbidity and mortality to determinehether surgery is a viable treatment option in this
ubset of patients.Results. Twenty-three of 25 patients had a minithora-
otomy compared with 2 who had video-assisted thoras-
opic surgery resection only. Thirteen had wedge resec-
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urgery, Royal Melbourne Hospital, Victoria, 3052, Australia; e-mail:[email protected].
2009 by The Society of Thoracic Surgeonsublished by Elsevier Inc
ions, 9 had lobectomies, and 3 had segmentectomies.arly surgical morbidity was 2 of 25, involving 1 pneu-othorax and 1 empyema. In-hospital mortality was 2,ith 1 death primarily related to surgery. Median sur-
ival was 342 days, and survival was significantly bettern patients with only one lesion. No patient experiencedate recurrence of invasive pulmonary fungal infection.esected pulmonary tissue also provided the best chance
or a proven diagnosis in 19 of 25 (76%).Conclusions. This study confirms that pulmonary re-
ection in high-risk immunocompromised patients withuspected invasive fungal infection can be carried outith excellent operative morbidity and mortality.
eutropenic patients are at high risk of developinginvasive fungal infections (IFI), particularly those
atients undergoing chemotherapy for hematologic ma-ignancies and allogeneic stem cell transplantation (SCT)1, 2]. The annual incidence of IFI is now 3.7% to 8.8% int risk patients following treatment with high dose che-otherapy for acute leukemia or allogeneic bone marrow
ransplantation [1, 3]. The epidemiology of fungal infec-ions has changed in the last two decades with the usef fluconazole, and now molds have replaced Candidapecies as the most common cause of IFI [3]. Invasivespergillosis is the most common mold infection, andhe lungs are the site of infection in more than 90% ofatients [4].However, the increasing use of broad-spectrum anti-
ungal prophylaxis to prevent invasive aspergillosis mayllow fungi other than Aspergillus species to become morerequent causes of infection [5, 6]. Furthermore, infec-ions occurring despite antifungal prophylaxis mandateggressive diagnostic procedures to determine the causef infection and appropriate antifungal therapy.The risk of IFI is directly related to the duration of
eutropenia as well as corticosteroid use and the pres-nce of graft-versus-host disease after SCT [1, 2]. Neu-
ccepted for publication Feb 24, 2009.
ddress correspondence to Dr Antippa, Department of Cardiothoracic
ropenic patients with IFI still have high morbidity andortality despite improved medical therapy, the avail-
bility of newer antifungal agents, and the tendency toreat patients earlier before waiting for a confirmediagnosis of invasive aspergillosis [3, 7]. Recent multi-enter reviews of patient survival from invasive aspergil-osis show a 4-month mortality of 62% in all hematologyatients [8] and a 77% attributable mortality at day 150fter infection in allogeneic SCT recipients [3]. The reporty Jantunen and colleagues [9] on a series of allogeneicCT recipients with invasive aspergillosis managed med-
cally also had only a 37% response to treatment and0.5% with a complete response; median survival afteriagnosis was 37 days.Despite these limited results, medical management has
een the cornerstone of treatment. The role of surgery,owever, is controversial, as the risk of lung resection in
he context of neutropenia and thrombocytopenia isnclear. American and European guidelines for surgical
ntervention in the treatment of invasive aspergillosisnclude a pulmonary lesion contiguous with a largeessel or pericardium, a single lesion as the source ofemoptysis, erosion into the pleural space and ribs, andn a case by case basis in localized extrapulmonary
esions [5, 10]. Other authors recommend resection ofevitalized tissue particularly when Zygomycetes or Sce-osporium species are involved as well as resection of a
ocalized Aspergillus lesion before allogeneic transplanta-
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ion [6, 11]. Few centers undertake surgical interventionutside of these guidelines [12]. However, contemporaryvidence shows surgery can be both diagnostic andherapeutic, leading to better outcomes when comparedith medical management alone [7, 13]. To further in-
orm this debate we describe a series of neutropenicatients with hematologic malignancies undergoing re-ection for fungal infection in an Australian tertiary-careeferral teaching hospital.
aterial and Methods
amples and Settingnstitutional ethics committee approval was obtained,nd the requirement for patient consent was waived.ncluded in the analysis were all neutropenic patientsith hematologic malignancies being treated with high-ose chemotherapy for acute leukemia or allogeneicCT, who underwent lung resection for proven, proba-le, or possible IFI between 2000 and 2007. This repre-ented one third of hematology patients admitted forresumed IFI during the same period. Twenty-threeatients in this series had received antifungal prophy-
axis before surgery with at least one of the followingpatients were entered into a separate study to determinehe best prophylactic agent): oral itraconazole, voricon-zole, or posaconazole, although 1 patient received onlyuconazole and 1 patient did not receive antifungalrophylaxis. All neutropenic patients with fever persist-
ng beyond 96 hours or recurring after response toroad-spectrum antibacterial agents underwent high-esolution computed tomography (CT) of the chest. Bron-hoalveolar lavage was performed routinely on thoseho had radiologic abnormalities suggestive of IFI (halo
ig 1. Computed tomographic scan of the chest with peripheral air-
wrescent sign.
ign, nodules, air crescent, or localized pathologic diseasen the absence of a microbiologic diagnosis; Figs 1 and 2).omputed tomography-guided core biopsy was per-
ormed when feasible, and panfungal polymerase chaineaction was performed on resected lung tissue in someatients after 2002 as part of an evaluation of this test [14].erum and bronchoalveolar lavage galactomannan test-
ng was not performed. Patients were operated on ifadiologic findings suggested complete resection wasossible, or in diffuse disease when histologic confirma-
ion was requested to aid antifungal treatment.
efinitionseutropenia was defined as an absolute neutrophil count
f less than 0.5 � 109 cells/L. Invasive fungal infectionas classified according to the internationally acceptedefinitions as proven (when there was sterile site tissuevidence of hyphae or a positive culture), probable (whenost, clinical, and microbiologic criteria were met), andossible (when host and clinical factors but no microbi-logic criteria were present but there was no microbio-
ogic confirmation of infection) [15].Early mortality was defined as death occurring within
0 days of surgery. In-hospital mortality was defined asortality during current hospital admission owing to any
ause and late mortality was death at greater than 30ostoperative days.
ERIOPERATIVE AND POSTOPERATIVE SUPPORTIVE CARE. Plateletnd granulocyte infusions were given to maintain plate-et counts greater than 50 � 109/L and granulocyte countsreater than 0.5 � 109/L. Recombinant human granulo-yte colony-stimulating factor was used in severely neu-ropenic patients. Antibiotic and antifungal medications
ig 2. Computed tomographic scan chest with halo sign.
ere continued in the perioperative and postoperative
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1534 THEODORE ET AL Ann Thorac SurgSURGERY FOR IFI 2009;87:1532–8
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eriods. Patients were extubated in the operating room,nd pain relief was administered by means of an epiduralhen patients had adequate platelets. All patients hadatient-controlled analgesia. Initial postoperative man-gement was in the high-dependency unit of the cardio-horacic ward, and patients were transferred to the he-
atology ward after removal of chest drains. Length ofostoperative antifungal therapy was at the discretion of
he treating hematologist. Most patients had a prolongedospital stay in the hematology unit. Surviving patientsere followed up in the hematology outpatientepartment.
tatistical Analysisata were analyzed using the Statistical Package for theocial Sciences (SPSS), version 15 (SPPS Inc, Chicago,L). The distribution of continuous variables, with thexception of age, was skewed, and logarithmic transfor-ations did not increase normality. As such, medians are
eported instead of means and the measures of disper-ion are 25th (quartile 1 [Q1]) and 75th (quartile 3 [Q3])ercentile ranks of the distribution. Group comparisonssed �2 or Mann-Whitney U tests. Actuarial survivalurves were graphed using the Kaplan–Meier method tollustrate overall sample survival and to show survivalifferences for patients who had diagnostic versus ther-peutic resections.
esults
isease Characteristicsetween September 2000 and May 2007, 25 patients were
dentified as undergoing pulmonary resection for IFI. All
Data are presented as number and % or median, quartile 1, and quartile 3.
T � computed tomographic. V
ad hematologic disorders and a recent history of pro-onged febrile neutropenia with documented periods ofeutrophil counts less than 0.5 � 109/L after high-dosehemotherapy (Table 1). There were 10 (40%) men and 1560%) women in the cohort. The mean age was 51.3 � 14.2ears (range, 20 to 72 years) at the time of surgery. Theost frequent underlying hematologic diagnosis was
cute myeloid leukemia.
iagnosisight (32.0%) patients had multiple infiltration sites onT scan; however, the majority of infiltrates were local-
zed lesions or halo signs (Table 1). Five (20.0%) patientsnderwent CT-guided core biopsy that failed to achieveistologic or microbiologic confirmation of the diagnosis.ronchoscopy with bronchoalveolar lavage was positive
n only 10% (2 of 21) of patients tested. Nineteen patientsad proven IFI on the basis of hyphae visualized onistologic specimens (n � 12), a cultured organism from
ung tissue (n � 6), or detected by polymerase chaineaction (n � 1; Table 2). Culture-diagnosed speciesdentified included two cases of Scedosporium apiosper-um and one each of Aspergillus niger and Scedosporium
rolificans. All other organisms identified were Aspergillusumigatus.
1535Ann Thorac Surg THEODORE ET AL2009;87:1532–8 SURGERY FOR IFI
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urgical Management
atients had surgery under general anesthesia, usingouble-lumen intubation and a limited lateral muscle-paring thoracotomy. Twenty-three (92.0%) had ainithoracotomy, and 2 (8.0%) had video-assisted thora-
oscopic surgery (Table 3). Two patients had primaryideo-assisted thoracoscopic surgery that was convertedo a small, lateral muscle-sparing thoracotomy. Patientsndergoing video-assisted thoracoscopic surgery resec-
ion were more likely to have diffuse bilateral disease,nd resection was primarily diagnostic. Three (12.0%)atients with diffuse bilateral fungal lesions had resec-
ion performed on the lung that was most affected.
arly Outcomes
here were no deaths directly attributable to operativentervention within the first 30 days and no reoperationsor bleeding. However, hospital mortality was 8% as 2atients died before discharge, 1 at day 32 of cerebralspergillosis and brain stem herniation and 1 at day 80 ofacterial sepsis. One patient experienced a pneumotho-ax after tube removal, and 1 patient had an empyemahat required decortication. Two minor complicationsncluded a pleural effusion and a pneumothorax, both ofhich required intercostal drainage.
ate Outcomes
n December 2007, 18 (72.0%) patients were deceased.edian survival after surgery was 342 days (Q1, 124; Q3,
ig 3. Total survival after lung resection for invasive fungal infec-ion. Survival function is plotted as the solid line, with censored pa-
Tients represented by crosses.
97.5) for the total sample as illustrated in Figure 3. Thereas insufficient evidence to suggest a difference in sur-
ival time between young (less than 60 years of age, 732ays; Q1, 123.7; Q3, 1821.7) versus older patients (60 yearsr older, 259 days; Q1, 109; Q3, 670.5; z � �1.36; p �.174).Deceased patients’ (n � 18, 72.0%) median survival was
39 days (Q1, 102.5; Q3, 666.2). For patients alive at lastollow-up in December 2007 (n � 7, 28.0%), medianurvival was 33.2 months (Q1, 12.6; Q3, 65.8). Not surpris-ngly there was a significant relationship between earlyr late mortality and whether patients had single orultiple lesions and because 3 patients had a primarily
iagnostic, not therapeutic, procedure for diffuse disease.omparison of survival for single or multiple lesions is
hown in Figure 4. Essentially patients with single lesionsn � 12, 70.6%) were more likely to survive more than 90ays after surgery than patients with multiple lesions
n � 2, 25.0%; �2(1) � 4.59; p � 0.032; 95% confidencenterval, 1.07 to 48.6).
omment
atients undergoing chemotherapy for acute leukemiand allogeneic SCT are at the highest risk for IFI [16].ortality remains high even in patients treated at the
arliest suspicion of IFI without microbiologically provennfection [17]. Although the role of surgery is not wellefined in these patients, it has several potential benefits.
ig 4. Survival comparison after diagnostic versus therapeutic resec-ion. Therapeutic resection is plotted as the dashed line, versus diag-ostic procedure as the solid line. Censored patients in the therapeu-
ic group are represented by crosses.
his report highlights the diagnostic and therapeutic role
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1536 THEODORE ET AL Ann Thorac SurgSURGERY FOR IFI 2009;87:1532–8
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f surgery for pulmonary IFI (predominantly invasivespergillosis) in this subset of patients.Diagnosis of IFI in these patients is difficult as theajority of patients present with pyrexia of unknown
rigin unresponsive to antibiotics. Unlike other series,ost of our patients presented with nonspecific symp-
oms and few had symptoms related to the respiratoryract. Most patients were taken to surgery with a pre-umptive diagnosis of invasive pulmonary aspergillosisrom suspicious CT scans in the setting of febrile neutro-enia [16]. High-resolution CT scans play a crucial role inrriving at a clinical diagnosis in this difficult set ofatients. The halo sign has emerged as a highly sugges-
ive sign for early invasive aspergillosis during neutro-enia [18]. Other frequent signs seen in these patients areround-glass appearance and cavitation.Surgical biopsies and resected specimens give a con-
rmed diagnosis with extremely good accuracy, often onhe same day, which expedites the choice of appropriatentifungal treatment. Importantly, the biopsy findings inur patients detected organisms other than Aspergilluspecies in 3 of the 25 cases. Thus, even when a microbi-logic diagnosis was not made, surgical resection andppearance of hyphae seen in tissue was still helpful inetermining whether the infection was likely to be as-ergillosis or another diagnosis such as infarction orbrosis, which occurred in 4 patients.Nonsurgical investigative modalities are plagued with
ow yield, and have low specificity and sensitivity, par-icularly in the presence of empiric antifungal therapy. Inur series, bronchoalveolar lavage cultured fungus innly 10% (2 of 21) of patients who had the procedure;revious series quote figures up to 40% [19]. Other new
ests such as enzyme-linked immunosorbent assay foretection of galactomannan antigen are plagued by lowpecificity and sensitivity, especially in those receivingntifungal therapy, and an inability to diagnose IFIsaused by molds other than Aspergillus [16, 19], whereasolecular diagnostic tests such as polymerase chain
eaction appear promising but have not been extensivelyalidated as diagnostic tools [20].Recently one group described the success of CT-
uided biopsy in diagnosing invasive pulmonary fungalnfection with the specimen minced, homogenized, andentrifuged and then submitted to calcofluor white stain,alactomannan, and Aspergillus polymerase chain reac-ion testing, but this method requires further evaluation21]. Computed tomography-guided biopsy did not yielddiagnosis in the 5 patients in our series who underwent
his procedure, although sections from biopsies werexamined by standard histologic stains only (Grocottethenamine silver stain, hematoxylin and eosin, and
eriodic acid–Schiff). This may reflect only the prior usef antifungal medication and is not reflective of CT-uided biopsies on patients in whom surgery was notubsequently performed. However, given the poor diag-ostic yield with current standard histologic prepara-
ions, the benefits of surgical resection to provide diag-osis may be superior to CT-guided biopsy in patients
ith suitable lesions. t
Therapeutic surgery was the most common indicationor intervention in our series (22 of 25 patients). Completereedom from residual and recurrent fungal infection wasbtained in all patients who underwent a therapeuticesection. Three patients had a purely diagnostic proce-ure because of diffuse bilateral lung lesions considered
oo widespread to attempt complete resection. Patientsith diagnosed or suspected fungal masses had surgery
or eradication of infection before transplantation. Effica-ious treatment is particularly important when patientsre waiting for SCT transplantation. Patients diagnosedith IFI who are undergoing repeated cycles of chemo-
herapy or progressing to SCT are at risk of reactivationf the IFI [22]. Patients with fibrosis and obliterativeronchiolitis only can progress to early transplantation,nd those in whom a diagnosis of IFI is made can beanaged with appropriate antifungal therapy before
urther immunosuppression. Four patients during thetudy period had a diagnosis of infarction or fibrosis;hese patients were able to quickly progress to furtherhemotherapy and SCT required for their underlyingalignancy. Two other patients who were diagnosed to
ave IFI on histologic examination had their antifungalegimen changed to a more appropriate agent. One of theactors influencing recurrence of IFI after allogeneic SCTs duration of antifungal therapy before transplantation,nd a definitive diagnosis of IFI may aid in planningransplant strategies [23]. The rate of relapse and recur-ence of IFI after resection has also remained extremelyow in most series, making a strong case for early surgicalntervention in this group of patients and considerationf combined surgical and medical therapy [16].In a minority of patients with multiple areas of fungal
isease involving both lungs, medical management washe first line of treatment and, with time, serial CT scansevealed either the regression, stasis, or progression ofesions. Those lesions that have progressed can then beargeted for surgical resection. Other, more aggressiveroups achieve the same result with bilateral stagedesections or video-assisted thoracoscopic surgery on oneide and open resection on the other. Some groups haveerformed video-assisted thoracoscopic surgery resec-
ions with excellent results; however, there was a highate of conversion to thoracotomy and several limitationsf the technique: inadequate opening of staplers, diffi-ulty with pleural invasion, and resection for deeplyocated lesions [24].
Mortality and morbidity were major concerns in neu-ropenic patients who often had concurrent thrombocy-openia. Our mortality rates and morbidity rates haveeen comparable if not better than previous reports. Inur series, there was no surgery-related mortality within0 days. One later death, at 32 postoperative days, washe result of progression of systemic fungal infection.nother at 80 postoperative days was owing to empyemand bacterial sepsis; total mortality was 8% (n � 2). Majororbidity included one case of postoperative empyema,
nd there were no reexploration for bleeding. This con-rms the findings of several series published recently
hat have shown that lung resections, both open and
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1537Ann Thorac Surg THEODORE ET AL2009;87:1532–8 SURGERY FOR IFI
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inimally invasive, can be performed with extremely loworbidity and mortality [7, 12, 24]. Bleeding and infection
ates have been low despite the fact that many of theatients were neutropenic and thrombocytopenic at the
ime of surgery, and other complications in publishederies including prolonged air leaks, pleural aspergillo-is, prolonged ventilation, and recurrent pleural effusionsere not encountered [12, 16, 25].Although medical management with voriconazole and
mphotericin B remain the mainstay of therapy [5, 6, 10],urther evaluation of surgical therapy should be under-aken as the benefit of timely definitive diagnosis andnstigation of early alterations of treatment strategies canmprove outcomes in these patients. We also speculatehat if the lesion is large, penetration of antifungal
edication may not be adequate.The extent of resection is also a major consideration.e believe that if there is only one definitive focus of
nfection it is reasonable to do a wide wedge resection ofhe lesion. Tissue preservation is vital, and multipleedge resections are preferable to lobectomy or segmen-
ectomies if adequate clearance of disease can bechieved. We have performed three wedge resectionsrom the same lobe on one occasion and have been ableo preserve a significant amount of functioning lungissue. Open thoracotomy and palpation of the lungsemains an important part of the operation to minimizeissue loss and at the same time obtain an adequate
argin around the invasive mass.In conclusion, the benefits of surgery in cohorts such as
his are twofold. In the first instance it appears surgery ishe optimal modality for definitive diagnostic purposes.n addition, it seems there are therapeutic benefits forhese difficult to treat patients, especially when surgery iserformed in conjunction with maximal medical treat-ent and optimization of preoperative fitness. Mortality
nd morbidity were rarely surgical, and generally oc-urred secondary to the underlying hematologic diseaseith much less frequency than the reported mortality ofatients having medical therapy in isolation.The evidence in this paper is, however, limited by the
ature of case series design, and thus it is difficult to drawonclusions as to whether medical therapy alone is su-erior to the combination of medical and surgical inter-ention. Given the relatively small patient numbers andariability in the primary hematologic disorder, the loca-ion of invasive pulmonary aspergillosis disease, and theype of resection undertaken, it is also difficult to deter-
ine in which patients surgical intervention will benefithe most. What one can surmise though, is that perform-ng pulmonary resections in this extremely unwell sub-roup is feasible, with low operative morbidity andortality.
o grants or financial support were received in the preparationf this manuscript. We wish to thank Dr Suvitesh Luthra, MCh
CTVS), for his help with data collection.
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9. Jantunen E, Ruutu P, Piilonen A, Volin L, Parkkali T, RuutuT. Treatment and outcome of invasive Aspergillus infectionsin allogenic BMT recipients. Bone Marrow Transplant 2000;26:759–62.
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2. Grigg AP, Slavin MA. Minimizing the risk of recurrent or
orty-Sixth Annual Meeting
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plantation or further intensive chemotherapy. Transpl InfectDis 2008;10:3–12.
3. Martino R, Parody R, Fukuda T, et al. Impact of the intensityof the pretransplantation conditioning regimen in patientswith prior invasive aspergillosis undergoing allogeneic he-matopoietic stem cell transplantation: a retrospective surveyof the Infectious Diseases Working Party of the EuropeanGroup for Blood and Marrow Transplantation. Blood 2006;108:2928–36.
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ark your calendars for the Forty-Sixth Annual Meeting ofhe Society of Thoracic Surgeons (STS) to be held at thereater Fort Lauderdale-Broward County Conventionenter, Fort Lauderdale, Florida, from January 25–27, 2010.he meeting is open to all physicians, residents, fellows,ngineers, perfusionists, physician assistants, nurses, orther interested individuals. Meeting attendees will berovided with the latest scientific information for practicingardiothoracic surgeons. Attendees will benefit from tra-itional Abstract Presentations, as well as Surgical Fo-ums, Breakfast Sessions, Surgical Motion Pictures, and
et Lab sessions. Parallel sessions on Monday anduesday will focus on specific subspecialty interests.An advance program with a registration form, hotel
uest activities will be mailed to STS members this fall.onmembers may contact the Society’s secretary, Douglas. Wood, MD, to receive a copy of the advanced program;owever, detailed meeting information will be available on
he STS website at www.sts.org.
ouglas E. Wood, MDecretaryhe Society of Thoracic Surgeons33 N. Saint Clair St, Suite 2320hicago, IL 60611-3658elephone: (312) 202-5800ax: (312) 202-5801mail: [email protected]
ebsite: www.sts.org
Ann Thorac Surg 2009;87:1538 • 0003-4975/09/$36.00
