Diagnostic and Interventional Imaging (2013) 94, 193—201

CONTINUING EDUCATION PROGRAM: FOCUS

Infectious chest complications in haematologicalmalignancies

S. Bommarta,∗, A. Bourdinb, A. Makinsonc,G. Duranda, A. Micheaua, V. Monnin-Baresa,F. Kleina, H. Kovacsika

a Montpellier University Hospitals, Arnaud de Villeneuve Hospital, Medical Imaging, 371,avenue Doyen-Gaston-Giraud, 34295 Montpellier cedex 05, Franceb Montpellier University Hospitals, Arnaud de Villeneuve Hospital, Department of RespiratoryMedicine, 371, avenue Doyen-Gaston-Giraud, 34295 Montpellier cedex 05, Francec Montpellier University Hospitals, Gui de Chauliac Hospital, Department of Infectious andTropical Disease, 80, avenue Augustin-Fliche, 34295 Montpellier cedex 05, France

KEYWORDSChest;Haematologicaldisease;Infection;Aspergillosis;

Abstract The management of infections in haematology is dictated by the patient’s type ofacquired or induced immune deficiency (neutropenia, deficiency in cell-mediated or antibody-mediated immunity), and findings from clinical examination, laboratory studies, or morphologicinvestigations. The CT scan dominates in the initial management and follow-up of thesepatients, since clinical features very often appear to be non-specific. The radiologist’s roleis to guide the clinician towards a specific diagnosis such as aspergillosis or pneumocystosis, or

Immunodeficiency to point them towards a non-infectious cause: tumour localisation, hypervolaemia, bronchiolitisobliterans suggestive of GVH disease, drug toxicity, or embolism.

© 2012 Éditions françaises de radiologie. Published by Elsevier Masson SAS. All rights reserved.

Infectious complications are common in patients with haematological malignancies.They develop not only because of the immune deficiency that is intrinsic to haemato-logical disease, but also because of the treatments used that cause immunosuppressionor aplasia [1]. Around 50% of patients with a haematological malignancy will present

a pulmonary infection during their management [2]. These events carry a heavy bur-den of morbidity that requires broad-spectrum anti-infective chemotherapy. They arethe direct cause of almost 40% of deaths in this population. The prognosis corre-lates to how early diagnosis is made, meaning that quick access to cross-sectional

∗ Corresponding author.E-mail address: s-bommart@chu-montpellier.fr (S. Bommart).

2211-5684/$ — see front matter © 2012 Éditions françaises de radiologie. Published by Elsevier Masson SAS. All rights reserved.http://dx.doi.org/10.1016/j.diii.2012.12.002

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Aspergillosis and other mycoses

Many clinical entities connecting Aspergillus and the lunghave been described, and these correlate with the level

94

maging is required: a key factor in the management ofung disorders is investigating the possibility of, for exam-le, a fungal infection [3]. CT scanning has been shown toe superior to standard X-ray imaging for identifying local-sation and spread of lesions as well as for an assessmentf aetiology [4]. CT is currently recommended with evi-ence level A (one or more good quality meta-analyses orandomised clinical trials) when there is a suspicion of annfectious chest complication in a patient in haematologicalncology [5]. It is also essential for carrying out or guidingiopsies, whether this is done by endoscopy or percutaneouseedle biopsy. Microbiological diagnosis based on imagingeatures is of course only a signpost that will always haveesser sensitivity and specificity than the Gold Standard oficrobiology testing. Nonetheless, the type and duration of

mmune suppression, when combined with certain specificorphologic findings, can point predominantly to particu-

ar pathogens and considering these factors together canssist with the decision-making process. Lungs are commonlyot the only organs involved, and an associated infectiousr non-infectious disease should always be searched (seehapter of non infectious lesions).

rientation and predisposing factors

here are three main mechanisms causing immunodeficiencyn haematological oncology and these have recently beenetailed by Godet et al. [6]. The emergence of pathogensepends on whether the patient has a deficiency in the typef immunity that is usually involved in controlling them, i.e.ellular-mediated or antibody-mediated immunity [4].

Three patterns are distinguished:neutropenia, which is usually caused by treatment, eitherchemotherapy or radiotherapy. This encourages bacterialor fungal lung infections to develop;deficiencies in cell-mediated immunity (immunosuppress-ant treatments, long-term corticosteroid use; lympho-proliferative diseases, bone marrow transplant). Theseencourage infections of intracellular bacteria, mycobac-teria, viruses (Herpes virus), fungi (pneumocystosis), andparasites (toxoplasmosis);deficiencies in antibody-mediated immunity (splenec-tomy, hypo/ergammaglobulinemia and myeloma). Theyare usually associated with infections of Streptococcuspneumoniae or Streptococcus haemophilus.

nvestigation technique

he chest CT scan can initially be carried out without inject-ng a contrast media. It will be carried out with contrastnhancement if there is a suspicion of pulmonary embolismr if the abdomen and pelvis are also to be examined. Whereronchiolitis is suspected, investigations are completed byaking expiration cross-sections using low-dose volume CT,r with four sequential staggered cross-sections. They can

e acquired during breath hold in maximum expiration oruring expiration (‘‘breathe, breathe, breathe’’) [7]. Tocquire a good quality expiration CT the patient needs toctively participate, as does the technician, so that the

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S. Bommart et al.

equired functional information to characterise the distalirways is captured.

MRI is not currently indicated in this context.

maging findings suggestive of infection

acterial infections

acteria remain the most common infective agent caus-ng lung disorders, or at least they are the pathogens thatre most often identified on microbiology. These infectionshould routinely be treated with broad-spectrum antibioticsargeting staphylococci and Gram-negative bacteria [8].acterial infections are usually non-specific, the radiologicalndings being an opacity or an uniform alveolar consolida-ion with air bronchogram (Fig. 1). This can be segmental,obar, or spread across several lobes [9]. The descriptionf the imaging features will attempt to define the spreadnd the associated abnormalities: underlying parenchyma orleural effusion. Mediastinal lymphadenopathy can be foundt the lymph nodes into which the infectious process is drain-ng. More diffuse lymphadenopathy may present when theres tumour proliferation.

In general, the infection frequently gains entry via aentral line catheter (Port a Cath, PICC line) [10]. Oftenlood cultures or bacteriology tests using specimens fromhe end of the catheter are used to check for infection afteremoval. In this specific case, the purpose of imaging is tossess the spread of septic localisations. The chest CT scans especially useful for demonstrating relatively cavitatedormations in the parenchyma that point to haematogenousissemination of bacteria (or sometimes fungus). An assess-ent of the heart chambers forms part of the assessment

f the spread of sepsis and this will look for thrombi of thealves pointing to associated endocarditis [11].

igure 1. Forty-one-year-old male. Pneumonia revealing M1 sub-ype acute myeloid leukaemia treated with empirical antibioticherapy with good progression (a, b).

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Figure 3. Forty-seven-year-old female managed for acute lym-phoblastic leukaemia. Severe sepsis following second cycle ofinduction chemotherapy. Diagnosis of invasive aspergillosis madeatc

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Infectious chest complications in haematological malignanci

of immune dysfunction that allowed them to develop:invasive aspergillosis, semi-invasive aspergillosis, chronicnecrotising aspergillosis, aspergillus bronchitis, and finallyallergic bronchopulmonary aspergillosis, which occupies theextreme end of this immunological and clinical spectrum.Aggressive opportunistic fungal infections can develop inpatients who present neutropenia persisting beyond 1 week[12,13].

Invasive pulmonary aspergillosis (IPA) is at the forefrontof these infections and it entails between 50 and 90%mortality. It complicates around 10% of allogeneic bone mar-row transplants and induction cycles in acute leukaemia.This diagnosis is considered in the haematological oncologypatients when they present severe infection that remainsresistant to broad-spectrum antibiotics for 4 days or more.Aspergillus is a ubiquitous fungus and contamination isairborne, through the inhalation of spores. When the cir-cumstances are favourable it can cause groups of cases.Aspergillus fumigatus is the most commonly found pathogenbut other agents can produce similar pictures: zygomyco-sis [14], candidiasis (Fig. 2a and b). Imaging, and CT inparticular, demonstrates non-specific pneumonia-like alve-olar consolidation in fungal infections. One or more nodularlesions surrounded by a ‘‘ground glass’’ halo may point morespecifically to this type of agent (Figs. 3 and 4). The groundglass opacity in this case relates to the presence of haemo-rrhagic areas peripheral to the central infarction. The halosign is highly suspicious in this context, even though it hasbeen demonstrated that this sign can also be seen in otherinfections (viruses, mycobacteria), inflammatory patholo-gies (Wegener’s granulomatosis), and tumours (metastases,lepidic growth pattern adenocarcinoma, Kaposi’s sarcoma)[15]. A reversed halo sign is, however, thought to be moresuggestive of zygomycosis. The progression of CT features ismarked by central necrosis and then retraction which thengives way to the air crescent sign (Fig. 5), and this usually

coincides clinically with recovery from neutropenia [16]. Asa general rule, the presence of well-delineated consolida-tion together with either a peripheral halo, an air crescent,or cavitation are the signs that point to probable IPA based

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Figure 2. a,b: 56-year old female with respiratory decompensation witwith central necrosis due to Candida tropicalis.

fter transthoracic needle biopsy. Indication for right upper lobec-omy upheld when patient recovers from aplasia taking vascularonnections into account.

n the current medical algorithms for the management ofebrile patients with neutropenia [17].

Apart from guiding diagnosis, the role of the radiologist iso describe the relationships between these formations andhe major vessels. This is because surgery may be indicatedf localisations are found close to vascular structures, in viewf the risk of massive haemoptysis.

Aspergillosis can readily affect the tracheobronchialree, which translates into a thickening of the walls, debrislling the bronchi, or non-specific centrilobular opacities.his presentation occurs more easily in less severe forms of

mmunodeficiency [18].

neumocystosis

neumocystis jiroverci infection (formerly Pneumocys-is carinii) is also a fungal infection due to recent

hin a relapse of M4 subtype acute myeloid leukaemia. Lung disease

196 S. Bommart et al.

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Figure 6. Repeat episode of fever two years after initial diag-nosis. Ground glass opacities predominantly in the upper zones.P

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igure 4. Invasive aspergillosis, multiple nodule form.

eclassification. A pneumocystosis infection in a patient liv-ng with HIV allows diagnosis of AIDS. It is however notpecific to this kind of acquired immune deficiency and itan been seen irrespective of the cause of immune sup-ression, with a predilection for post-allogeneic transplantatients [19]. Imaging in pneumocystosis is highly distinctrom that seen in other fungal infections. Indeed, the findingf extensive ‘‘ground glass’’ opacities predominating in thepper zones is highly suggestive of pneumocystosis in thisetting (Fig. 6). Other features classically associated withIV (cystic lesions, crazy-paving sign) are less often found

n haematological disease. These signs can be present wheniagnosis has been delayed due to a subacute disease course20].

iral lung disease

iral lung diseases caused by Herpes, cytomegalovirus oraricella-zoster virus (VZV) are usually conditions that are

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igure 5. Air crescent sign during a progressing invasive aspergillosis.

neumocystosis (same patient as figure 1).

eactivated due to immune deficiency. Lung infections areresented as ‘‘ground glass’’ or reticular opacities (Fig. 7)21,22]. Alveolar consolidation or nodules are possible [22].he development of a cough during an epidemic combinedith findings of bronchial origin or ground glass opacities onT points to a community-acquired virus.

uberculosis and atypical mycobacteria

hen cell-mediated immunity is affected, this can cause aeactivation of tuberculosis that may be isolated or asso-iated with other pathogens. Signs of this diagnosis areonsolidation in the upper zones with nodular opacitiesssociated with endobronchial spread (Fig. 8). Disseminatedmilliary) forms occur most commonly when the patient has

severe immune deficiency. In these cases, multiple regularodules distributed haematogenically may be observed.

Infectious chest complications in haematological malignancies

Figure 7. Lung disease with hypoxaemia in a 56-year old femalebeing monitored for lymphoma. Predominantly diffuse patternground glass opacities: CMV lung infection.

Figure 8. B-lymphoma treated with CHOP in a 43-year old male.Alveolar consolidation has developed that is related to a site ofhypermetabolism seen in the parenchyma on PET: atypical mycobac-teria.

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Figure 9. a,b: persistent alveolar consolidation with air bronchogram

197

on-infectious lesions of the parenchyma

he non-infectious causes of parenchymal or vascularnvolvement can be presented on top of the signs of infec-ion. A routine search should be made for them so that aisease that can be cured using methods other than antibi-tics is not misdiagnosed.

ulmonary oedema

prescription of pre-treatment hyperhydration or the usef cardiotoxic chemotherapy such as anthracyclines can behe cause of pulmonary oedema. It is rarely difficult toiagnose clinically, although symptoms during the inter-titial oedema stage of decompensated left heart failurean be more non-specific. If thickening of the perilobularepta is present, and all the more so if this is combinedith pleural effusion, and even quite commonly mediasti-al lymphadenopathy, this diagnosis must be considered,specially when it accompanies tangible signs of lungisease.

arenchymal tumour localisations

ymphomas can be present in the form of single or mul-iple areas of parenchymal consolidation and images maye misunderstood to be suggestive of an infectious cause.his finding is very typical in MALT lymphomas (Fig. 9a and).

pecific case of pulmonary infiltration by leukemiclast cellshe finding of diffuse ground glass opacities togetherith acute dyspnoea can be explained by a build-upf circulating blast cells in the arterioles (pulmonaryeukostasis), usually seen in acute myeloid leukaemia.

his phenomenon is generally accompanied by multiplergan presentations and patients often make poor progress.linical signs and laboratory studies back up this diagno-is.

in a 79-year old male: non-Hodgkins lymphoma, MALT subtype.

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stem cell transplant recipients will present respiratory signsof rejection (Graft Versus Host Disease [GVHD]). Bronchi-olitis obliterans is one way in which it may be identified.

98

Infiltration of leukemic cells develops in the same set-ing but it can be distinguished because in this case tumourells localise to the interstitium, which explains why someresentations mimic pulmonary oedema or appear to be lym-hangitis [23,24].

rug or radiation-induced lung disease

he presence of ground glass opacities with straight edgesn the irradiated field that do not respect the pleural fis-ures, appearing during radiotherapy or in the following sixonths, is suggestive of acute radiation-induced lung dis-

ase.Furthermore, there are many treatments used in haema-

ological oncology that can cause an immune responseeading to hypersensitivity reaction lung disease. The pre-entation can be extremely variable but shows involvementf the interstitium. The most classically seen forms arerouped together by drug on the website Pneumotoxhttp://www.pneumotox.com).

The purpose of multidisciplinary consultation is toxclude other diagnoses, to confirm the chronology of theatient’s treatments in order to establish which one theesponse may be attributed to using extrinsic information,nd possibly to suggest other investigations for diagnosis.

lveolar haemorrhage

cquired or induced thrombocytopenia can predisposeatients to alveolar haemorrhage. The filling of the alve-lar space appears on imaging as ground glass opacities,ometimes combined with a reticular pattern (crazy-paving)25]. The patient does not always expectorate blood (around5% of cases) but when this clinical sign is present, it isnother argument in favour of this diagnosis. If there isny doubt, fiberoptic bronchoalveolar lavage can confirmiagnosis. Alveolar haemorrhage can also complicate numer-us other clinical settings (paraneoplastic syndrome, drugreatments, viral lung diseases etc.), principally pulmonaryedema, which is discussed above.

ulmonary alveolar proteinosis

ulmonary alveolar proteinosis or alveolar lipoproteinosisan be idiopathic or secondary to a haematological malig-ancy. It characteristically affects the interstitium, showinground glass opacities combined with infralobular and per-lobular reticular patterning (crazy-paving) (Fig. 10). Theiagnosis is confirmed if milky fluid is collected on bron-hoalveolar lavage [26,27].

ulmonary embolism

ith risk factors such as hyperviscosity syndrome, confine-

ent to bed, and a malignant tumour occurring together,

hromboembolic diseases become a common event in theanagement of haematological malignancies [28]. If aatient presents dyspnoea that has developed recentlyhen the possibility of this diagnosis should be investi-ated.

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eticular pattern together forming the crazy-paving sign: secondaryulmonary alveolar proteinosis.

ronchiolitis

ronchiolitis obliterans with organising pneumonia (BOOP, name which has been replaced by cryptogenic organiz-ng pneumonia or COP in idiopathic cases) is a differentialiagnosis identified by pathological and anatomical findingsf subpleural alveolar consolidation that sometimes punc-uates the course of a haematological malignancy (Fig. 11).he aetiopathogenesis remains complex given that therere a multitude of factors that are potentially implicateddrug and physical treatments, underlying haematologicalisease, autoimmune response etc.).

Furthermore, 10 to 15% of allogeneic haematopoietic

igure 11. Fifty-eight-year-old female monitored for chronicymphocytic leukaemia for 13 years. Invasive aspergillosis diagnosednd treated 3 years ago. Signs of recurrence in the alveoli. Trans-ronchial biopsy confirmed bronchiolitis obliterans, which resolvedn corticosteroid therapy.

Infectious chest complications in haematological malignancies 199

being

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Figure 12. a—d: air trapping in a 34-year old male with dyspnoea

bronchiolitis obliterans due to GVHD.

This presents as dyspnoea and signs of obstructive dis-ease on PFT. CT demonstrates mosaic lung attenuationthat is more pronounced on images taken on expiration

(Fig. 12) [29—31]. These presentations are very often asso-ciated with a series of non-respiratory symptoms linkedto the rejection, mainly erythroderma and gastrointestinaldisorders.

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monitored for acute myeloid leukaemia and allogeneic transplant:

onclusion

hest infections are a common and serious complication in

aematological oncology. The interpretation of CT findings,onsidered together with the setting, assists in therapeuticanagement by pointing towards a microbiological cause or

o an intercurrent non-infectious pathology (Fig. 13).

200 S. Bommart et al.

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igure 13. CT signs and the diagnoses they point to.

isclosure of interest

he authors declare that they have no conflicts of interestoncerning this article.

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