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Pulmonary complications following bone marrow transplantation

¹ Department of Clinical Radiology, Leeds General Infirmary, Great George Street, Leeds LS1 3EX and ² Department of Clinical Haematology, St. James's University Hospital, Beckett Street, Leeds LS9 7TF, UK

	Abstract

Top Abstract Introduction Time course of immune... Radiology of pulmonary... Neutropenic phase - before... Non-infectious pulmonary... Infectious pulmonary... Early phase - after... Late phase Conclusion References

 
Pulmonary complications account for significant morbidity and mortality in patients following bone marrow transplants (BMT). They are distinct from other immunosuppressed patients in that there is a predictable course of immunosuppresion and therefore of likely pulmonary complications. This is important when interpreting abnormal radiology as the predictable time course will enable narrowing the differential diagnoses to certain pulmonary complications that characteristically occur at a particular time following BMT. Early recognition and correct treatment of the pulmonary complications should minimize the significant mortality and morbidity. This review aims to discuss the role of radiology in the diagnosis and management of pulmonary complications following BMT.

	Introduction

Top Abstract Introduction Time course of immune... Radiology of pulmonary... Neutropenic phase - before... Non-infectious pulmonary... Infectious pulmonary... Early phase - after... Late phase Conclusion References

 
A successful programme of allogeneic transplantation to consolidate standard chemotherapy treatment of haematological malignancies was begun in the late 1960s. This allowed a very large (ablative) dose of chemotherapy and total body irradiation to be given to kill any remaining malignant cells. This high dose also inevitably killed the patients' own stem cells, but rescue from aplasia was then achieved by an infusion of stem cells in marrow collected from a healthy compatible donor. Variations on this technique are now the treatment of choice for haematological malignancies [1].

The finding that only one in four patients have a compatible sibling donor, led to the introduction of autologous transplantation. Here, after conventional treatment to achieve a remission, the patient's own marrow is harvested prior to ablative treatment and then used afterwards as rescue from ablation. This technique has a lower transplant related mortality because there is no graft versus host disease (GVHD), but there is a higher relapse rate because there is no graft versus leukaemia (GVL) effect. More recently, promising results have been obtained using non-ablative stem cell transplants, where the patient is immunosuppressed to allow the allogeneic graft to take, in the expectation that the GVL effect alone will cure the patient, without the need for damaging ablative treatment. Nowadays peripheral blood stem cells are often used rather than the stem cells from bone marrow transplantation (BMT).

Pulmonary complications account for significant morbidity and mortality in patients following BMT, occurring in 70% and are a factor in more than 30% of transplant related deaths [2, 3]. The risks of pulmonary complications depend on the underlying malignancy, the conditioning regimen employed, the type of BMT and the development of GVHD [4, 5].

Pulmonary complications directly related to BMT are divided into infectious and non-infectious groups. Other complications not involving the lung parenchyma such as pulmonary emboli will not be discussed further. BMT patients are distinct from other immunosuppressed patients in that there is a predictable time course of immunosuppression. This is important when interpreting abnormal radiology as the predictable time course will help to narrow the differential diagnoses to certain pulmonary complications that characteristically occur at a particular time following BMT (Table 1) [3, 6, 7]. Early diagnosis enabling treatment of the pulmonary complications helps minimize the significant mortality and morbidity.

	Time course of immune dysfunction following BMT

Top Abstract Introduction Time course of immune... Radiology of pulmonary... Neutropenic phase - before... Non-infectious pulmonary... Infectious pulmonary... Early phase - after... Late phase Conclusion References

 
Immunosuppression starts with the conditioning regimen such as chemotherapy and total body irradiation, usually becoming evident about 1 week before a standard BMT [8]. The onset of immunosuppression is variable depending on the type of conditioning regimen. Profound neutropenia occurs in all patients during the neutropenic phase following BMT. Neutrophils are the first to recover, usually within 2–4 weeks following BMT, but the lymphocyte count may take months to return to normal. Nearly all immune-functions are impaired during the first 4–5 months [8]. Both cell-mediated and humoral immune functions usually take 6–12 months to recover. In BMT patients without GVHD, the immunity will usually return to normal after 1 year following BMT [4].

The three important time periods following BMT can be divided into: the neutropenic phase; the early phase; and the late phase.

	Radiology of pulmonary complications following BMT

Top Abstract Introduction Time course of immune... Radiology of pulmonary... Neutropenic phase - before... Non-infectious pulmonary... Infectious pulmonary... Early phase - after... Late phase Conclusion References

 
Plain chest radiography remains the mainstay for diagnosis and assessing progression of pulmonary complications following BMT but high resolution CT (HRCT) has an increasingly important role [7]. In the presence of a normal chest radiograph, HRCT may demonstrate a significant pulmonary abnormality in 10% of immunosuppressed patients [9, 10]. However, with a normal HRCT, pulmonary disease is unlikely [11]. HRCT not only enables detection of pulmonary disease, but also helps narrow the differential diagnosis and guide further management. HRCT findings are invaluable in deciding the best technique to obtain a tissue diagnosis, either bronchoscopic or surgical biopsy and to guide the bronchoscopist or surgeon to sample the optimum site [12]. HRCT is also useful in monitoring response to treatment or detecting further complications.

	Neutropenic phase – before engraftment

Top Abstract Introduction Time course of immune... Radiology of pulmonary... Neutropenic phase - before... Non-infectious pulmonary... Infectious pulmonary... Early phase - after... Late phase Conclusion References

 
This phase during which there is a profound neutropenia occurs a week following BMT and extends for a period of 7 days to 30 days. Non-infectious causes contribute between 50% and 80% of the pulmonary complications and are most commonly pulmonary oedema, drug toxicity and diffuse alveolar haemorrhage (DAH) [8]. The combination of severe neutropenia and mucositis during this period also predisposes patients to infectious pulmonary complications, predominantly bacterial and fungal infections, notably aspergillosis [6].

	Non-infectious pulmonary complications

Top Abstract Introduction Time course of immune... Radiology of pulmonary... Neutropenic phase - before... Non-infectious pulmonary... Infectious pulmonary... Early phase - after... Late phase Conclusion References

 
Pulmonary oedema
This is a common early complication during this period, reported in up to 65% patients [2], due to infusion of large volumes of fluid combined with cardiac and renal impairment secondary to chemotherapy. In addition, radiotherapy, chemotherapy and septicaemia also lead to capillary membrane leakage resulting in non-cardiogenic oedema [3]. Chest radiographic findings are typical of pulmonary oedema with bilateral diffuse ground glass pulmonary opacities often accompanied by Kerley B lines. In contrast, cardiomegaly is generally absent [13].

HRCT findings include prominent pulmonary vessels, interlobular septal thickening, ground glass attenuation and pleural effusions [14]. Pulmonary oedema is almost always diagnosed clinically with chest radiography rather than with HRCT.

Drug toxicity
This is most frequently associated with chemotherapeutic agents such as bleomycin, methotrexate and busulfan. The addition of radiotherapy increases the risks of the pulmonary toxicity with a reported incidence in up to 30% cases [15]. Radiology findings are variable and non-specific. There are two main patterns of abnormality seen on HRCT. The most common pattern is hypersensitivity pneumonitis with bilateral non-specific ill-defined ground glass change and consolidation and nodular opacities with frequent involvement of the posterior segment of the lower lobes. The less common pattern seen is non-cardiogenic pulmonary oedema [15]. Pulmonary fibrosis may develop at a later stage [16].

Diffuse alveolar haemorrhage
DAH was initially seen in approximately 20% of autologous BMT [17], but is now uncommon. It has an associated mortality of up to 100% [4, 5]. The exact cause of DAH is unknown. However, it is likely to be multifactorial and some authors believe that it is due to influx of the neutrophils into the lung since the onset of DAH often coincides with the bone marrow engraftment period—7 to 21 days following BMT [2, 4]. It is important to exclude infection, but endothelial cell injury in the presence of thrombocytopenia probably underlies most cases.

Clinically, the patient presents with acute dyspnoea, non-productive cough, hypoxia and fever. Frank haemotypsis is uncommon and the clinical signs may be slight despite the rapid deterioration in radiographic appearances, which is a hallmark of the condition.

Chest radiographic findings are non-specific and include bilateral areas of diffuse ground glass and patchy consolidation, predominantly perihilar and in the lower lung zones and often rapidly deteriorate [18]. Bronchoalveolar lavage often shows a progressively bloodier return of the lavage fluid and haemosiderin laden macrophages [3].

	Infectious pulmonary complications

Top Abstract Introduction Time course of immune... Radiology of pulmonary... Neutropenic phase - before... Non-infectious pulmonary... Infectious pulmonary... Early phase - after... Late phase Conclusion References

 
Bacterial infections are common in the neutropenic phase with a reported incidence ranging from 20% to 50% [2]. Infections are most commonly caused by a variety of bacteria, but sputum culture is not usually helpful.

Bacteraemia is common and frequently caused by gram-negative bacteria from gastrointestinal tract and oral mucosa as a result of aspiration [6]. Fortunately, death from bacterial infections is unusual at this stage owing to the wide usage of broad-spectrum antibiotics [8].

Fungal infections are a common cause of pneumonia following BMT with a reported incidence of up to 70% [19]. The usage of particulate air filter masks and laminar airflow rooms has decreased the incidence of fungal infections [4]. The most common pathogen is Aspergillus, seen in about 10% of patients [8, 20]. In the immunocompromised, Aspergillus may be angioinvasive, invading blood vessels and causing haemorrhagic infarction or airway invasive causing tracheobronchitis, bronchiectasis or pneumonia, often these will overlap. The reported incidence of angioinvasive versus airway invasive aspergillosis is 70% and 30%, respectively [21, 22]. Candida is seen less frequently. Nocardia is occasionally isolated, especially in patients on corticosteroid therapy [23]. Fungal infections cause significant mortality of up to 90% and occur most frequently after allogeneic transplants.

Clinically, the patient may present with fever, dyspnoea, dry cough, pleuritic pain and sometimes haemotypsis, but early diagnosis before these features develop is important if treatment is to be successful. Amphotericin B, or liposomal amphotericin if there is renal impairment, are currently the most commonly used antifungal treatments [24].

Plain chest radiographic findings include combinations of ill-defined nodules or masses with or without cavitation and focal areas of consolidation (Figure 1a). In the early stages of infections, HRCT is more sensitive and specific than radiography [25]. On HRCT, early angioinvasive aspergillosis characteristically shows a nodule or mass surrounded by a halo of ground glass, known as the "CT halo sign" which represents haemorrhagic infarction around the consolidated fungal infection [25, 26]. However, the CT halo sign is also seen in other infections such as candidiasis (Figure 2b), Nocardia, herpes simplex virus and cytomegalovirus (CMV) pneumonia and also non-infectious conditions such as alveolar cell carcinoma, Wegener's granulomatosis and metastatic angiosarcoma [27] and therefore it is not absolutely diagnostic of angioinvasive aspergillosis. Pulmonary infarction causing segmental or subsegmental consolidation may also be seen. Cavitation of nodules appearing as an air-crescent sign on HRCT (Figure 1b) occurs during the recovery phase of the infection when the neutropenia is recovering. Cavitation generally occurs 2 weeks after the appearance of nodules, usually with a white blood cell count of more than 1000 mm^-3 and is considered to be a good prognostic sign [28, 29]. In 15–30% of patients with invasive aspergillosis, the fungus invades the airways. HRCT findings are of patchy peribronchial or peribronchiolar consolidation and patches of consolidation, centrilobular nodules less than 5 mm and occasionally tree-in-bud [21]. Bronchoscopy with lavage is more likely to be positive for organisms in patients with airway invasive aspergillosis than in those with angioinvasive aspergillosis. In our unit, we monitor patients with prolonged severe neutropenia following chemotherapy twice weekly for Aspergillus antigens to aid early diagnoses [30].

View larger version (56K): [in this window] [in a new window]   Figure 1. (a) Angioinvasive aspergillosis pneumonia diagnosed on bronchoscopy in a 22-year-old man with acute myeloid leukaemia and prolonged neutropenia following bone marrow transplantation. Chest radiograph shows a cavitating right upper lobe mass and left pleural effusion. (b) High resolution CT of the same patient at the time of 1a, shows an "air-crescent sign" due to cavitation of the pulmonary nodule. This occurred about 3 weeks after the appearance of the nodules and indicates that the neutropenia is recovering.

View larger version (99K): [in this window] [in a new window]   Figure 2. (a) 66-year-old man with acute myeloid leukaemia who had prolonged neutropenia following bone marrow transplantation. Chest radiograph shows multiple micronodules secondary to candida infection. (b) High resolution CT of the same patient shows multiple micronodules with surrounding ground glass (arrow), also known as the "CT halo sign" that represents haemorrhagic infarction around the consolidated fungal infection.

Other fungal infections such as Nocardia, Mucormycosis and Cryptococcus may occur following BMT. Usually they present with radiographic findings similar to those in Aspergillus infection. Nocardia may be more aggressive and should be considered when a nodule is seen to cross a fissure.

CMV and Pneumocystis carinii pneumonia (PCP) more frequently present in the early phase post BMT between 30 days and 100 days, but may occur earlier.

	Early phase – after engraftment

Top Abstract Introduction Time course of immune... Radiology of pulmonary... Neutropenic phase - before... Non-infectious pulmonary... Infectious pulmonary... Early phase - after... Late phase Conclusion References

 
This phase occurs between 30 days and 100 days following BMT. Immunosuppression is due to an underlying deficit of cellular and humoral mediated immunity and may be severe if there is GVHD requiring treatment with immuosuppressives. The gradual improvement of neutrophils leads to decreasing incidence of fungal infections but increasing viral infections, mostly CMV pneumonia. PCP is now less common since the introduction of PCP prophylaxis [6]. Herpes virus is common but usually limited to the mucocutaneous areas.

The most important non-infectious pulmonary complication is interstitial pneumonitis, also known as engraftment syndrome (ES). Pathologically, it represents a form of diffuse alveolar damage.

Infectious pulmonary complications
CMV infections occur in up to 70% of patients following BMT. CMV pneumonitis is an important pulmonary complication and occurs in up to 40% patients, often between 6 weeks and 12 weeks following BMT [7, 31]. It is of considerable clinical importance in all types of allogeneic BMT [31], and once pneumonitis has developed there is a mortality rate of about 85% [32].

The infection is normally caused by reactivation of the latent virus from the recipient or the donor during profound immunosuppression, but it can also be caused by infusion of CMV positive blood products if these are not screened. Donor and recipient are tested prior to allogeneic BMT and if either has a CMV titre >1:16 they have been previously exposed to CMV and there is a risk of reactivation after BMT. In this situation weekly PCR studies followed by pre-emptive (before the patient develops clinical signs of infection) treatment (if the copy numbers are high or rising) with Ganciclovir or Foscarnet improves survival [33]. If treatment is delayed until the patient presents clinically with shortness of breath, fever, non-productive cough and hypoxia or with pneumonitis, therapy is unlikely to be successful [3].

Plain radiographic findings include areas of diffuse ground glass change, and nodules, mainly in the mid and lower zones [34]. Mediastinal air can be associated with CMV oesophagitis (Figure 3) [35]. HRCT findings include multiple micronodules and associated areas of consolidation or ground glass attenuation (Figures 3, 4) [36].

View larger version (118K): [in this window] [in a new window]   Figure 3. High resolution CT in a patient with cytomegalovirus pneumonitis and oesophagitis, shows bilateral upper lobe ground glass changes with cavitation of the left upper lobe consolidation and air in the mediastinum.

View larger version (110K): [in this window] [in a new window]   Figure 4. Cytomegalovirus pneumonia in a 47-year-old man with chronic myeloid leukaemia following bone marrow transplantation. High resolution CT shows areas of consolidation in both lower lobes, patchy ground glass attenuation and multiple micronodules.

View larger version (109K): [in this window] [in a new window]   Figure 5. 65-year-old man with multiple myeloma and prolonged neutropenia. High resolution CT shows characteristic appearances of Pneumocystis carinii pneumonia: diffuse bilateral and symmetrical perihilar ground glass attenuation.

Clinically, the patient presents with skin rash, dyspnoea, fever, non-productive cough and hypoxaemia and may be treated with diuretics and steroids.

The chest radiographic findings include bilateral pleural effusions, transient pulmonary infiltrates and interstitial pulmonary oedema [39].

	Late phase

Top Abstract Introduction Time course of immune... Radiology of pulmonary... Neutropenic phase - before... Non-infectious pulmonary... Infectious pulmonary... Early phase - after... Late phase Conclusion References

 
This phase occurs after 100 days following BMT. The BMT patient's immune system usually recovers to normal by the end of 1 year. Most pulmonary complications are non-infectious. They include obliterative bronchiolitis, cryptogenic organizing pneumonia (COP), COP-like reactions and chronic GVHD [3, 6]. Open lung biopsy is often necessary to establish a definitive diagnosis.

Infectious pulmonary complications are uncommon during this period except in the presence of GVHD associated with Epstein Barr virus (EBV) infection. BMT patients with GVHD have impaired immune systems and this is further compromised with immune-suppressive therapy, predisposing them to bacterial and viral infections [3, 6].

Non-infectious complications
Obliterative bronchiolitis
Obliterative bronchiolitis occurs in up to 10% of patients, usually within 6 months to 12 months following BMT [2, 24]. It rarely occurs after autologous transplantation [2]. The pathogenesis is complex and probably multifactorial. Most cases are thought to be secondary to bronchial mucosal damage from GVHD with inflammation of the small airways and subsequent obliteration. It has a high mortality rate of about 40% [4]. Clinically, the patient develops a non-reversible airflow obstruction with increasing non-productive cough and dyspnoea or there may just be an asymptomatic deterioration in pulmonary function tests [2, 3]. Currently, there is no effective medical therapy.

Chest radiograph findings may be minimal or there may be signs of hyperinflation, recurrent pneumothoraces and occasional focal/diffuse opacities. HRCT shows bronchial dilatation, bronchial wall thickening, peripheral vascular pruning and mosaic lung attenuation with air trapping on expiratory scans (Figure 6) [7].

View larger version (138K): [in this window] [in a new window]   Figure 6. High resolution CT (HRCT) of a patient with systemic graft versus host disease (GVHD) HRCT shows mild bronchial dilatation, bronchial wall thickening, peripheral vascular pruning and areas of patchy lung attenuation with air trapping. Appearances suggest obliterative bronchiolitis in GVHD.

Chest radiography shows patchy consolidation in multiple lobes. HRCT characteristically demonstrates patchy consolidation particularly with a peribronchovascular and/or a peripheral distribution in immunocompetent patients. In immunocompromised patients following BMT, ground glass attenuation and nodules are a more frequent finding, usually more randomly distributed. The nodules generally have smooth, well-defined margins [7, 40]. Sometimes this nodular appearance may be related to COP-like reaction to an underlying infection or secondary to drug therapy [40].

Chronic GVHD
GVHD is a result of immune reaction of immunocompetent donor cells against immunocompetent host tissue and occurs in up to 50% of patients who survive longer than 6 months [3]. In most patients chronic GVHD follows acute GVHD. Patients with pulmonary GVHD may also have disease elsewhere, particularly in the skin, liver, gastrointestinal tract and sinuses. The pulmonary complications include infections, chronic aspiration, obliterative bronchiolitis and lymphoid interstitial pneumonia [3].

Other conditions occur rarely such as post-transplantation lymphoproliferative disorder associated with EBV infection including lymphoid hyperplasia and lymphoid interstitial pneumonia. Tumour recurrence such as leukaemia and lymphoma should also be considered.

	Conclusion

Top Abstract Introduction Time course of immune... Radiology of pulmonary... Neutropenic phase - before... Non-infectious pulmonary... Infectious pulmonary... Early phase - after... Late phase Conclusion References

 
Pulmonary complications are an important cause of mortality and morbidity after BMT and most of the pulmonary complications following BMT have a non-specific radiographic appearance. Timely HRCT has an increasingly important role for early diagnosis of aspergillus infection when treatment is likely to be helpful. HRCT increases detection of pulmonary abnormalities even in the presence of a normal chest radiograph and can help to narrow the differential diagnoses. It is valuable in directing further investigation, deciding if bronchoscopic biopsy or surgical biopsy is the most appropriate investigation and directing the bronchoscopist or surgeon to the best site for biopsy.

Radiology, both chest radiography and HRCT play a pivotal role. They should be interpreted together with the clinical information particularly in relation to the time following BMT, as this is important in helping to narrow the differential diagnoses. It is vital that all patients thought to have pulmonary complications following BMT are managed with a multidisciplinary team approach including haematologist, radiologist and chest physician.

Received for publication July 2, 2002. Revision received January 9, 2003. Accepted for publication March 10, 2003.

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Top Abstract Introduction Time course of immune... Radiology of pulmonary... Neutropenic phase - before... Non-infectious pulmonary... Infectious pulmonary... Early phase - after... Late phase Conclusion References

 

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