Infection post transplant Central nervous system aspergillosis in allogeneic stem cell transplant recipients
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1 (2003) 31, & 2003 Nature Publishing Group All rights reserved /03 $ Infection post transplant Central nervous system aspergillosis in allogeneic stem cell transplant recipients E Jantunen 1,2, L Volin 1, O Salonen 3, A Piilonen 3, T Parkkali 1, V-J Anttila 1, A Paetau 4 and T Ruutu 1 1 Department of Medicine, Helsinki University Central Hospital, Helsinki, Finland; 2 Department of Medicine, Kuopio University Hospital, Kuopio, Finland; 3 Department of Radiology, Helsinki University Central Hospital, Helsinki, Finland; and 4 Department of Pathology, Helsinki University Central Hospital, Helsinki, Finland Summary: Invasive aspergillosis (IA) is relatively common in allogeneic stem cell transplant (SCT) recipients. Although lungs are the most common site, central nervous system (CNS) involvement is also observed in this setting. We have retrospectively studied 14 cases of CNS aspergillosis found in a cohort of 455 allogeneic SCT recipients (incidence 3%). All patients, except one, had experienced acute graft-versus-host disease treated with high-dose methylprednisolone, and eight patients (57%) had also received ATG. The median time to the diagnosis of CNS aspergillosis was 124 days (range days) from SCT. Pulmonary aspergillosis had been diagnosed earlier in four patients (29%). The most common initial symptoms of CNS aspergillosis were convulsions, hemiparesis, and mental alteration. Neuroradiological studies revealed single (two patients) or multiple (seven patients) focal lesions of cm in diameter. Despite clinical suspicion in many patients, a confirmed diagnosis of CNS aspergillosis was made during life in only one patient. A total of 12 patients (86%) received amphotericin B. Despite therapy, all patients died 0 27 days (median seven days) after the initial CNS symptoms. CNS aspergillosis is not uncommon in allogeneic SCT recipients. Clinical manifestations are usually dramatic and progress quickly. Earlier and more effective treatment of IA is needed to prevent dissemination of infection into the CNS. (2003) 31, doi: /sj.bmt Keywords: aspergillosis; central nervous system; allogeneic stem cell transplantation; radiology Invasive aspergillosis (IA) is a frequent clinical problem in allogeneic stem cell transplant (SCT) recipients with an incidence of 4 10%. 1 4 The prognosis of IA is very poor. 5,6 Lungs are the most common site of aspergillosis and are affected in about 90% of patients. 7 Central nervous system (CNS) involvement is also common in allogeneic SCT Correspondence: Dr E Jantunen, Department of Medicine, Kuopio University Hospital, PO Box 1777, Kuopio, Finland Received 31 May 2002; accepted 14 September 2002 recipients. Previous studies have indicated that CNS aspergillosis may be found in 40 50% of patients with IA. 2,8 Although several reports on CNS aspergillosis have been published, 9 13 most of them include few allogeneic SCT recipients We have therefore retrospectively analysed the incidence as well as clinical, radiological, and neuropathological findings of CNS aspergillosis among 455 consecutive allogeneic SCT recipients transplanted during a period of 12 years. Patients and data collection A total of 455 adult patients received allogeneic SCT at the Department of Medicine, Helsinki University Central Hospital during All patient records were retrospectively evaluated to find cases of possible CNS aspergillosis. Autopsy records were also reviewed. In addition to the demographics of patients with CNS aspergillosis, the time from SCT to diagnosis of CNS aspergillosis was also recorded. The occurrence and treatment of graft-versus-host disease (GVHD) were considered in all patients. Further, symptoms suggesting a CNS infection were sought from the patient records. Laboratory data collected included studies on the cerebrospinal fluid (CSF). All neuroradiological studies including computerized tomography (CT) and magnetic resonance imaging (MRI) were reviewed by two radiologists (one of them a neuroradiologist). Neuropathological autopsy records were available for all patients. Results Of the 455 allogeneic SCT recipients, 14 had CNS aspergillosis (incidence 3%). Patient characteristics are summarized in Table 1. Median time to the diagnosis was 124 days (range days) from SCT. In four patients (29%), the diagnosis of definite or probable invasive pulmonary aspergillosis had been made 9 91 days earlier. Initially, all patients engrafted, but 11 (79%) were neutropenic at the time of diagnosis. All patients, except one, had experienced acute GVHD prior to the diagnosis of CNS aspergillosis. In all, 13 patients (93%) had been treated with high-dose methylprednisolone (MP), and eight
2 192 Table 1 Characteristics of 14 patients with CNS aspergillosis after allogeneic stem cell transplantation Gender Female 8 Male 6 Age (years), median (range) 45 (17 61) Disease AML 5 CML 4 ALL 3 MDS 2 Donor Sibling 9 Unrelated 5 Table 2 Neurological symptoms and signs in 14 patients with CNS aspergillosis Symptom/sign No. of patients Convulsions 3 followed by hemiparesis 1 Hemiplegia/hemiparesis 2 Mental alteration 4 followed by hemiparesis and convulsions 3 Ophthalmoplegia and hemiparesis 1 Loss of consciousness 1 Figure 1 A 50-year-old patient with CNS aspergillosis. Axial MR image (T2-weighted FLAIR sequence) shows multiple hyperintense lesions. (57%) had also received ATG. The median dose of MP at the time of diagnosis was 1 mg/kg/day ( mg/kg/day). Clinical and laboratory findings Nine patients (64%) were febrile. The most common initial neurological symptoms were convulsions, hemiparesis, and mental alteration (Table 2). Neurological symptoms usually progressed quickly. Median time from the initial CNS symptoms to the diagnosis or to death was 7 days (0 27 days). CSF was examined in five patients. The most common finding was a moderate increase in the protein concentration. In one patient Candida albicans grew from CSF, and in another patient a minute amount of mould was seen on microscopy of the CSF. No antigen or PCR tests were performed on CSF in any of these patients. Neuroradiological findings Neuroradiological studies (CT, MRI) had been performed because of neurological symptoms in nine patients (64%) within a month prior to the diagnosis of CNS aspergillosis. In eight patients at least one CT examination was done. Three of the studies were nonenhanced and five were performed with a contrast medium. All MRI examinations included gadolinium-enhanced images. On the first study, two out of nine patients had only one lesion; all the others had multiple CNS lesions (Figure 1). The maximum diameter of the lesions ranged from 0.2 to 9 cm. No enhancement was observed in five patients who underwent CT examination with contrast medium. A faint ring-like gadolinium-enhancement was observed around most lesions in MRI (Figure 2). One patient had a large haemorrhagic lesion (Figure 3); in four other patients smaller haemorrhagic areas could be seen in some lesions. The findings are summarized in Table 3. Treatment and outcome Nine patients (64%) received systemic amphotericin B at the time of the first neurological symptoms or the presumptive diagnosis of CNS aspergillosis. Altogether, 12 patients (86%) received amphotericin B therapy for proven or suspected aspergillosis. No treatment responses were observed, and the neurological symptoms usually progressed within a few days. The median survival was only 7 days (range 0 27 days) from the onset of the neurological symptoms or signs. Autopsy findings All patients underwent autopsy, which confirmed the diagnosis of CNS aspergillosis in each patient including the patient in whom neurosurgical biopsy had shown aspergillosis in the temporal lobe 10 days prior to death. The most common macroscopic findings were focal necrotic lesions. In two patients, a major cerebral haemorrhage was observed in association with aspergillosis. In one patient, Candida infection was observed in the
3 193 Figure 2 A 45-year-old patient with CNS aspergillosis. Axial T1- weighted postcontrast MR image shows lesions with hypointensity cores and minimally enhancing rims in both frontal lobes. Figure 3 A 46-year-old patient with CNS aspergillosis. CT scan shows diffuse bleeding in right temporoparietal region. Table 3 Neuroradiological findings in nine patients with CNS aspergillosis after allogeneic stem cell transplantation Patient/symptom CT MRI F61 convulsions C /+, normal (day+1 a ) Small lesions (0.5, 1 cm) in both occipital lobes (day+6) M56 hemiparesis, mental alteration C /+, 2 cm lesion in the right internal capsule corresponding to CT (day+7) (day 0) F50 ophthalmoplegia, hemiparesis C, corresponding to MRI (day+3) >20 cerebral lesions, three cerebellar lesions, one in mecencephalon and one in pons (day+1) M45 mental alteration C /+, right frontal 1 cm lesion (day+1) The same lesion, now 6.5 cm in diameter (day+11) F45 mental alteration ND Seven supratentorial lesions, two biggest 5.5 cm in diameter, haemorrhage (day+1) F41 mental alteration, convulsions, C /+, three supratentorial lesions, biggest Corresponding to CT (day+12) hemiparesis 4.5 cm (day+11) F31 convulsions, hemiparesis C, corresponds to MRI (day+2) Ten supratentorial lesions (day+1) F46 hemiplegia C /+, large intracranial haematoma (9 cm) in ND the right temporoparietal region with oedema and midline shift (day 0) M46 hemiparesis C, five lesions in basal ganglia (biggest 2 cm) (day 0) ND a No. of days from initial neurological symptoms. F, female; M, male; CT, computerized tomography; MRI, magnetic resonance imaging; ND, not done, C no contrast medium; C+ with contrast medium. meninges (diagnosed by culture of the CSF 11 days earlier), in addition to focal necrotic lesions caused by Aspergillus in both hemispheres. In addition to necrosis and haemorrhage, microscopy revealed fungal invasion and thrombus formation in vessels nourishing the areas of focal lesions (Figure 4). Fungal septate hyphae, typical for moulds, were observed in all cases. The Aspergillus species could be cultured in eight patients (Aspergillus fumigatus in all). Isolated CNS aspergillosis was not observed in this material. Besides CNS, aspergillosis was observed in the lungs (12 patients, 86%), kidneys (four patients, 29%), liver (three patients, 21%), heart (three patients 21%), and gut (two patients, 14%). The involvement of the spleen, the
4 194 Figure 4 A small white-matter blood vessel with angioinvasive branched hyphae (5 mm wide) in the vessel wall. The lumen of the vessel is partially occluded by mural thrombosis caused by invasive Aspergillus infection. Autopsy specimen from the brain, paraffin section, Gomori methenamine silver (GMS) staining, magnification 220. thyroid gland and the adrenal gland was found in one patient (7%) each. CNS aspergillosis as a cause of death Altogether, 168 out of 455 SCT recipients (37%) died within a year after SCT. Therefore, the minimum figure for deaths because of CNS aspergillosis was 8% in this material. Discussion The present retrospective study is one of the largest series of allogeneic SCT recipients with CNS aspergillosis. A strong association with GVHD, dramatic clinical presentation, and relentless progression despite therapy were the major observations. They differ, at least in part, from the features seen in less immunocompromised patients with CNS aspergillosis. CNS aspergillosis has been considered a rare disease. This is certainly the case in patients who have undergone autologous SCT or who have received chemotherapy for leukaemia or other cancers. A retrospective Italian study showed that CNS involvement was observed in only 14% of patients with acute leukaemia and IA. 12 However, a previous report of Saugier-Veber et al, 2 suggested CNS involvement in up to 40% of allogeneic SCT recipients with IA. We observed CNS involvement in about half of our patients with IA (14/33) during the study period, but this is likely to be an underestimation, as not all patients who were diagnosed with IA during life and subsequently died were autopsied. The present study yielded an incidence of 3% of CNS aspergillosis in a cohort of allogenic SCT recipients during a 12-year period. A similar incidence has recently been reported by de Medeiros et al 18. Coley et al 15 observed an incidence of 1.2%. In an autopsy series, an incidence of 5% was reported; 490% of the patients were allogeneic transplant recipients. 19 By contrast, Graus et al 20 and Maschke et al 16 found no CNS aspergillosis in autologous SCT recipients. Clinical features were usually dramatic, consisting of mental alteration, convulsions, and hemiparesis. The clinical features observed were similar to those in the series by Hagensee et al, 21 where altered mental status was observed in 52% of the patients and hemiplegia and seizures in 33 and 30% of the patients, respectively. Although these clinical signs, as such, are nonspecific, in high-risk patients they are suggestive of an intracranial process and an indication for neuroradiological studies. The diagnosis of invasive aspergillosis is difficult, and this is certainly also the case with CNS aspergillosis. Examination of CSF usually gives a low diagnostic yield, which was also observed in some of the present patients. However, CSF examination is useful for differential diagnosis of other pathogens or CNS involvement with malignant cells. Recently, detection of Aspergillus antigen or DNA in CSF has been suggested to be useful in the diagnosis of CNS aspergillosis. 22 A definitive diagnosis of CNS aspergillosis requires histopathological samples, that can be obtained only by neurosurgery. These procedures are often not practical in this setting and may unnecessarily delay the start of therapy. In allogeneic SCT recipients, CNS aspergillosis is almost always associated with pulmonary disease, 21 which was also confirmed in this study. Thus, patients with previously suspected pulmonary aspergillosis who develop neurological symptoms or signs should initially be treated as having CNS aspergillosis.
5 Neuroradiological studies are helpful in the diagnosis of CNS infections in transplant recipients. Both CT and MRI are useful, but MRI may be more accurate and reveal more lesions than CT. 14 MRI and CT appearances of CNS aspergillosis have been studied in detail by several investigators. 11,13,14,17,23 Neuroradiological findings may be of use in the differential diagnosis of CNS infections. 15,16 Of other pathogens, Candida or other fungi, Toxoplasma gondii and also bacteria should be taken into consideration. 16,18,21,24 The treatment of invasive aspergillosis has proved disappointing in allogeneic SCT recipients. 5,6,25,26 Although the response rate in patients with pulmonary disease has been only 10 30%, the prognosis is even worse in patients with CNS involvement. In our series the median survival was only 7 days after the first symptoms, which is comparable to other reports. 14,21 However, some promising case reports have been published suggesting that the therapy may be effective in some patients with acute leukaemia 27,28 or even in allogeneic SCT recipients. 29,30 Amphotericin B, the standard therapy for aspergillosis, as well as itraconazole both have poor penetrance into the CNS Voriconazole has better penetrance 28 and may thus become the therapy of choice in patients with CNS aspergillosis. Recently, voriconazole has been found superior to amphotericin B in the primary treatment of invasive aspergillosis. 34 Another study suggested a partial response or stable disease in 42% of the patients with CNS aspergillosis treated with voriconazole, 35 but only a minority of the patients were allogeneic SCT recipients. Given the currently poor prognosis of CNS aspergillosis, combination chemotherapy might also be worth trying. In vitro studies as well as animal models have suggested additive or synergistic effects of caspofungin and voriconazole against Aspergillus sp. 36,37 However, the diagnosis of CNS aspergillosis is often delayed, the clinical situation is usually complex with severe immunosuppression and efficacy of current therapies is suboptimal. Therefore, treatment results are hard to improve in this patient population. Owing to the often multifocal nature of the CNS infection, surgery is not usually useful in this setting. To conclude, CNS aspergillosis is fairly common in allogeneic SCT recipients and is usually associated with pulmonary aspergillosis. The clinical presentation is often dramatic and the prognosis is dismal. More effective modes of treatment for IA are needed to prevent dissemination of the infection into the CNS. Acknowledgements This study was financially supported by Blood Disease Research Foundation of Finland. References 1 McWhinney PHM, Kibbler CC, Hamon MD et al. 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MRI of cerebral aspergillosis in patients who have had bone marrow transplantation. Am J Neuroradiol 1995; 16: Coley SC, Jäger HR, Szydlo RM, Goldman JM. CT and MRI manifestations of central nervous system infection following bone marrow transplantation. Clin Radiol 1999; 54: Maschke M, Dietrich U, Prumbaum M et al. Opportunistic CNS infection after bone marrow transplantation. Bone Marrow Transplant 1999; 23: Dietrich U, Hettman M, Maschke M et al. Cerebral aspergillosis: comparison of radiological and neuropathologic findings in patients with bone marrow transplantation. Eur Radiol 2001; 11: de Medeiros BC, de Medeiros CR, Werner B et al. Central nervous system infections following bone marrow transplantation. J Hematother Stem Cell Res 2000; 9: Mohrman R, Mah V, Vinters HV. Neuropathologic findings after bone marrow transplantation: an autopsy study. Hum Pathol 1990; 21: Graus F, Saiz A, Sierra J et al. Neurologic complications of autologous and allogeneic bone marrow transplantation in patients with leukaemia: a comparative study. Neurology 1996; 46: Hagensee ME, Bauvens JE, Kjos B, Bowden RA. Brain abscess following marrow transplantation: experience at the Fred Hutchinson Cancer Research Center, Clin Infect Dis 1994; 19:
6 Kami M, Ogawa S, Kanda Y et al. Early diagnosis of central nervous system aspergillosis using polymerase chain reaction, latex agglutination test and enzyme-linked immunosorbent assay. Br J Haematol 1999; 106: Yuh WT, Nguyen HD, Gao F et al. Brain parenchymal infection in bone marrow transplant patients: CT and MRI findings. Am J Roentgenol 1994; 162: Bleggi-Torres LF, de Medeiros BC, Werner B et al. Neuropathological findings after bone marrow transplantation: an autopsy study of 180 cases. Bone Marrow Transplant 2000; 25: Denning DW. Therapeutic outcome of invasive aspergillosis. Clin Infect Dis 1996; 23: Patterson TF, Kirkpatrick WR, White M et al. for the I3 Aspergillus Study Group. Invasive aspergillosis. Disease spectrum, treatment practices and outcomes. Medicine 2000; 79: Coleman JM, Hogg GG, Rosenfeld JV, Waters KD. Invasive central nervous system aspergillosis: cure with liposomal amphotericin B, itraconazole, and radical surgery: case report and review of the literature. Neurosurgery 1995; 36: Schwartz S, Milatovic D, Thiel E. Successful treatment of cerebral aspergillosis with a novel triazole (voriconazole) in a patient with acute leukaemia. Br J Haematol 1997; 97: Baslar Z, Soysal T, Hanci M et al. Successfully treated invasive central nervous system aspergillosis in an allogeneic stem cell transplant recipient. Bone Marrow Transplant 1998; 22: Khoury H, Adkins D, Miller G et al. Resolution of invasive central nervous system aspergillosis in a transplant recipient. Bone Marrow Transplant 1997; 20: Collette N, van der Auwera P, Pascual-Lopez A et al. Tissue distribution and bioavailability of amphotericin B in cancer patients treated with amphotericin B deoxycholate. Antimicrob Agents Chemother 1989; 33: Collette N, van der Auwera P, Meunier F et al. Tissue distribution and bioavailability of amphotericin B administered in liposomes in cancer patients. J Antimicrob Chemother 1991; 27: Como JA, Dismukes WE. Oral azole drugs as systemic antifungal therapy. N Engl J Med 1994; 330: Herbrecht R, Denning DW, Patterson TF et al. Voriconazole versus amphotericin B for primary therapy of invasive aspergillosis. N Engl J Med 2002; 347: Denning DW, Ribaud P, Milpied N et al. Efficacy and safety of voriconazole in the treatment of acute invasive aspergillosis. Clin Infect Dis 2002; 34: Perea S, Gonzalez G, Fothergill AW et al. In vitro interaction of caspofungin acetate with voriconazole against clinical isolates of Aspergillus spp. Antimicrob Agents Chemother 2002; 46: Kirkpatrick WR, Perea S, Coco BJ, Patterson TF. Efficacy of caspofungin alone or in combination with voriconazole in a Guinea pig model of invasive aspergillosis. Antimicrob Agents Chemother 2002; 46:
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