Eur J Clin Microbiol Infect Dis (1999) 18 : 324329

Q Springer-Verlag 1999

Article

Etiology, Clinical Features and Outcome of Splenic Microabscesses in HIV-Infected Patients with Prolonged Fever
M. Bernabeu-Wittel, J.L. Villanueva, J. Pachn, A. Alarcn, L.F. Lpez-Corts, P. Viciana, F. Cadaval, A. Talegn
Abstract A prospective study was conducted to determine the etiology, clinical features, and outcome in a series of 32 consecutively enrolled HIV-infected patients with prolonged fever in whom high resolution (7.5 Mhz) sonography revealed multiple splenic microabscesses. Conventional (3.5 Mhz) sonography showed no splenic abnormalities in any patients. The diagnoses were: tuberculosis (14), visceral leishmaniasis (7), disseminated Mycobacterium avium complex infection (5), Salmonella spp. bacteremia (2), lymphoma (2), disseminated Rhodococcus equi infection (1), disseminated Candida krusei infection (1) and Pneumocystis carinii pneumonia (1). Twenty-eight patients were followed up for six months and four were lost to follow-up. In 16 patients with a clinical cure and microbiological eradication, the findings on follow-up high resolution sonography were normal, and in two patients the microabscesses persisted; ten patients died. In conclusion, the findings suggest splenic microabscesses may be a frequent condition in HIV-infected patients with prolonged fever, being an unspecific manifestation of the opportunistic diseases causing fever of unknown origin in this population. They cannot be detected by conventional abdominal sonography, whereas high resolution sonography is a useful technique for their detection and follow-up.

Introduction
In the diagnostic work-up in HIV-infected patients with prolonged fever, imaging methods are frequently used to detect a possible focal origin causing the fever. Abdominal sonography, usually performed with a 3.5 Mhz transducer, has proven useful in the diagnosis of intraabdominal and retroperitoneal lesions in HIVinfected patients with prolonged fever, the rate of

detection of focal lesions of the spleen in these patients using this method being 12% [13]. Computerized tomography (CT) is also a sensitive method for detecting abdominal abnormalities [46]. Recently, abdominal sonography performed with a 5 Mhz-transducer was successfully used to investigate AIDS patients, multiple liver lesions and small focal splenic lesions (microabscesses) being detected in 14% of them [7]. However, the etiology was not determined accurately, and no follow-up sonographic examination was performed. Thus, there is a lack of information on the clinical features, etiology and outcome in patients in whom these lesions are detected. Sonography using a high resolution transducer (7.5 Mhz) has been used in the examination of subcutaneous tissue and the thyroid gland [8, 9]. This transducer has a higher resolution, detecting small lesions not detected by conventional transducers. However, the value of high resolution sonography in detecting

M. Bernabeu-Wittel (Y), J.L. Villanueva, J. Pachn, A. Alarcn, L.F. Lpez-Corts, P. Viciana Department of Infectious Diseases, Hospital Universitario Virgen del Roco. Avda. Manuel Siurot s/n, E-41013 Seville, Spain F. Cadaval, A. Talegn Department of Radiology, Hospital Universitario Virgen del Roco, Seville, Spain

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abdominal abnormalities in HIV-infected patients with prolonged fever is not known. This study was conducted in 32 HIV-infected patients with prolonged fever in whom multiple splenic microabscesses were detected by 7.5 Mhz abdominal sonography. In all of them conventional sonography (3.5 Mhz) showed a normal spleen or regular splenomegaly, being unable to detect any focal lesions. The etiology, clinical manifestations and outcome in these patients are described.

microscopic identification of parasites/cysts on toluidine blue stain and/or direct immunofluorescence test (Pneumo-cel IF Test; Cellabs, Australia). (iv) Bacteremia or fungemia: two sets of positive blood cultures. (v) Lymphoma: pathological studies. In the case of the diagnosis of mycobacterial disease, bone marrow aspirate (BMA) without evidence of parasites and negative conventional blood cultures were required. In other diagnostic categories negative mycobacterial cultures of sputum, urine and/or blood and negative conventional blood cultures (in categories other than Category iv) were required. The patients included in the study were followed up for a sixmonth period after the diagnosis was established. Clinical and microbiological responses were evaluated after the first, second and sixth month of follow-up. Follow-up 3.5 Mhz and 7.5 Mhz abdominal sonographies were performed 1 to 2 months after the diagnosis and in the sixth month in the case of persistence. The criteria for persistence were defined as follows: continuation of fever, growth of the same microorganism in control cultures, and/ or presence of splenic microabscesses on follow-up sonography. The criteria for cure were defined as follows: complete clinical resolution when defervescence of signs and symptoms and absence of splenic microabscesses on follow-up sonography where reached, and eradication of the pathogen as indicated by negative results of microbiological investigations (stains or cultures) of different samples performed if clinically indicated.

Patients and Methods

The prospective study was performed in a tertiary teaching hospital which serves a mainly urban population of 640,000 persons. The study period was from October 1996 to September 1997. The subjects were consecutively enrolled HIV-infected patients who attended the hospital because of fever lasting 14 days or longer. All patients who fulfilled the following criteria were included in the study: presence of fever 638.5 7C for more than 14 days, presence of splenic microabscesses detected by abdominal sonography, and establishment of an accurate etiological diagnosis in accordance with the predefined criteria given below. HIV-infection was categorized according to the CDC 1993 Revised Classification System [10]. All patients were subjected to a physical examination, and blood, serum electrolyte, creatinine and liver function tests were performed. Representative samples were collected for microbiological and pathological investigations at the discretion of the clinician in charge of the patient. A chest radiograph and 3.5 Mhz and 7.5 Mhz transducer abdominal sonograms were obtained in all patients. An abdominal CT (Sytec 3000, GE Medical Systems, USA) was performed with intravenous iodine containing contrast medium in 11 patients before the beginning of treatment. For this purpose, 120 ml of iodixanol (Nykomed, Ireland) containing 325 mg of iodine/ml was injected at 1 m/sec, scanning beginning after a 45 sec delay. Imaging was performed with 5 mm-thick sections at 5 mm intervals. Abdominal sonography was performed with a real-time electronic sonograph (Siemens Sonoline-versa) using 3.5 Mhz and 7.5 Mhz transducers. Two independent radiologists, who were unaware of the symptoms of the patients, first evaluated the conventional (3.5 Mhz) scans and then the specific transthoracic scans of the spleen performed with a 7.5 Mhz transducer. Thoracic wall abnormalities had previously been ruled out. The number (none, one, two, three, multiple), sonographic appearance (anechogenic, hypoechogenic, hyperechogenic) and size/diameter (~5 mm, 65 mm) of the observed lesions were evaluated. A microabscess was defined as a hypoechogenic lesion ~5 mm in diameter. Hypoechogenic lesions 65 mm in diameter were termed macroabscesses. The etiological diagnosis was established after microbiological and/or pathological study of spleen samples obtained by splenectomy or necropsy, or of other representative non-spleen samples. The following diagnostic categories and criteria were used: (i) Tuberculosis, Mycobacterium avium complex (MAC) and other mycobacterial infections: isolation of Mycobacterium spp. in Lwenstein-Jensen medium and identification of species by a polymerase chain reaction technique (Gen-Probe Systems; BioMrieux, France). (ii) Visceral leishmaniasis: microscopic identification of amastigotes in blood or bone marrow aspirate/biopsy specimens on Giemsa stain. (iii) Pneumocystis carinii infection:

Results
Clinical Features and Etiology. Thirty-two of the 138 evaluated patients were included in the study: 29 (91%) males and 3 (9%) females. The other 106 patients were excluded for the following reasons: in 99 patients focal lesions of the spleen were not detected, in four patients with splenic microabscesses no etiological diagnosis could be reached after extensive diagnostic studies and in three patients macroabscesses more than 2.5 cm in diameter were detected with 3.5 Mhz and 7.5 Mhz transducers. The risk factor for HIV acquisition was intravenous drug abuse in 26 (81%) patients, homosexual male intercourse in two patients, heterosexual intercourse in two patients and previous administration of contaminated coagulation factor concentrates in two patients. The mean age was 33 years (range 1739) and the median CD4c lymphocyte count was 40 cells/ml (range 3354); all patients were in the C clinical stage of the disease. Ten patients were receiving antiretroviral treatment consisting of retrotranscriptase inhibitor analogues in combination. All patients received medical attention because of prolonged fever. The median duration of fever before the first visit was 23 days (range 1490). Other frequent signs and symptoms are shown in Table 1. The chest radiograph was normal in 24 (75%) patients, but showed interstitial infiltrates in five and alveolar infiltrates in three. Laboratory findings are shown in Table 2. Thirty-three diagnoses were established in the 32 patients as follows: tuberculosis (14 cases), visceral leishmaniasis (7 cases), disseminated Mycobacterium

326 Table 1 Signs and symptoms in AIDS patients with prolonged fever and splenic microabscesses Sign/symptom Hepatosplenomegaly Peripheral adenopathy Cough/expectoration Abdominal pain No. (%) of patients 23 18 13 9 (72) (56) (40) (28)

splenic microabscesses in all 32 patients. No differences in size (all ~5 mm in diameter), number (in all patients there were multiple lesions) or sonographic appearance (all lesions were hypoechogenic) of the lesions were detected among patients with different etiological diagnoses. Abdominal CT was performed in 11 patients. It was normal in three, showed homogeneous hepatosplenomegaly in five, homogeneous splenomegaly in two, and intraabdominal or retroperitoneal adenopathy in three. Follow-Up. Twenty-eight patients could be followed up, and four patients (all diagnosed as having tuberculosis) were lost to follow-up. In 18 patients a follow-up sonography was performed 1 to 2 months after the diagnosis and beginning of treatment. Thirteen of them were cured in the first two months and three after six months, and in all of them the follow-up sonography showed no abnormalities. Two patients showed persistence after six months of follow-up. One of them had disseminated isoniazid-resistant tuberculosis and developed tuberculous meningitis, sonography also showing persistence of splenic microabscesses. In the other one, who was first diagnosed as having lymph node tuberculosis, the adenopathy disappeared but he continued to be febrile and after five months developed multiple splenic macroabscesses, detectable on 3.5 Mhz and 7.5 Mhz sonography. Finally, he underwent splenectomy, and pathological investigations revealed a Hodgkinbs lymphoma. Ten patients died during the first month of follow-up. Mortality was attributable to opportunistic disease in all but one patient who died of acute pancreatitis after administration of meglumine antimoniate. In eight of the deceased necropsy was refused. In one patient necropsy revealed multiple small abscesses in the spleen with growth of Candida krusei from pus. In a second patient hepatic infiltration, multiple small nodules in the spleen and multiple adenopathy were observed on necropsy, pathological investigations showing high grade Tcell lymphoma. In the survivors the total duration of fever was 35 days (range 19100), 10 days (range 160) being the median duration of fever after treatment. The outcome and response to treatment differed depending on the etiology of the splenic microabscesses (Figure 1). Of the 14 patients with tuberculosis, four were lost to follow-up, six were cured, two showed persistence of the splenic abscesses after six months, and two died. Visceral leishmaniasis was cured in six (86%) patients. After specific treatment, a complete clinical response and microbiological eradication were achieved in two patients with MAC infection and in the patient with Pneumocystis carinii pneumonia. Salmonella bacteremia was cured in one patient. The outcome was death in the patients with nonHodgkins lymphoma, disseminated candidiasis and Rhodococcus equi infection.

avium complex infection (5 cases), Salmonella bacteremia (2 cases), disseminated Rhodococcus equi infection (1 case), disseminated Candida krusei infection (1 case), Pneumocystis carinii pneumonia (1 case) and lymphoma (2 cases). In one case both tuberculosis and Hodgkins lymphoma were diagnosed. The diagnosis was established on the basis of results of microbiological investigation of the following nonspleen samples in 30 cases: bone marrow aspirate in nine cases (7 visceral leishmaniasis, 1 tuberculosis, 1 MAC infection), lymph node biopsy in eight cases (5 tuberculosis, 3 MAC infection), sputum in seven cases (tuberculosis), blood cultures in four cases (2 Salmonella bacteremia, 1 MAC infection, 1 disseminated Candida krusei infection), urine in one case (tuberculosis), lung biopsy material in one case (Pneumocystis carinii pneumonia), and pleural effusion fluid in one case (Rhodococcus equi pneumonia). Spleen samples provided the etiological diagnosis in three cases (1 disseminated Candida krusei infection, 1 Hodgkins lymphoma, 1 nonHodgkins lymphoma). Sonography and Computed Tomography Findings. Abdominal 3.5 Mhz sonography was normal or showed only homogeneous hepatosplenomegaly. Abdominal 7.5 Mhz sonography revealed multiple

Table 2 Laboratory results in HIV-infected patients with prolonged fever and splenic microabscesses Laboratory parameter Liver function a GGT 1 50 IU/l AST 1 37 IU/l Alkaline phosphatase 1 280 IU/l Hepatitis (AST 1 185 IU/l and ALT 1 200 IU/l) Hematological parameters Anemia b Leukopenia (~4500 cells/ml) Thrombopenia (~100,000 cells/ml) Neutropenia (~1000 cells/ml)
a

No. of patients (%) 26 (81) 23 (72) 19 (59) 2 (6) 30 22 7 4 (94) (69) (22) (12.5)

GGT, gamma glutamyl transpeptidase; AST, aspartate aminotransferase; ALT, alanine aminotransferase b Males: hemoglobin~13 g/dl; females: hemoglobin~11.7 g/dl

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Figure 1 Outcome in HIV-infected patients with prolonged fever and splenic microabscesses according to the etiological diagnosis. MAC, Mycobacterium avium complex

Discussion
In this study using abdominal sonography with a 7.5 Mhz transducer, multiple splenic microabscesses were detected in 36 (26%) of the 138 patients evaluated, whereas no such microabscesses were detected using a 3.5 Mhz transducer. These results are better than those obtained by other investigators who detected microabscesses in 14% of patients using a 5 Mhz transducer [7]. The rate of detection of any focal lesion of the spleen increased to 28% with a 7.5 Mhz transducer (36 cases of microabscesses and 3 cases of macroabscesses), while the detection rate with a 3.5 Mhz transducer was only 2.2% (3 cases of macroabscesses). In other studies using conventional sonography, the rate of detection of splenic macroabscesses was 12% [1, 3], and only a few case reports describing these lesions in HIV-infected patients have been published [1119]. Our findings suggest that splenic microabscesses may be a frequent condition in HIV-infected patients with prolonged fever that goes undetected when conventional abdominal sonography is performed. Sonography with a 7.5 Mhz transducer is sensitive, detecting not only microabscesses but also larger lesions. Although the evaluation of CT was not the aim of this study, it was performed at the discretion of the physician who treated the patient. No focal lesions of the spleen were detected in any of the 11 patients who underwent CT. Splenic microabscesses occurred in patients with advanced HIV infection. The mean duration of fever before the first evaluation was relatively long (21 days), and the signs and symptoms were unspecific, not suggesting a focal etiology. The chest radiograph was normal in 75% of patients, and any changes in laboratory test values were also unspecific. Since Durack and Street [20] reexamined the phenomenon of fever of unknown origin (FUO) and defined the first criteria for HIV-associated FUO, several clinical studies have been

conducted evaluating this phenomenon [2124]. In these studies, clinical, radiological or microbiological evidence of a focal condition was considered as an exclusion criterion [2124]. Applying the criteria of Lozano et al [24], 11 patients in the present study could be considered as having FUO. However, applying the results of 7.5 Mhz sonography as exclusion criterion, none of these patients would have fulfilled the FUO criteria. Whether or not the presence of splenic microabscesses should be considered as an exclusion criteria for HIV-associated FUO remains to be elucidated. In the present study there was a broad spectrum of etiologies, a lack of specific diagnostic procedures when splenic microabscesses were detected, and an accurate etiological diagnosis was established using non-spleen samples in most cases, so that the use of 7.5 Mhz abdominal sonography findings as exclusion criteria for FUO does not seem justified since there is a high degree of unspecificity when these findings are considered alone. Examination of non-spleen samples provided the etiological diagnosis in 93.7% of the patients. In only two patients examination of spleen samples was necessary to reach a final diagnosis. Although the objective of the present study was not to evaluate the usefulness of different diagnostic procedures, the cure after specific treatment with resolution of splenic microabscesses in 16 patients, and the concordance of blood culture results and postmortem findings in the patient disseminated candidiasis strongly suggest the diagnosis was accurate. The persistence of fever and splenic microabscesses in the patient with disseminated tuberculosis in whom treatment failed, and in the patient finally diagnosed as having Hodgkins lymphoma suggests that continuation of fever and/or the finding of spleen abnormalities on follow-up sonography are a sign of treatment failure or another disease. Considering these findings and the risk of severe complications after splenic puncture [2527], we think that use of this procedure is not justified and that other diagnostic samples obtained with less risk to the patient provide a final diagnosis in most HIV-infected patients with prolonged fever and splenic microabscesses. However, splenic fine-needle aspiration using a 22 gauge spinal needle has been advocated recently for the diagnosis of hematological disorders involving the spleen in nonHIV-infected patients, the procedure being shown to have a very low rate of complications [28, 29]. Further studies are necessary to determine the usefulness of this method in HIV-infected patients with prolonged fever and splenic microabscesses. There was a broad spectrum of etiologies of the splenic microabscesses in the present study. The most frequent etiological diagnoses were tuberculosis (43% of cases), visceral leishmaniasis (21%) and disseminated MAC infection (15%). These etiologies differ from those in splenic macroabscesses in the general population

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[3033], but are very similar to the etiologies of FUO in HIV-infected patients in our area [2124]. In two previous studies in Spain, tuberculosis (42% and 48% respectively), visceral leishmaniasis (14% and 16% respectively) and MAC infection (14% and 7% respectively) were the main causes of FUO in this population [22, 24]. Almost all cases reported of fever and focal lesions of the spleen in AIDS patients have been due to disseminated mycobacterial infection, and the lesions detected were always macroabscesses [1119]. Visceral leishmaniasis often occurs in HIV-infected patients living in the Mediterranean area [3436]. Disseminated and atypical forms of this disease have become more frequent in recent years [36, 37], however infection with Leishmania spp. has not previously been reported as a cause of focal lesions of the spleen. In Hodgkins and non-Hodgkins lymphoma splenic nodules with a sonographic pattern identical to that of macroabscesses may develop [2, 25, 38]. Since AIDS patients are at a high risk of developing lymphomas [39, 40], this disease should be taken into account in patients with advanced HIV infection, prolonged fever and evidence of splenic microabscesses, especially in view of our findings. Tuberculosis was cured in 60% of the patients by means of medical treatment, splenectomy only being necessary in one patient with a final diagnosis of Hodgkins lymphoma. This outcome is better than that reported in previous studies, in which splenectomy was necessary in 40% of patients with tuberculosis and macroabscesses of the spleen [1119]. The rate of clinical and parasitological cure and also of survival after meglumine antimoniate treatment in patients with visceral leishmaniasis (83%) was similar to that reported in other studies [3436]. In conclusion, the findings of this study suggest that splenic microabscesses may be a frequent condition in patients with advanced HIV infection and prolonged fever. They are an unspecific manifestation of the opportunistic diseases that mainly cause FUO in HIVinfected patients in southwestern Europe. Splenic microabscesses are not detectable on conventional (3.5 Mhz) abdominal sonography, whereas sonography using a 7.5 Mhz transducer is a useful technique for their detection and follow-up.

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