Original Article
Clinical and Pathological Features of Bacillary Peliosis Hepatis in Association with Human Immunodeficiency Virus Infection
N Engl J Med 1990; 323:1581-1586December 6, 1990
- Abstract
- Abstract
Background.
Peliosis hepatis is characterized by cystic, blood-filled spaces in the liver and is seen in patients with chronic infections or advanced cancer and as a consequence of therapy with anabolic steroids. Cutaneous bacillary angiomatosis is a bacterial infection that occurs in patients with human immunodeficiency virus (HIV) infection; its histologic appearance is that of a pseudoneoplastic vascular proliferation.
Methods.
We studied liver tissue from eight HIV-infected patients with peliosis hepatis, two of whom also had cutaneous bacillary angiomatosis. For comparison we examined tissue from four patients who had peliosis hepatis without HIV infection. Tissues were examined histologically on routine sections and with special stains and electron microscopy.
Results.
The histologic features seen in peliosis hepatis associated with HIV infection, but not in the four cases unrelated to HIV infection, were myxoid stroma and clumps of a granular purple material that on Warthin—Starry staining and electron microscopy proved to be bacilli. The bacilli, which could not be cultured, were morphologically identical to those found in the skin lesions of cutaneous bacillary angiomatosis. The clinical courses of two of the patients with this "bacillary peliosis hepatis" indicate that it responds to antibiotic treatment.
Conclusions.
HIV-associated bacillary peliosis hepatis is an unusual, treatable opportunistic infection, probably caused by the same organism that causes cutaneous bacillary angiomatosis. Our failure to find bacilli in non-HIV-associated cases implies that other pathogenetic mechanisms may also be responsible for peliosis hepatis. (N Engl J Med 1990; 323:1581–6.)
Media in This Article
Figure 1
Gross Appearance of the Liver in Patient 2.Figure 2
Microscopical Appearance of the Liver.Article Activity
- Article
PELIOSIS HEPATIS is a rare condition characterized by cystic, blood-filled spaces in hepatic parenchyma.1 2 3 4 5 6 7 8 9 10 11 12 13 14 15 Splenic peliosis has also been reported, either alone16 17 18 19 or with hepatic peliosis.2 3 4 , 10 , 11 , 19 , 20 Early cases of peliosis hepatis were seen in patients with wasting due to pulmonary tuberculosis or advanced cancer.1 2 3 4 Recently, anabolic steroids and other drugs have been implicated.5 6 7 8 9 10 11 12 13 14 15 Three reports describe peliosis hepatis in patients with human immunodeficiency virus (HIV) infection.21 22 23
We have seen two HIV-infected patients with peliosis hepatis who also had cutaneous bacillary angiomatosis, a recently described pseudoneoplastic vascular proliferation containing bacteria.24 25 26 27 28 29 30 31 32 33 Bacillary angiomatosis usually presents clinically as erythematous papules and nodules. On biopsy, there is lobular capillary proliferation containing protuberant or atypical endothelial cells. Its clinical and histologic appearance can cause bacillary angiomatosis to be confused with Kaposi's sarcoma or other vascular neoplasms. Several histologic features, including the presence of bacilli with positive results on Warthin—Starry staining, distinguish bacillary angiomatosis from other entities.32 Although potentially fatal,27 it responds to erythromycin and other antibiotics. 24 , 25 , 30 , 31 , 33
We examined liver tissue from the two patients with bacillary angiomatosis and peliosis hepatis for the presence of bacteria. We also studied liver tissue from six additional patients infected with HIV who had peliosis hepatis but did not have cutaneous bacillary angiomatosis. This report documents the clinical and pathological features of this unusual opportunistic infection in these eight patients.
Methods
We studied seven liver-biopsy specimens and two livers obtained at autopsy from eight patients with HIV disease and peliosis hepatis. For comparison, we studied four cases of peliosis hepatis that preceded the HIV epidemic (all occurred before 1978) obtained from autopsy files. One of these patients died of metastatic breast carcinoma, one of aplastic anemia treated with anabolic steroids, one of gram-negative septicemia, and one of amyotrophic lateral sclerosis who was also treated with anabolic steroids for anemia.
Tissues were routinely fixed in neutral buffered formalin, embedded in paraffin, and sliced into 4-μm sections. Hematoxylin and eosin, Fite, Brown and Brenn, Gomori methenamine silver, and Warthin—Starry stains were used as previously described.34 , 35 Tissue for electron microscopy was removed from paraffin blocks, deparaffinized in xylene, post-fixed in osmium tetroxide, and embedded in epon. Sections were stained with uranyl acetate—lead citrate and examined with a Jeol 100CX electron microscope.
Results
Clinical Findings
The clinical features of the patients at presentation are summarized in Table 1Table 1
Clinical Features at Presentation.. All patients were positive for antibody to HIV type 1. Most patients had had fever, abdominal pain, and gastrointestinal symptoms for one week to two months before presentation. Weight loss of 4.5 to 16 kg (10 to 35 lb) and cachexia (exact weight loss unknown) were also seen. Hepatomegaly was present in every patient, sometimes manifested as abdominal distention. Splenomegaly (Patients 1, 3, 4, 5, 6, and 8) and abdominal or retroperitoneal lymphadenopathy (Patients 1, 2, 4, 5, 6, and 8) were also detected clinically or by imaging studies. In Patients 1 and 3, CT or ultrasonography showed heterogeneity of the hepatic or splenic parenchyma in addition to organomegaly.Liver enzyme levels in serum were abnormal at the time of presentation in all patients. Aminotransferase levels were normal or mildly to moderately elevated (up to six times normal; average, two times normal). The gamma-glutamyltransferase and alkaline phosphatase levels were usually moderately to severely elevated (up to 10 times normal; average, 5 times normal) in the presence of a normal or only slightly elevated total bilirubin level. Most patients had the leukopenia, anemia, and thrombocytopenia often seen with advanced HIV disease.36 Two patients (5 and 6) had progressive pancytopenia, which was thought to be due to hypersplenism and was treated with splenectomy.
Liver-Biopsy Cultures
Cultures of liver tissue obtained by biopsy were performed in four patients (1, 3, 4, and 8). In one (Patient 3), Mycobacterium avium–intracellulare was recovered; however, the same organism was also cultured from a peripheral-blood sample and a lymph-node aspirate and thus may represent a disseminated intercurrent infection. Acid-fast stains of the liver-biopsy specimen from Patient 3, as well as those from the other seven patients, were negative. Cryptococcus neoformans was recovered from the liver-biopsy specimen from Patient 8, but no organisms were seen in tissue on fungal staining. The remaining liver-biopsy cultures for acid-fast bacteria and fungi were negative, as were all liver-biopsy cultures for routine bacteria and viruses.
Pathological Findings
The gross appearance of the peliotic liver was observed at autopsy in Patient 2. It weighed 3500 g (normal weight, 1500 g). Numerous cystic, blood-filled spaces up to several millimeters in diameter, as well as foci of necrosis 1 or 2 cm in diameter, were visible throughout the parenchyma (Fig. 1Figure 1
Gross Appearance of the Liver in Patient 2.). The spleen was grossly normal.Hematoxylin-and-eosin staining of sections of liver from these eight patients showed a spectrum of changes ranging from multiple dilated, blood-filled spaces (Patients 2, 3, 4, 5, 6, and 8) (Fig. 2Figure 2
Microscopical Appearance of the Liver.) to infrequent foci of dilated capillaries in a fibromyxoid stroma, resembling granulation tissue (Patients 1 and 7). In Patients 2 and 6, the peliotic spaces were large, occupying more than one lobule and compressing adjacent liver cells. The peliotic spaces were often separated from surrounding liver cells by varying amounts of fibromyxoid stroma containing a mixture of inflammatory cells, dilated capillaries, and clumps of granular purple material (Fig. 3Figure 3
Granular Purple Material (Arrows) Subsequently Identified as Bacilli.). A flattened, partial endothelial lining was present in some areas, whereas other peliotic spaces merged directly with surrounding sinusoids. Partially organized thrombi and foci of necrosis were seen in Patient 2.Two patients (5 and 6) underwent splenectomy. Both had splenomegaly (spleen weights, 780 and 540 g; normal weight, 150 g) and peliosis of the spleen. The fibromyxoid changes seen in the liver were less prominent in the spleen. In Patient 2, who died with massive hepatic peliosis, the spleen weighed 150 g at autopsy and no splenic peliosis was seen. Abdominal lymph nodes from two patients (2 and 6) showed an angiomatous capillary proliferation effacing the lymph-node architecture. In the patients with cutaneous bacillary angiomatosis (Patients 2 and 3), the characteristic lobular capillary proliferation with protuberant endothelial cells and neutrophils was seen.32
Stains of peliotic liver for fungi and acid-fast bacteria and Gram's staining with Brown and Brenn stain were negative for all eight patients. Warthin—Starry staining showed clumps of rod-shaped bacteria within the fibromyxoid areas of the liver in all patients (Fig. 4Figure 4
Clumps of Bacilli (Arrows) Identified by Warthin—Starry Staining of a Section of Liver.) and in surrounding sinusoids in Patient 6. Numerous similar clumps of bacilli were also seen in the peliotic spleen (Patients 5 and 6), angiomatous lymph node (Patients 2 and 6), and skin lesions (Patients 2 and 3) of bacillary angiomatosis. Rare clumps of bacilli were also seen in the nonpeliotic spleen in Patient 2. These bacilli corresponded to the granular purple material seen within the fibromyxoid areas in the liver or in the spleen, lymph nodes, or skin lesions on sections stained with hematoxylin and eosin.Electron microscopy of tissue from Patients 2 through 7 confirmed that the Warthin—Starry—positive rods were bacilli (Fig. 5Figure 5
Electron Micrograph of Bacilli in a Section of Peliotic Liver (Bar = 1 μm; ×14,580).), ultrastructurally similar to the reported agents of cat scratch disease and bacillary angiomatosis (there was insufficient tissue from Patients 1 and 8 for ultrastructural examination).24 , 25 , 37 38 39 Although atypical mycobacteria were cultured from the liver and blood of Patient 5, the organisms did not have the unstained cell walls and dense peripheries characteristic of atypical mycobacteria.40 An autopsy was performed on Patient 6, who died of sepsis 20 months after the diagnosis of peliosis hepatis was made on the basis of biopsy. Interestingly, there was no residual peliosis. Instead, the liver showed fibrosis and hemosiderosis. There were also focal lymphoma and scattered granulomas. Special stains revealed acid-fast bacteria in the granulomas (M. avium–intracellulare had been cultured from the patient several months before), as well as gram-positive bacilli in the liver sinusoids.
Liver sections from the four patients who had peliosis unrelated to HIV showed no areas of myxoid stroma or the granular purple material characteristic of bacillary masses. Neither Warthin—Starry staining nor electron microscopy revealed bacilli.
Therapy and Outcome
The antibiotic treatments and outcomes of these patients are summarized in Table 2Table 2
Therapy and Outcome.. In four cases, bacillary peliosis was identified retrospectively (Patients 1, 2, 4, and 6), and antibiotics were given for other coincidental infections. In four patients (3, 5, 7, and 8) bacillary peliosis was identified at the time of biopsy. Patients 3 and 8 responded to erythromycin, whereas in Patients 5 and 7, complicating factors such as intercurrent infections or malignant conditions, hepatotoxic treatments, and drug eruptions (which led to changes in antibiotics) prevented any conclusions about the course of bacillary peliosis.Discussion
Peliosis hepatis is a lesion of uncertain pathogenesis that occurs in patients with wasting due to advanced cancer and in patients treated with anabolic steroids or other drugs.1 2 3 4 5 6 7 8 9 10 11 12 13 14 15 It has also been reported in association with a variety of infections, notably pulmonary tuberculosis,1 , 2 as well as other bacterial41 , 42 and viral43 infections, including HIV infection.21 22 23 Experimental infection with the 9H leukemia virus has caused peliosis hepatis in rats.44 The eight cases of peliosis hepatis we describe here are different in that bacteria were actually found within lesional tissue, suggesting a direct etiologic role. The presence of typical cutaneous bacillary angiomatosis in two of these patients, coupled with the finding of morphologically identical bacteria in the liver and in skin lesions, suggests that the same agent is responsible for both cutaneous bacillary angiomatosis and this illness, which we call bacillary peliosis hepatis. Our failure to identify bacteria in patients with non—HIV-associated peliosis hepatis implies that there are other causes of peliosis hepatis as well.
The possibility of a role for cachexia in causing peliosis hepatis in these patients is suggested by the loss of weight in some patients as well as by the known association of peliosis hepatis with wasting diseases. Not all our patients lost weight, however, and in some the amount lost was minor. In addition, severe weight loss is common in patients with advanced HIV disease, whereas peliosis hepatis is not. These observations, coupled with the finding of bacteria in the peliotic areas in all cases, suggest that although weight loss may be contributory, it is not the principal cause of the peliosis hepatis in these HIV-infected patients.
The way that a bacillus could induce peliosis is suggested by the recent identification of an angiogenic factor elaborated by cultured Bartonella bacilliformis.45 The lesions of chronic bartonellosis are clinically and histologically similar to those of cutaneous bacillary angiomatosis.25 It is possible that the lesions of HIV-associated bacillary peliosis hepatis and bacillary angiomatosis may be due to bacteria that produce a similar angiogenic factor. The different tissue reactions seen in the liver and spleen (peliosis) as compared with the skin and lymph nodes (angiomatosis) may be due to different responses of the endothelial cells in these sites to a common stimulus.
The bacteria seen in these eight cases resemble the recently identified bacillus that causes cat scratch disease in size, staining characteristics, and ultrastructural appearance.37 38 39 , 45 46 47 48 49 50 Previous reports have documented liver and spleen involvement in non—HIV-associated cat scratch disease51 52 53 54 55 56 57 58 and in one patient with the acquired immunodeficiency syndrome from whom the bacillus that causes cat scratch disease was cultured.59 Three patients in the present series had documented exposure to cats, and such exposure has been noted in previous reports of bacillary angiomatosis.25 , 31
There are reasons to be cautious in attributing bacillary peliosis hepatis and cutaneous bacillary angiomatosis to the cat-scratch-disease bacillus, however. In contrast to cat scratch disease, in which a granulomatous or suppurative tissue response is typical,52 53 54 , 56 , 60 , 61 vascular changes predominate in bacillary peliosis hepatis and cutaneous bacillary angiomatosis. Antibiotic sensitivity data also suggest differences. Clinical responses to erythromycin have been reported in bacillary angiomatosis24 , 25 , 30 , 31 and were seen in two of our patients with peliosis hepatis, whereas the cat-scratch-disease bacillus is resistant to erythromycin in vitro.50 The agent of bacillary angiomatosis has also been noted to have a whole-cell fatty acid Chromatographic profile similar to that of B. bacilliformis but distinct from that of the bacillus that causes cat scratch disease (Cockerell C: personal communication).
Thus, although it is possible that bacillary angiomatosis and these cases of bacillary peliosis hepatis are due to the cat-scratch-disease bacillus, it is necessary to invoke at least host differences, if not a different or variant pathogen, to explain these inconsistencies. Definitive identification of the causative bacillus awaits successful culture. Our failure to culture the organism with the use of routine methods implies that it is fastidious, since numerous bacilli were seen in tissue.
Some histologic features in bacillary peliosis hepatis were distinctive and may provide clues to the diagnosis. The peliotic spaces were often associated with fibromyxoid stroma containing a few inflammatory cells, capillaries, and clumps of granular purple material; the clumps corresponded to the clusters of bacteria seen on Warthin—Starry staining and electron microscopy. These changes were not present in the liver tissue of patients with non—HIV-associated peliosis hepatis that we examined.
Clinically, most of these patients presented with constitutional symptoms such as weight loss and fever in addition to gastrointestinal symptoms or abdominal pain. Hepatomegaly was present in all cases. Laboratory findings typically included a mild-to-moderate elevation of the serum aminotransferase level and a moderate-to-severe elevation of the alkaline phosphatase level in association with a normal or only mildly elevated bilirubin level. Progressive pancytopenia occurred in two patients. Imaging studies showed abdominal lymphadenopathy and a heterogeneous hepatic or splenic parenchyma in some cases. Rupture with hemoperitoneum has previously been reported in both peliosis hepatis8 and peliosis of the spleen15 , 16 and is another possible mode of presentation, underscoring the need for rapid diagnosis and therapy in these cases.
Retrospective case identification or complicating clinical factors prevent us from drawing conclusions about the efficacy of antibiotic therapy in many of the cases. However, two patients (3 and 8) had clear clinical responses to erythromycin (2 g daily), with defervescence, diminution of liver size and enzyme abnormalities, and subjective improvement. Reports on cutaneous bacillary angiomatosis, which was present in two of these patients and which we believe is caused by the same agent that is responsible for bacillary peliosis hepatis, suggest that doxycycline and antituberculous drugs,25 , 29 , 31 in addition to erythromycin,24 , 25 , 30 , 31 may be effective against this infection. Inadequately treated, HIV-associated bacillary peliosis can be progressive (as in Patients 2 and 4) and may be fatal (as in Patient 2).
We are indebted to David Geller for his invaluable editorial assistance; to Drs. Jeffrey Aaron, Lawrence Mintz, John Stansenn, Richard Cazen, Lawrence Waites, William Lockyer, and Timothy Berger of San Francisco for kindly providing follow-up information on their patients; to Dr. Thomas Rogers of Oakland, California, for procuring additional pathological samples from Patient 2; and to Col. Peter Angritt of the Armed Forces Institute of Pathology, who kindly shared his experience with peliosis in HIV-infected patients with us and was the first to recognize the presence of bacteria in these patients.
Source Information
From the Departments of Pathology (L.A.P., T.S.B.Y., S.L.N., G.H., A.C.S., L.D.F., P.E.L.), Laboratory Medicine (S.M.G.), and Dermatology (P.E.L.), University of California, San Francisco; the Departments of Internal Medicine (S.P.C.) and Pathology (H.Z.K., R.L.G.), Mount Zion Hospital, University of California, San Francisco; the Department of Pathology, Pacific Presbyterian Medical Center, San Francisco (R.G.-K.); and the Institute for Forensic Sciences, Oakland, Calif. (S.V.M.). Address reprint requests to Dr. LeBoit at the Department of Pathology, HSW-501. School of Medicine, University of California, San Francisco, CA 94143–0506.
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