Case Report. Unusual Aspects of Acute Q Fever-Associated Hepatitis
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1 Case Report Unusual Aspects of Acute Q Fever-Associated Hepatitis STEVEN H. YALE, M.D., PIET C. DE GROEN, M.D., JULIUS D. TOOSON, M.D., AND PAUL J. KURTIN, M.D. We describe a 37-year-old farmer with a 3-week history of fevers and hepatitis, in whom Q fever was diagnosed. The diagnosis was based on the findings of characteristic "ring" granulomas on a bone marrow biopsy specimen and confirmed by complementfixation antibody tests to Coxiella bumetii. Unusual aspects of this case included (1) relatively low complement-fixation antibody titers, (2) prolonged pro- thrombin time, (3) false-positive results of a sérologie test for the human immunodeficiency virus (HIV), and (4) ring granulomas that progressed to atypical granulomas in biopsy specimens. (Mayo Clin Proc 1994; 69: ) AIDS = acquired immunodeficiency syndrome; ELISA = enzyme-linked immunosorbent assay; HIV = human immunodeficiency virus The rickettsial organism Coxiella bumetii is known to cause Q fever. The disease is transmitted primarily by sheep and cattle and less commonly by drinking unpasteurized milk.'2 Both an acute and a chronic variant of the disease are well recognized. The acute variant is characterized by headache, fever, general malaise, myalgia, and sometimes pneumonia and hepatitis. The most important predisposing risk factors for the chronic variant, predominantly characterized by Q fever associated with endocarditis, are underlying heart disease and immunocompromising conditions.2 In this article, we describe an unusual case of acute Q fever associated with hepatitis in a farmer who was found to have relatively low complement-fixation titers, a prolonged prothrombin time, false-positive results of a sérologie test for the human immunodeficiency virus (HIV), and "ring" granulomas that progressed to atypical granulomas. REPORT OF CASE A previously healthy 37-year-old sheep and goat farmer from North Dakota consulted his local physician on Apr. 12, 1993, because of a 4-day history of progressive fatigue, myalgias, intermittent bilateral headache without visual changes, and recurrent fevers as high as 40 C associated with chills. On physical examination, findings were normal. Laboratory studies yielded the following results: alkaline phosphatase, 122 U/L (normal, 31 to 113); lactate dehydrogenase, 409 U/L (normal, 89 to 221); aspartate aminotransferase, 100 U/L (normal, 9 to 48); total bilirubin, 0.4 mg/dl (normal, 0.2 to 1.2); and prothrombin time, 12.5 seconds. From the Department of Internal Medicine (S.H.Y., J.D.T.), Division of Gastroenterology and Internal Medicine (P.C.d.G.), and Division of Hematopathology (P.J.K.), Mayo Clinic Rochester, Rochester, Minnesota. Address reprint requests to Dr. P. C. de Groen, Division of Gastroenterology, Mayo Clinic Rochester, 200 First Street SW, Rochester, MN Results of sérologie tests for hepatitis A, B, and C viruses were negative. Initially oral and subsequently intravenous erythromycin therapy was given. Despite 6 days of antibiotic treatment, his symptoms persisted, and he was referred to our institution for further evaluation of hepatitis and fever of undetermined cause. On admission to our institution, elicitation of additional history revealed that no other family members or close contacts were ill. No history of alcohol use, blood transfusions, HIV-related risk factors, travel outside the Midwest, or exposure to tuberculosis or toxins was noted. One month before the current illness, the farmer's sheep were in parturition. In early April, he nurtured a lamb with pneumonia; despite antibiotics and tube feedings, the animal died 2 days before the farmer's symptoms developed. No other lambs, sheep, or goats were ill or had had spontaneous abortions. On physical examination, the patient's blood pressure was 130/100 mm Hg, the heart rate was 100 beats/min, and the respiratory rate was 12/min. He was febrile; his temperature pattern during hospitalization is summarized in Figure 1. No enlarged lymph nodes were detected. Fine rales were present over the base of the left lung posteriorly. Cardiac examination showed an S4 gallop rhythm without a pericardial rub or murmur. The abdomen was soft and nontender; no hepatosplenomegaly or stigmas of liver disease were noted. Results of a neuromuscular examination were normal. Laboratory studies yielded the following results: hemoglobin, 12.1 g/dl (normal, 13.5 to 17.5); platelet count, 138 X 107L (normal, 150 to 450); and leukocyte count, 6.3 X 107 L (normal, 3.5 to 10.5), with a differential cell count of 40% segmented neutrophils, 7% bands, 41% lymphocytes, 11% monocytes, and 1 % eosinophils. The prothrombin time was 26 seconds (international normalized ratio, 2.6). The peripheral blood smear showed large granular lymphocytes and Mayo Clin Proc 1994; 69: / 994 Mayo Foundation for Medical Education and Research
2 770 ACUTE Q FEVER HEPATITIS Mayo Clin Proc, August 1994, Vol I 390 i I /01 5/02 5/03 5/04 5/05 5/06 5/07 5/08 5/09 5/10 5/11 5/12 5/13 5/14 1/ Λ V V V * \ ft V rf f 0 \J \Λ Alkaline phosphatase Aspartate aminotransferase Alanine aminotransferase Total bilirubin Direct bilirubin Calcium Albumin Prothrombin time Fig. 1. Temperature profile of 37-year-old man during hospitalization for acute fevers and hepatitis. Alkaline phosphatase, aspartate aminotransferase, and alanine aminotransferase values are in U/L; bilirubin and calcium values in mg/dl; albumin value in g/dl; and prothrombin time in seconds. target cells. Findings on the electrolyte panel were normal. The results of pertinent chemistry tests performed throughout the patient's hospitalization are listed in Figure 1. Results of a sérologie test for HIV-1 and HIV-2 showed a positive enzyme-linked immunosorbent assay (ELISA) (Abbott Laboratories) with an indeterminate Western blot assay (weak p24, weak pi60). A subsequent HIV p24 antigen assay (ELISA) was negative. Lymphocyte subset analysis revealed a total CD4 cell count of 396 μ/l (normal, 589 to 1,505) and a total CD8 cell count of 396 μ/l (normal, 325 to 997), with a helper-suppressor ratio of 1. Blood cultures were negative for bacteria and fungi. Results of sérologie, tests done at admission are listed in Table 1. A chest roentgenogram showed linear atelectasis or fibrosis at both lung bases, greater on the left than on the right. A small amount of fluid or pleural thickening was noted at both costophrenic angles. Findings on a chest roentgenogram on hospital day 5 were normal. Abdominal ultrasonography showed gallbladder thickening and incomplete distention. Echotexture of the spleen and liver was normal. Computed tomography of the abdomen disclosed a single enlarged perihepatic lymph node that was not evident on an examination 5 days later. Both the liver and spleen were normal in appearance. Computed tomography of the head showed normal findings. Administration of vitamin K did not correct the prolonged prothrombin time, and the patient's fevers persisted. Therefore, on hospital day 3, a bone marrow biopsy and aspirate were performed to determine the cause of the persistent fevers. The bone marrow biopsy specimen showed numerous fibrin ring granulomas strongly suggestive of Q fever (Fig. 2). The aspirate was hypercellular with mild granulocytic and megakaryocytic hyperplasia. Normal stainable iron was present. Cultures for bacteria and acid-fast organisms were negative. Doxycycline therapy (100 mg twice a day) was initiated, and the dose was increased (to 200 mg) 2 days later. On hospital day 5, the results of the Q fever sérologie tests done at the time of admission were completed Table 1. Results of Serologie Tests Performed, on Admission, in 37-Year-Old Man With Hepatitis and Fever Organism Adenovirus Blastomycosis Brucella Chlamydia Coccidioidomycosis Cytomegalovirus Epstein-Barr virus Hepatitis A, B, and C viruses Histoplasmosis Legionella Leptospirosis Murine typhus Q fever (Coxiella burnetii) Day 1 Day 9 Day 28 Day 83 Toxoplasma Tularemia Varicella-zoster *VCA = viral capsid antigen. Serologie result 1:16 IgG<l:10 IgG<l:5;IgM<l:10 IgG 1:160; IgM<l:10(VCA*) 1:32 (normal, <1:128) Nonspecific 1:64 (borderline; normal, <1:128) 1:32 (normal, <1:2) 1:64 1:256 1:512 IgG 1:40; IgM<l:10
3 Mayo Clin Proc, August 1994, Vol 69 ACUTE Q FEVER HEPATITIS 771 and showed a complement-fixation antibody titer to C. burnetii at 1:32. A subsequently obtained echocardiogram showed an ejection fraction of 49%. Mild valve thickening and a small pericardial effusion were noted, but no valvular vegetations were evident. After doxycycline had been administered for 3 days, ciprofloxacin (500 mg) was added and given orally twice a day. During the next 9 hospital days, the patient continued to have a hectic fever pattern; temperatures were as high as 40.2 C (Fig. 1). Liver enzymes were increased. Laboratory results on hospital day 11 were as follows: alkaline phosphatase, 656 U/L; aspartate aminotransferase, 244 U/L; alanine aminotransferase, 286 U/L; total bilirubin, 1.0 mg/dl; and prothrombin time, 16.0 seconds. Therefore, a liver biopsy was performed. This procedure revealed multiple small noncaseating epithelioid cell granulomas and one typical ring granuloma (Fig. 2). In addition, areas of spotty necrosis, small clusters of inflammatory cells in sinusoids, and some ductular proliferation in conjunction with minimal portal and periportal fibrosis were evident. Proliferated Kupffer cells contained ferritin and hemosiderin. Because of the persistently prolonged prothrombin time, which failed to correct despite three doses of vitamin K- replacement therapy administered subcutaneously, special coagulation studies were performed. The diluted Russell viper venom time was prolonged and inhibited; it was corrected with the platelet neutralization procedure. This finding is consistent with a circulating lupuslike anticoagulant. The patient was afebrile on hospital day 12 and was dismissed 2 days later, after remaining afebrile for 48 hours. Antibiotic therapy, including ciprofloxacin (500 mg) twice a day and doxycycline (200 mg) twice a day, was continued for an additional 2 weeks "after dismissal. At 1- and 3-month follow-up, the patient remained afebrile, and clinical recovery was complete. Results of the sérologie test for Q fever were 1:256 at one month and 1:512 or more at 3 months; results were negative for HIV. DISCUSSION Our patient had a 3-week period of persistent fevers and hepatitis due to the rickettsial organism C. burnetii, the causative agent of Q fever. The diagnosis was supported by the characteristic but not pathognomonic ring granuloma found in both bone marrow and liver biopsy specimens and confirmed by complement-fixation antibodies to C. burnetii. Our laboratory was still using the complement-fixation method to soluble phase II Coxiella antigen (see subsequent discussion) at the time of diagnosis. A titer greater than 1:2 suggests exposure to C. burnetii; titers 1:32 or higher strongly suggest acute infection. A fourfold or greater increase in complement-fixation antibody titer between acute and convalescent serum levels is diagnostic of Q fever. Fig. 2. A, Bone marrow biopsy specimen, showing typical "ring" granuloma (arrow). B and C, Liver biopsy specimens, showing one typical ring granuloma (B) (arrow) and one atypical granuloma (Q (arrow). (Hematoxylin-eosin; original magnification, Xl25.) Recently, our laboratory began using the more sensitive immunofluorescence assay.3 Our patient presumably contracted the infection through inhalation of infected aerosolized droplets from the parturient ewe or goat placenta. Sheep placenta has been reported
4 772 ACUTE Q FEVER HEPATITIS Mayo Clin Proc, August 1994, Vol 69 to contain as many as 10 9 infectious doses (ID^) per gram of tissue during late gestation. 4 Other potential sources of disease transmission include inhaling aerosolized dust, consuming fresh goat cheese, and drinking unpasteurized milk from subclinically infected animals.' The initial symptoms of Q fever are nonspecific and may resemble a "flulike" illness; however, the presence of daily fever spikes up to 40 C for 1 month is distinctly unusual in a typical viral illness in a nonimmunocompromised host. Other possible clinical manifestations and complications include pneumonia, hepatitis, endocarditis, and meningoencephalitis.' 4 Liver abnormalities noted in Q fever include hepatomegaly, liver tenderness, jaundice, and increased serum bilirubin, aminotransferases, and alkaline phosphatase. 2 4 These findings are known to occur in the absence of pulmonary involvement. 4 Q fever can follow either an acute or a chronic clinical course. The distinction between the acute and chronic state is based on quantitative antibody titer to phase I and II antigens. Antibodies to phase II antigens occur early during the course of Q fever, followed by a later increase in antibodies to phase I antigens in patients with chronic disease. 5 Serologie tests for chronic Q fever show a high and prolonged IgG antibody titer to both phase I and II antigens. 4 High specific IgM and IgG antibody titers to phase II antigens have been found in patients with granulomatous hepatitis. 5 The clinical significance of false-positive sérologie results of ELIS A for HIV in the presence of Q fever is unclear. The serum from intravenous drug addicts has shown falsepositive sérologie reactions to rickettsiae; however, no association has been noted between positive rickettsial serology and HIV antibodies. 6 High titers of rheumatoid factor have been found in the sera from patients with granulomatous hepatitis and endocarditis and account for the high IgM titers found in Q fever. The sera from our patient had anticomplementary activity that interfered with the results of unrelated complement-fixation antibody tests to adenovirus, histoplasmosis, coccidioidomycosis, and blastomycosis. The presence of the transient anticomplementary activity in patients with granulomatous hepatic Q fever may reflect the presence of immune complexes. 7 These immune complexes compromise IgM antibodies directed at the Fc receptor of IgG. Using platelet aggregation and platelet iodinated protein A tests to detect circulating immune complexes, Lumio and associates 7 showed that 10 of 11 patients had circulating immune complexes to a component of C. burnetii. Although rheumatoid factor was not measured in our patient, the titer in complement-fixation tests to C. burnetii was low despite florid ring granulomas on a bone marrow biopsy specimen. Therefore, we suspect that both the somewhat low titer relative to the severity of this patient's disease and the anticomplementary interference observed on complementfixation assays were likely due to the presence of circulating immune complexes. A special coagulation profile was obtained in our patient when the increased prothrombin time failed to correct despite vitamin K supplements. The results indicated the presence of a lupuslike anticoagulant in the serum. Anticardiolipin antibodies have been reported in patients with acute infection and presumably accounted for the prolonged prothrombin time in our patient because his prothrombin time corrected after the acute infection subsided. 8 In a study of 92 patients in France, Brouqui and colleagues 2 detected the presence of anticoagulant antibodies in 2 of the 9 patients tested. Underlying heart disease and immunodeficiency states have been reported to be the most common factors predisposing to chronic Q fever. 2 Additionally, patients with the acquired immunodeficiency syndrome (AIDS) seem to be more susceptible and symptomatic to Q fever than are nonimmunocompromised persons. 2 9 Defects in T-lymphocyte response to Coxiella antigens may be an important factor in persistent and chronic infection with this organism. 10 Histopathologic findings that may be detected in liver specimens include ring, atypical, and nonspecific granulomas (see subsequent discussion), inflammatory cells, histiocytes, multinucleated giant cells, fat vacuoles, and fibrin. Other associated findings in liver specimens can include Kupffer cell hyperplasia and focal liver cell necrosis."' 6 Pellegrin and coworkers 16 reviewed the pathologic findings in 17 patients with granulomatous hepatitis and classified the granulomatous changes into three characteristic groups: typical, atypical, and nonspecific lesions. Typical lesions consisted of eosinophilic fibrinoid material, either within or surrounding the granuloma. In the latter situation, the concentric fibrinoid material forms a ring around an oval or round central space, which probably represents a fat-containing vacuole. Atypical lesions consist of either granulomas and fibrinoid material not arranged in an annular manner or not containing a central clear space or a noncaseating granuloma that has central fibrinoid necrosis surrounded by multinucleated giant cells. Nonspecific lesions represent granulomas that lack fibrinoid material but contain a central clear space. Pellegrin and associates' 6 suggested that the early lesions are confined to the hepatic sinusoids and that the atypical lesions represent the advanced phase of the typical lesion. Travis and colleagues' 7 reported that the ring granuloma represents not only an early phase of the inflammatory response to C. burnetii but also a persistent type in untreated patients. Our patient's bone marrow biopsy specimen, obtained 25 days after the onset of initial symptoms, showed numerous typical fibrin ring granulomas. A liver biopsy specimen, obtained 8 days later, showed only a single ring granuloma but many atypical noncaseating granulomas.
5 Mayo Clin Proc, August 1994, Vol 69 ACUTE Q FEVER HEPATITIS 773 These findings support the theory that the fibrin ring granuloma undergoes transition to the more advanced atypical granuloma later in the course of Q fever. Additionally, the liver biopsy specimen showed the presence of minimal portal and periportal fibrosis. Atienza and coworkers 18 described a patient whose initial liver biopsy specimen showed minimal portal fibrosis; subsequent biopsy samples demonstrated extensive liver fibrosis and portal hypertension despite antibiotic therapy with doxycycline and cotrimoxazole. The chemotherapeutic approach to Q fever depends on whether the acute or chronic variant is being treated. Acute infection is generally self-limited, and most infections resolve without antibiotic therapy. 19 The tetracycline analogue doxycycline remains the mainstay of therapy for acute infections. The tetracyclines have been shown to decrease the duration of fever if administered during the first 3 days after infection. 20 The quinolones or rifampin is an alternative therapy for patients unable to take or tolerate doxycycline. Currently, therapy is recommended for 2 to 3 weeks. 19 Chronic infection that manifests as endocarditis can be persistent, and recurrent infections are known to occur despite antibiotic therapy. Yeamen and associates, 21 using in vitro L929 fibroblast cells, showed that the most effective antibiotics in eradicating C. burnetii in chronically infected cells were the quinolones (difloxacin, ciprofloxacin, and oxolinic acid) and rifampin. In 25 patients treated with either doxycycline or doxycycline and ciprofloxacin, the combination of doxycycline and ciprofloxacin was shown to be associated with a lower mortality. 22 For the treatment of Q fever associated with endocarditis, Levy and colleagues 22 recommended the combination of doxycycline and quinolones for a minimal duration of 3 years. After 3 years, if the level of IgG against phase I antigen is less than 1:400 and no IgA antibody against phase I is found, therapy can be discontinued. 22 In contrast, Raoult 19 recommended treatment as long as patients had IgG anti-phase I antigen titers greater than 1:200 and IgA anti-phase I antigen titers greater than 1:25. CONCLUSION We report several unusual aspects associated with a case of acute Q fever. Awareness of Q fever and its findings, especially in nonendemic regions, is important to ensure that appropriate therapy is initiated in a timely fashion in order to prevent the development of chronic endocarditis. REFERENCES 1. Tissot Dupont H, Raoult D, Brouqui P, Janbon F, Peyramond D, Weiller P-J, et al. Epidemiologie features and clinical presentation of acute Q fever in hospitalized patients: 323 French cases. Am J Med 1992; 93: Brouqui P, Tissot Dupont H, Drancourt M, Berland Y, Etienne J, Leport C, et al. Chronic Q fever: ninety-two cases from France, including 27 cases without endocarditis. Arch Intern Med 1993; 153: Edlinger E. Immunofluorescence serology: a tool for prognosis of Q-fever. Diagn Microbiol Infect Dis 1985;3: Sawyer LA, Fishbein DB, McDade JE. Q fever: current concepts. Rev Infect Dis 1987;9: Peacock MG, Philip RN, Williams JC, Faulkner RS. Serological evaluation of Q fever in humans: enhanced phase I titers of immunoglobulins G and A are diagnostic for Q fever endocarditis. Infect Immun 1983;41: Jimenez-Mejias ME, Pachon-Diaz J, Viciana-Fernandez P, Torronteras R. False-positive serology of rickettsial disease in parenteral drug addicts [letter]. J Infect Dis 1989;160: Lumio J, Penttinen K, Pettersson T. Q fever in Finland: clinical, immunological and epidemiological findings. Scand J Infect Dis 1981;13: Vaarala O, Palosuo T, Kleemola M, Aho K. Anticardiolipin response in acute infections. Clin Immunol Immunopathol 1986;41: Raoult D, Levy P-Y, Tissot Dupont H, Chicheportiche C, Tamalet C, Gastaut J-A, et al. Q fever and HIV infection. AIDS 1993;7: Koster FT, Williams JC, Goodwin JS. Cellular immunity in Q fever: specific lymphocyte unresponsiveness in Q fever endocarditis. J Infect Dis 1985;152: Hofmann CE, Heaton JW Jr. Q fever hepatitis: clinical manifestations and pathological findings. Gastroenterology 1982;83: Dupont HL, Homick RB, Levin HS, Rapoport MI, Woodward TE. Q fever hepatitis. Ann Intern Med 1971;74: Westlake P, Price LM, Russell M, Kelly JK. The pathology of Q fever hepatitis: a case diagnosed by liver biopsy. J Clin Gastroenterol 1987; 9: Qizilbash AH. The pathology of Q fever as seen on liver biopsy. Arch Pathol Lab Med 1983; 107: Thung SN, Gerber MA, Lebovics E, Reichman S. Granulomatous hepatitis in Q fever. Mt Sinai J Med 1986;53: Pellegrin M, Delsol G, Auvergnat JC, Familiades J, Faure H, Guiu M, etal. Granulomatous hepatitis in Q fever. Hum Pathol 1980; 11: Travis LB, Travis WD, Li CY, Pierre RV. Q fever: a clinicopathologic study of five cases. Arch Pathol Lab Med 1986; 110: Atienza P, Ramond MJ, Degott C, Lebrec D, Rueff B, Benhamou JP. Chronic Q fever hepatitis complicated by extensive fibrosis. Gastroenterology 1988;95: Raoult D. Antibiotic treatment of rickettsiosis, recent advances and current concepts. Eur J Epidemiol 1991;7: Powell OW, Kennedy KP, Mclver M, Silverstone H. Tetracycline in the treatment of "Q" fever. Australas Ann Med 1962; 11: Yeaman MR, Mitscher LA, Baca OG. In vitro susceptibility of Coxiella burnetii to antibiotics, including several quinolones. Antimicrob Agents Chemother 1987; 31: Levy PY, Drancourt M, Etienne J, Auvergnat JC, Beytout J, Sainty JM, et al. Comparison of different antibiotic regimens for therapy of 32 cases of Q fever endocarditis. Antimicrob Agents Chemother 1991;35:
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