Mikako Nakajima 1, Hidetake Shimizu 1, Akihisa Miyazaki, Sumio Watanabe 1, Noriyuki Kitami 2, and Nobuhiro Sato 1
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1 J Gastroenterol 1999; 34: Detection of IgA, IgM, and IgG subclasses of anti-m2 antibody by immunoblotting in autoimmune cholangitis: Is autoimmune cholangitis an early stage of primary biliary cirrhosis? Mikako Nakajima 1, Hidetake Shimizu 1, Akihisa Miyazaki, Sumio Watanabe 1, Noriyuki Kitami 2, and Nobuhiro Sato 1 1 Department of Gastroenterology, Juntendo University School of Medicine, Hongo, Bunkyo-ku, Tokyo , Japan 2 TJK Kenshin Center, Tokyo, Japan Editorial on page 657 Reprint requests to: N. Sato Received: December 17, 1998 / Accepted: May 28, 1999 Abstract: Autoimmune cholangitis (AIC) has been proposed as a distinct disease entity from primary biliary cirrhosis (PBC), without antimitochondrial antibody (AMA) and anti-m2 antibody but with a high titer of antinuclear antibody (ANA) in the serum. However, negativity for AMA and anti-m2 antibody was determined by different methods in different studies. We hypothesized that anti-m2 antibody negativity in AIC resulted from methodological differences, including selection of the immunoglobulin subclass of the autoantibody. Twenty-three patients compatible with AIC whose serum tested negative for AMA and positive for ANA ( 1:80) were compared with 71 AMApositive PBC patients. Laboratory findings, histology, and the pattern of anti-m2 antibody assessed by immunoblotting were compared. Alkaline phosphatase, total bilirubin, total cholesterol, and IgM values were lower in patients with AIC (P 0.05, 0.01, respectively). Anti-smooth muscle antibody was detected more frequently in patients with AIC (P 0.01). However, anti-m2 antibody was detected using immunoblotting not only in PBC but also in AIC cases. IgA class alone, IgM class alone, or both IgA and IgM classes of anti-m2 antibody were detected in 13%, 17%, and 22% of AIC patients, respectively, whereas they were not detected in PBC patients (P 0.05, P 0.01, P 0.01). IgG class anti-m2 was detected in all patients with PBC, whereas it was detected in 48% of patients with AIC (P 0.01). Histological evaluation showed that the early stages of disease were found more frequently in AIC (78%) than in PBC patients (39%) (P 0.01). Anti-M2 antibody was detected by immunoblotting in all AIC patients. Hence, AIC is not a distinct disease from PBC. For diagnosing AIC and/or PBC, anti-m2 antibody should be examined by the immunoblotting assay to detect not only IgG but also IgA and IgM subclasses. Key words: autoimmune cholangitis, primary biliary cirrhosis, immunoblot, anti-m2 antibody, IgA Introduction Primary biliary cirrhosis (PBC) is a chronic, progressive autoimmune liver disease of unknown etiology. The diagnosis of PBC is based on histological findings and laboratory evidence of chronic cholestasis and various autoantibodies. In particular, the detection of antimitochondrial antibody (AMA) and specific AMA for PBC (anti-m2 antibody) is indispensable for the diagnosis of PBC. 1 AMA is routinely detected by the indirect immunofluorescence test (IF). Nevertheless, this technique lacks diagnostic specificity, since it can give positive results in other diseases such as chronic active hepatitis, drug-induced hepatitis, and cardiomyopathies. 2 Berg and colleagues showed that the AMA in PBC was due to fixed antigen on the inner mitochondrial membrane. 3 The autoantibody for this antigen, defined as M2, has specificity as a marker for the serological diagnosis of PBC. In 1988, M2 antigens were identified as components of the 2-oxo acid dehydrogenase complexes located within mammalian mitochondria, 4,5 and it was reported that the E2 component of the pyruvate dehydrogenase complex (PDC) was one of the major antigens corresponding to AMA. Furthermore, it was reported that expression of either PDC-E2 or a cross-reacting molecule with PDC-E2 was increased in the apical region of the biliary epithelium in patients with PBC. 6 Therefore, PDC-E2 might be
2 608 M. Nakajima et al.: Subclasses of anti-m2 antibody and autoimmune cholangitis directly associated with the etiology of PBC. However, AMA cannot be detected in serum from about 10% of patients with clinical and pathological features of PBC. 7 In a previous study, we reported that anti-m2 antibody has four major proteins (70, 50, 47, 40kDa) and was detected in both AMA-positive and AMA-negative PBC patients by the immunoblotting method with IgG, IgA, and IgM subclasses. 8,9 Recently, AMA-negative PBC in which AMA and anti-m2 antibodies are not detected but a high titer of antinuclear antibody (ANA) is present in the serum was proposed as autoimmune cholangitis (AIC) However, in each report, the absence of detectable AMA and anti-m2 antibodies, a necessary criterion for AIC, was determined by different methods, such as immunofluorescence (IF) assay, enzyme-linked immunosorbent assay (ELISA), and immunoblotting. We hypothesized that anti-m2 antibody negativity in AIC resulted from methodological differences, including selection of antigens and the immunoglobulin subclass of the autoantibody. In this study, to clarify whether AIC is a distinct disease from PBC, we identified 23 patients showing clinical and histological features compatible with AIC whose serum tested negative for AMA and anti-m2 antibody by ELISA and positive for ANA ( 1 :80), and compared them with 71 AMA-positive patients with PBC. Methods Patients The subjects were 23 Japanese patients showing clinical and histological features compatible with PBC based on internationally accepted criteria, 14 whose serum tested negative for AMA and anti-m2 antibody by ELISA and positive for ANA ( 1:80). We defined them as having AIC. We compared AMA-positive patients with PBC (71 cases) with patients with AIC. All patients gave informed consent and were enrolled into the study. Serological tests In patients with AIC or PBC, serum levels of alanine aminotransferase (ALT), alkaline phosphatase (ALP), total bilirubin, γ-glutamyl transpeptidase (γ-gtp), total cholesterol, immunoglobulin G (IgG), IgA, and IgM were determined. On the basis of histological analysis of liver tissues, the patients were classified into four grades according to the criteria of Scheuer. 15 Stages 1 and 2 were defined as early stage, and stages 3 and 4 were defined as late stage. The IF test was performed to detect AMA, anti-smooth muscle antibody (ASMA), and ANA in unfixed frozen sections of rat liver and stomach as well as the Hep-2 line. Initially, antibody for AMA was diluted 1: 20 in phosphate-buffered saline (PBS) and 1: 40 for ASMA and ANA; the fluorescence titer was determined by increasing the dilution until an end point was reached. Serum samples were assayed for IgG class anti-pdh by ELISA Pyruvate dehydrogenase complex (PDC), which contained PCD-E2 and protein X, was purified from beef heart by the methods of Perham, 16 and horseradish peroxidase-conjugate γ goat anti-human IgG was used to detect IgG class anti- PDC. Serum was diluted 1 :1000 in PBS, and anti-pdc values were calculated from the reciprocal ELISA titer using a standard curve of optical densities measured spectrophotometrically at 492 nm against IgG. Values of anti-pdc greater than 20 ng/ml were defined as positive. 17,18 For immunoblotting, mitochondrial inner membrane proteins were prepared from beef heart mitochondria according to the modified method of Schneider and Hogeboona, 19 then treated with digitonin according to the methods of Schnaitman and Greenwalt, 20 sonicated, and centrifuged, as described previously. 21 Sodium dodecyl sulfate-polyacrylamide gel electrophoresis was carried out following the method of Laemmli, 22 and electrophoretic immunoblotting was performed by the method of Towbin et al. 23 Western blotting was performed with 1:100 diluted serum. Nitrocellulose membranes to which the proteins were transferred were developed with horseradish peroxidase-conjugated, goat anti-human IgG, IgA, and IgM. When serum samples reacted with one, two, or three immunoglobulin classes, they were classified as IgG / A / M auto-antibody positive. 8,9,21,24 Statistical analysis Statistical analysis was performed by the Wilcoxon rank-sum test (two-tailed) for laboratory findings and the chi-square test with Fisher s exact test (two-tailed) for others, as appropriate. Results The clinical features and the positive rates for AMA, ANA, and ASMA among patients with AIC and PBC are shown in Table 1. No significant differences were noted between AIC and PBC patients with respect to age, sex, and associated disorders. Asymptomatic patients were significantly more frequent among the AIC patients than the PBC patients. ANA and ASMA were detected significantly more frequently in the AIC patients than the PBC patients. Table 2 shows the laboratory findings. ALP, total bilirubin, IgM, and total cholesterol were lower in the AIC patients than with
3 M. Nakajima et al.: Subclasses of anti-m2 antibody and autoimmune cholangitis 609 PBC patients. Indeed, total bilirubin was less than 2 mg/ dl in all AIC patients, whereas in 10 of 71 PBC patients, total bilirubin was greater than 2 mg/dl (data not shown). No significant differences were found for AST, ALT, γ-gtp, IgG, and IgA. Table 1. Clinical features and the positivity of antimitochondrial antibody (AMA), antinuclear antibody (ANA), and anti-smooth muscle antibody (ASMA) AIC PBC Feature (n 23) (n 71) Female:male ratio 23 :0 63 :8 Age (mean SD) yr (n 23) (n 71) (n 22) (n 68) Number of asymptomatic 21** 48 patients Pruritus 1 8 Jaundice 0 10 Number of associated (n 23) (n 71) disorders (%) Sjogren syndrome 2 15 Sicca syndrome 0 3 Chronic thyroiditis 2 4 RA 0 3 SLE 1 1 PSS 0 5 AMA ( 1: 40) (n 23) (n 71) 0* 71 ANA ( 1 :80) (n 23) (n 61) 23* 19 ASMA ( 1 :40) (n 23) (n 41) 9* 3 RA, Rheumatic arthritis; SLE, systemic lupus erythematosus; PSS, progressive systemic sclerosis; AIC, autoimmune cholangitis; PBC, primary biliary cirrhosis Significance was determined by Fisher s exact test * P 0.01 for AMA, anti-m2 antibody, ANA, and ASMA **P 0.05 for asymptomatic Anti-M2 was detected by the immunoblotting assay in AIC and PBC patients. Representative results of anti-m2 determined by immunoblotting are shown in Fig. 1. The Western immunoblot shows the reactivity of serum from an AMA ( ) PBC patient as the positive control and from three AIC patients. Control sera reacted with each of four M2 antigens in all immunoglobulin subclasses. Whereas the serum of patient 1 reacted with 47 kda in only the IgG immunoglobulin subclass, the serum of patient 2 reacted in only the IgA subclass, and the serum of patient 3 reacted in only the IgM subclass. The pattern of anti-m2 antibody for the IgG, IgA, and IgM subclasses is shown in Table 3. Anti- M2 antibody was detected not only in PBC patients but also in AIC patients; nevertheless, AMA was not detected. The IgG class anti-m2 of antibody was detected in all PBC patients, whereas it was detected in 11 of 23 (48%) AIC patients. Further, IgG, IgA, and IgM classes of anti-m2 antibody were all detected in 46 of 71 (65%) PBC patients, but in only 2 of 23 (9%) subjects in the AIC group. In AIC patients, IgA class alone, IgM class alone, or both IgA and IgM classes of anti-m2 were detected in 13%, 17%, and 22%, respectively, whereas they were not detected in PBC patients. The histological stage was classified into two groups, early stage (stages 1 and 2 by Sheuer s classification) and late stage (stages 3 and 4). The number of earlystage AIC and PBC patients in each immunoglobulin class of anti-m2 is shown in Table 4. The early stage was found more frequently in AIC patients (18 of 23) than in PBC patients (28 of 71). Moreover, among the patients in the early stage, IgA class alone, IgM class alone, and both IgA and IgM classes of antibodies were detected in nine AIC patients, whereas these classes of antibodies were not detected in PBC patients. Positive results for IgM class anti-m2 were significantly Table 2. Laboratory findings in PBC and AIC Normal AIC (n 23) PBC (n 71) Finding range mean SD mean SD Significance* Total-Bilirubin P 0.05 (mg/dl) ALP (IU/l) P 0.01 AST (IU/l) NS ALT (IU/l) NS γ-gtp (IU/l) NS Total cholesterol P 0.05 (mg/dl) IgG (mg/ml) NS IgA (mg/ml) NS IgM (mg/ml) P 0.01 * Significance was determined by Wilcoxon s rank-sum test, as appropriate NS, Not significant at P 0.05; AMA, antimitochondrial antibody; n, number of subjects; ALP, alkaline phosphatase; AST, aspartate aminotransferase; ALT, alanine aminotransferase; γ-gtp, γ-glutamyl transpeptidase
4 610 M. Nakajima et al.: Subclasses of anti-m2 antibody and autoimmune cholangitis Fig. 1. Results of anti-m2 antibody determined by immunoblotting. Western immunoblot showing reactivity of sera of an AMA( ) PBC patient as the positive control and three autoimmune cholangitis (AIC) patients with beef heart mitochondria prepared as described in Methods. Control sera reacted with each of four M2 antigens in all immunoglobulin subclasses. Whereas the serum of patient 1 reacted with 47 kd only in the IgG immunoglobulin subclass, the serum of patient 2 reacted with 47kD only in the IgA immunoglobulin subclass, and the serum of patient 3 reacted with 47 kd only in the IgM immunoglobulin subclass Table 3. The pattern of anti-m2 antibody for the IgG, IgA, and IgM subclasses determined by immunoblotting Immunoglobulin class AIC (n 23) PBC (n 71) Significance* IgG 11 (48%) 71 (100%) P 0.01 IgG alone 7 (30%) 7 (10%) P 0.05 IgA alone 3 (13%) 0 (0%) P 0.05 IgM alone 4 (17%) 0 (0%) P 0.01 IgG and IgA 0 (0%) 5 (7%) NS IgG and IgM 2 (9%) 13 (18%) NS IgA and IgM 5 (22%) 0 (0%) P 0.01 IgG, IgA, and IgM 2 (9%) 46 (65%) P 0.01 Total 23 (100%) 71 (100%) * Significance was determined by Fisher s exact test NS, Not statistically significant at P 0.05; AIC, autoimmune cholangitis; AMA, antimitochondrial antibody; PBC, primary biliary cirrhosis; n, number of subjects IgG: IgG alone (IgG IgA) (IgG IgM) (IgG IgA IgM) Table 4. The number of stage 1 2 (Sheuer s classification) patients with AIC and PBC in each of the immunoglobulin classes determined by immunoblotting Immunoglobulin class AIC (n 23) PBC (n 71) Significance* Histological stage 1 2 n 18 n 28 P 0.01 IgG 9 28 P 0.01 IgG alone 5 3 NS IgA alone 3 0 NS IgM alone 4 0 P 0.05 IgG IgA 0 2 NS IgG IgM 2 7 NS IgA IgM 2 0 NS IgG IgA IgM 2 16 P 0.01 Stages were determined using Sheuer s classification, and immunoblotting was performed as described in Methods Significance was determined by Fisher s exact test NS, Not statistically significant at P 0.05; n, number of subjects; AIC, autoimmune cholangitis; PBC, primary biliary cirrhosis; IgG, immunoglobulin G; IgA, immunoglobulin A; IgM, Immunoglobulin M IgG:IgG alone (IgG IgA) (IgG IgM) (IgG IgA IgM)
5 M. Nakajima et al.: Subclasses of anti-m2 antibody and autoimmune cholangitis 611 more frequent in AIC patients than in PBC patients in the early stage. Discussion Since Brunner 10 reported immunocholangitis, a number of cases of PBC without AMA have been reported, 11,13 and these cases have been termed immunocholangitis, autoimmune cholangiopathy, or AIC. Notably, Michieletti 12 proposed that a syndrome was distinct from PBC because they had significantly higher ASMA and lower IgM and aspartate aminotransferase than AMA-positive patients in addition AMA-negative and ANA-positive, and he termed this syndrome AIC. However, histological examination by these authors revealed no significant differences between AIC and AMA-positive PBC patients. Originally, Bruner 10 and Ben-Ari 11 reported that AIC patients achieved remission on prednisolone with or without azathioprine. However, recently the effectiveness of immunosuppressive therapy has become less important in distinguishing AIC and PBC. 25,26 Therefore, differences between AIC and AMA-positive PBC cannot be determined on the basis of clinical and histological findings; now only serological findings can distinguish AIC from PBC. In this study, we identified 23 patients with clinical and histological PBC whose serum was negative for AMA by IF and anti-m2 antibody by ELISA and positive for ANA ( 1:80); these patients formed our AIC group. These patients showed characteristics of AIC, such as more frequent detection of ASMA and lower serum IgM concentrations. Furthermore, they showed the other characteristics of significantly lower ALP, total bilirubin, and total cholesterol values. With respect to histological findings, 18 of 23 in our AIC group were classified as early stage, and Michieletti reported 9 of 17 AIC patients without fibrosis. Therefore, it is possible that early-stage PBC patients were included frequently in our AIC group. Anti-M2 was detected by immunoblotting in all our AIC patients; however, the pattern of anti-m2 for the immunoglobulin classes was different from that found in PBC patients. The pattern of anti-m2 antibody expression was different in individual patients with AIC and PBC; IgG class anti-m2 antibody was detected in all PBC patients, whereas IgM alone, IgA alone, and both IgA and IgM classes of anti-m2 antibody were detected more frequently in AIC patients. Indeed, early-stage histology was found significantly more frequently in AIC patients who had IgM anti-m2 antibody alone, and none of the AIC patients had levels of total bilirubin higher than 2 mg/dl. Therefore, it is suggested that the patients in our AIC group have early-stage PBC. Secretory IgA is the predominant immunoglobulin of the mucosal immune system, and IgA is the major protein in bile. Nishio et al. 27 found mitochondrial autoantigens and AMA in bile. They hypothesized that during transport through the bile duct epithelial cells, IgA class AMA in PBC might bind to mitochondrial antigens, thereby causing cytotoxicity by inhibiting key metabolic pathways. In this study, AIC patients in whom the IgA class anti-m2 antibody was detected were all included in early stage. Therefore, we considered that the mucous immune system, including scretory IgA, might be related to the pathogenesis of PBC and AIC. While, all of the 4 patients in whom only the IgM class of anti-m2 antibody was detected were also early stage. As in a normal immune response to viral infection, IgM class anti-m2 antibody may appear at first and switch to IgG class anti-m2 antibody. However, IgM class antibody did not disappear in the late stage of PBC, and these patients had elevated levels of serum IgM. The continued presence of IgM may result the failure of IgM to switch to IgG class antibody. 28 Mattalla et al. reported that AMA reactivity was primarily detected IgM and IgA class. 29 It may support our result in which IgM and IgA was more frequently detected in AIC patients whom we consider as early PBC. Flora et al. reported that eight patients without AMA and with ANA or ASMA categorized as AIC developed PBC when AMA became positive. They stated that the autoimmune marker alone distinguishes AIC as an early-stage variant within the spectrum of nonsuppurative destructive cholangitis, which usually presents as classic PBC. 30 In this study, it is suggested that AIC is an early stage of PBC with the IgG class of anti-m2 antibody absent in the serum. In conclusion, because IgM and IgA and/or IgG classes of anti-m2 antibody were shown to be present by immunoblotting in AIC patients in whom class anti-m2 antibody was not detected by ELISA, it is suggested that AIC is not a distinct disease from PBC. Therefore, it is recommended that to diagnose AIC and/ or PBC, anti-m2 antibody should be examined by the immunoblotting assay to detect not only IgG but also IgA and IgM subclasses. Acknowledgments. We thank Toshikazu Saeki of Komagome Hospital and Eiji Harada of National Tokyo Hospital, Tokyo, Japan for donating PBC sera. References 1. Walker JG, Doniach D, Roitt IM, et al. Serological test in diagnosis of primary biliary cirrhosis. Lancet 1965;I: Klatskin G, Kantor FS. Mitochondrial antibody in primary biliary cirrhosis and other diseases. Ann Intern Med 1972;77: Berg PA, Kein R, Lindenborn-Fotinos J. Antimitochondrial antibodies in primary biliary cirrhosis. J Hepatol 1986;2:
6 612 M. Nakajima et al.: Subclasses of anti-m2 antibody and autoimmune cholangitis 4. Fussey SPM, Guest JR, James OFW, et al. Identification and analysis of the major M2 autoantigens in primary biliary cirrhosis. Proc Natl Acad Sci USA 1988;85: Coppel RL, McNeilage J, Surh CD, et al. Primary structure of the human M2 mitochondrial autoantigen of primary biliary cirrhosis: dihydrolipoamide acetyltransferase. Proc Natl Acad Sci USA 1988;85: Ruth EJ, Gerald DJ, John BM, et al. Distribution of pyruvate dehydrogenase dihydrolipoamide acetyltransferase (PDH-E2) and another mitochondrial marker in salivary gland and biliary epithelium from patients with primary biliary cirrhosis. Hepatology 1994;19: Provenzano G, Diquttro O, Croxi A, et al. Immunoblotting as a confirmatory test for antimitochondrial antibody in primary biliary cirrhosis. Gut 1993;34: Kitami N, Komada T, Ishii H, et al. Immunological study of anti- M2 in mitochondrial antibody-negative primary biliary cirrhosis. Intern Med 1995;34: Kitami N, Ishii H, Shimizu H, et al. Immunoreactivity to M2 protein in antimitochondrial antibody-negative patients with primary biliary cirrhosis. J Gastroenterol Hepatol 1994;9: Brunner G, Klinge O. A cholangitis with antinuclear antibodies (immunocholangitis) resembling chronic nonsuppurative destructive cholangitis. Dtsch Med Wochenschr 1987;112: Ben-Ari Z, Dhillon AP, Sherlock S. Autoimmune cholangiopathy: part of the spectrum of autoimmune chronic active hepatitis. Hepatology 1993;18: Michieletti P, Wanless IR, Katz A, et al. Antimitochondrial antibody-negative primary biliary cirrhosis: a distinct syndrome of autoimmune cholangitis. Gut 1994;35: Colombato LA, Alvarez F, Cote J, et al. Autoimmune cholangiopathy: the result of consecutive primary biliary cirrhosis and autoimmune hepatitis? Gastroenterology 1994;107: Leevy CM, Tygstrup N. Standardisation and nomenclature, diagnostic criteria and diagnostic methodology for disease of liver and biliary tract. In: Leevey CM editor. Proc IV Quadr Meeting International Association Study of Liver, Acapulco, Mexico, Basel: Karger; Scheuer PJ. Primary biliary cirrhosis. In: Liver biopsy interpretation. 3rd ed. London: Balliere Tindal; 1980.p Stanley CJ, Perham RN. Purification of 2-oxo acid dehydrogenase multienzyme complexes from ox heart by new methods. Biochem J 1980;191: Nagai S, Manna M, Meyer zum Buschenfelde K-H, et al. Detection of mitochondrial antibodies directed against the primary billiary cirrhosis (M2) antigen by enzyme-linked immunosorbent assay (ELISA). J Immunol Methods 1983;60: Kaplan MM, Gandolfo JV, Quaroni EG. An enzyme-linked immunosorbent assay (ELISA) for detecting antimitochondrial antibody. Hepatology 1984;4: Schneider WC, Hogeboom GH. Intracellular distribution of enzyme: further studies on distribution of cytochrome in rat liver homogenate. J Biol Chem 1950;183: Schnaitman C, Greenawalt JW. Enzymatic properties of the inner and outer membranes of rat liver mitochondria. J Cell Biol 1986;38: Ishii H, Saifuku K, Namihisa T. Multiplicity of mitochondrial inner membrane antigens from beef heart reacting with antimitochondrial antibodies in sera of patients with primary biliary cirrhosis. Immunol Lett 1985;9: Laemmli UK. Cleavage of structural proteins during assembly of the head of bacteriophage T4. Nature 1970;227: Towbin H, Staehelin T, Gordon J. Electrophoretic transfer of proteins from polyacrylamide gels to nitrocellulose sheets: procedure and some applications. Proc Natl Acad Sci USA 1979;76: Ishii H, Saifuku K, Namihisa T. Reactivities and clinical relevance of antimitochondrial antibodies to four mitochondrial inner membrane proteins in sera of patients with primary biliary cirrhosis. Hepatology 1987;7: Taylor SL, Culp KS, Fleming CR, et al. Autoimmune association in primary biliary cirrhosis. Mayo Clin Proc 1982;57: Kim WR, Poterucha JJ, Jorgensen RA, et al. Does antimitochondrial antibody status affect response to treatment in patients with primary biliary cirrhosis? Outcome of ursodeoxycholic acid therapy and liver transplantation. Hepatology 1997; 26: Nishio A, Van de Water J, Leung PSC, et al. Comparative study of antimitochondrial autoantibodies in sera and bile in primary biliary cirrhosis. Hepatology 1997;25: Thomas HC, Holden R, Verrier JJ, et al. Immune response to FX 174 in man 5. Primary and secondary antibody production in primary biliary cirrhosis. Gut 1976;17: Mattalia A, Quaranta S, Leung PSC, et al. Characterization of antimimitochondrial antibody in healthy adult. Hepatology 1998;27: Flora K, Benner K, Lee R, et al. Primary autoimmune cholangitis as a variant of primary biliary cirrhosis (abstract). Hepatology 1994;20:152A 30.
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