metricas
covid
Buscar en
Annals of Hepatology
Toda la web
Inicio Annals of Hepatology Evaluation of liver diseases in Iranian patients with primary antibody deficienc...
Información de la revista
Vol. 8. Núm. 3.
Páginas 196-202 (julio - septiembre 2009)
Compartir
Compartir
Descargar PDF
Más opciones de artículo
Visitas
1103
Vol. 8. Núm. 3.
Páginas 196-202 (julio - septiembre 2009)
Open Access
Evaluation of liver diseases in Iranian patients with primary antibody deficiencies
Visitas
1103
Farzaneh Motamed*, Asghar Aghamohammadi
,,
Autor para correspondencia
aghamohammadi@sina.tums.ac.ir

Correspondence and reprint request
, Mahmoud Soltani*, Mahboubeh Mansouri§, Nima Rezaei*,, Shahram Teimourian,, Nima Pouladi, Sina Abdollahzadeh, Nima Parvaneh*,
* Pediatrics Center of Excellence, Children’s Medical Center, Tehran University of Medical Sciences, Tehran, Iran.
Growth and Development Research Center, Tehran University of Medical Sciences, Tehran, Iran.
Pasteur Institute of Iran, Tehran, Iran.
§ Mofid Hospital, Shahid Beheshti University of Medical Sciences, Tehran, Iran.
Students’ Scientific Research Center, Tehran University of Medical Sciences, Tehran, Iran.
Este artículo ha recibido

Under a Creative Commons license
Información del artículo
Resumen
Texto completo
Bibliografía
Descargar PDF
Estadísticas
Figuras (1)
Tablas (4)
Table 1.. Laboratory parameters in patients with primary antibody deficiencies.
Table 2.. Diagnostic parameters in patients with primary antibody deficiencies.
Table 3.. Liver involvement in antibody deficient patients.
Table 4.. Clinical features of primary antibody deficient patients with chronic liver disease.
Mostrar másMostrar menos
Abstract

Introduction. Patients with primary antibody deficiency (PAD) can complicate with liver disease. This study was performed in order to study the prevalence and causes of hepatobiliary diseases in Iranian patients with PAD.

Material and methods. Sixty-two patients with PAD were followed-up and signs and symptoms of liver disease were recorded. All patients were screened for hepatitis C virus (HCV-RNA) and those patients with any sign of liver disease or gastrointestinal complaints were tested for Cryptosporidium parvum.

Results. Clinical evidences of liver disease, including hepatomegaly, were documented in 22 patients (35.5%). Eight patients (13%) had clinical and/or laboratory criteria of chronic liver disease. Only one patient was HCV-RNA positive; he had stigmata of chronic liver disease and pathologic evidence of chronic active hepatitis with cirrhosis. Cryptosporidium parvum test was positive for one patient with hyper-IgM syndrome. In liver biopsy of patients with liver involvement, one had histological findings related to sclerosing cholangitis, and five had mild to moderate chronic active hepatitis with unknown reason.

Conclusions. Chronic active hepatitis is the most common pathologic feature of liver injury in Iranian patients with PAD. Liver disease in PAD usually accompanies with other organ involvements and could increase the mortality of PAD. Whether this high rate of liver disease with unknown origin (75%) is the result of an unidentified hepatotropic virus or other mechanisms such as autoimmunity, is currently difficult to understand.

Key words:
Liver disease
Primary antibody deficiency
HCV infection
Chronic active hepatitis
Texto completo
Introduction

Primary immunodeficiency diseases (PID) include a heterogeneous group of disorders that render the host to be susceptible to a wide set of infections. Primary antibody deficiencies (PAD) are the most common forms of PID in human,1-3 with a wide spectrum, ranging from severe reduction of all serum immunoglobulins with absence of B cells to a selective antibody deficiency with normal serum immunoglobulins.4 Failure of antibody production in PAD patients causes chronic and recurrent bacterial infections most notably in respiratory and gastrointestinal tracts.5-11

Delay in diagnosis and inadequate treatment cause severe complications and irreversible organ damages resulting in increased morbidity and mortality,12-19 while early diagnosis and use of immunoglobulin replacement therapy reduce serious bacterial infections in these group of patients.13,20-22

Liver involvement either may be a clinical manifestation or considered as a life threatening complication of primary immunodeficiencies. The incidence of liver disease (LD) in all types of PID varies from 18 to 55% in several documented studies.14-16,23,24 Hepatobiliary complications range from mild biochemical abnormalities to end-stage liver disease and mainly caused by hepatotropic viruses (HCV),25-28Cryptosporidiumparvum29 and autoimmunity.30

In the present study, we described the spectrum of hepatobiliary disorders in a large group of well-characterized Iranian patients with primary antibody deficiencies. The aim of this study was to investigate the mode of presentation, clinical features, etiology, and the outcome of liver disease among patients with primary antibody deficiencies.

Material and MethodsSubjects

Sixty-two patients with PAD whom were diagnosed and followed up during a 20 years period (19852006) were enrolled in this study.

The diagnosis of primary antibody deficiency was based on diagnostic criteria of PAGID (the Pan-American Group for Immunodeficiency) and ESID (the European Society for Immunodeficiencies).31 The diagnosis of patients with X-linked agammaglobulinemia (XLA) and hyper-IgM syndromes (HIGM) has been confirmed by mutation analysis.

All patients had been routinely screened for infectious and non-infectious related complications periodically during their follow up. Concerning liver disease, this screening included serum concentrations of aminotransaminases (ALT, AST), alkaline phosphatase (ALP), bilirubin, albumin and coagulation tests (PT, PTT), that were performed at least twice yearly.

Study Design

During the current study period (May 2005 until September 2006), alive patients were investigated with focus on clinical and laboratory features of liver involvement. A questionnaire was designed that included the demographic data, the diagnosis, age at onset, diagnostic delay, and the results of clinical and laboratory findings.

The liver injury documented based on, at least two-fold increase of serum levels of aminotransferases (ALT, AST). Chronicity was defined with persistent elevation of aminotransferases for at least six months or presence of chronic liver disease stigmata such as stiffness and nodularity of liver, or enlargement of left liver lobe, clubbing, palmar erythema and spider angioma, at the first examination.14,16,32

Screening the Hepatitis C Virus

All patients (except P4 who was not alive during the time of study) were screened for hepatitis C virus (HCV) infection using HCV-PCR technique described in detail elsewhere.33,34 HCV cDNA was obtained by reverse transcription from HCV mRNA using the synthetic primer NCR2 located in the highly conserved 5’ non-coding region of the HCV genome.

Screening of Cryptosporidium parvum

The screening of Cryptosporidium parvum in stool specimens was performed in patients with any sign of liver disease or gastrointestinal complaints. This screening was based on detection of oocysts by light microscopy (with modified Ziehl-Neelsen staining), and was documented with PCR modality.29

Other Investigations

We looked for other causes of liver involvement (autoimmune hepatitis, HBV infection, CMV infection, primary biliary disease, metabolic liver disease, obesity, drug induced hepatitis and malignancies) if the results of screening for HCV and C. parvum were negative. None of the patients had signs of any systemic infections at the time of study.

Abdominal ultrasound exam and percutaneous liver biopsy under sedation were performed in the presence of chronic liver disease stigmata at the first examination, positive result for HCV infection, or at least two-fold increase of serum levels of aminotransferases (ALT, AST) for over six months.

Magnetic Resonance Cholangiopancreatography (MRCP) performed if the patient had C. parvum in stool or dilatation of biliary system on ultrasonography to rule out the sclerosing cholangitis.

Statistical Methods

Statistical analysis was performed using the chisquare test. Survival curve was illustrated according to the Kaplan-Meier method.

ResultsPatients’ Characteristics

Sixty-two patients with PAD, including: 38 patients with common variable immunodeficiency (CVID), 19 with XLA and five with HIGM, were introduced. There were 48 males and 14 females; the median age of patients was 10.3 years (range 2-56). Forty six patients (75%) were under 18 years. Patients were followed-up for a mean of five years (range 0.2-19 years).

Baseline laboratory findings, including serum immunoglobulin levels and immunophenotyping of peripheral blood lymphocytes, are summarized in the table 1.

Table 1..

Laboratory parameters in patients with primary antibody deficiencies.

Laboratory Parameters  Normal range  CVIDXLAHyper IgM
    Median  (Range)  Median  (Range)  Median  (Range) 
Immunoglobulins (mg/dL)               
IgG  800-1,800  121 (0-500)  100  (0-700)  135  (0-460)   
IgA  90-145  6.5  (0-220)  (0-30)  17  (0-420) 
IgM  80-300  15  (0-230)  10  (0-76)  625  (540-1,260) 
Cellular Count               
WBC  4,000-10,000  6,757  (1,310-15,100)  8,200  (2,800-22,700)  4,850  (2,500-5,800) 
Lymphocyte (%)  25-35  36.5  (15.7-96)  42  (4-79)  44  (10-66) 
Lymphocyte Markers (%)               
CD3  65-95  72.8  (38.42-99)  91.6  (30-97)  61  (43-84) 
CD4    31  (4.5-68.37)  44  (16.3-93.62)  30  (20-40) 
CD8    35.08  (18-73)  33  (17-75)  40.5  (12-52) 
CD19  3-25  10  (2-33)  0.5  (0-2)  14  (8.9-19) 
CD4/CD8 ratio    0.9  (0.16-3.47)  1.37  (0.22-3.54)  0.74  (0.38-3.33) 
Liver Enzymes(IU/L)               
AST  5-42  22  (9-251)  16  (0.12-148)  29  (17-34) 
ALT  5-40  22.5  (9-147)  21  (8-138)  31  (12-42) 

The time elapsed between onset of clinical symptoms and diagnosis of antibody deficiency (diagnostic delay) was 39 months for CVID, 24 months for XLA, and 36 months for HIGM. Age at onset of disease, diagnostic age, delay in diagnosis, follow up period and current age of patients are recorded in the table 2.

Table 2..

Diagnostic parameters in patients with primary antibody deficiencies.

Diagnosis  CVIDXLAHyper IgM
  Median (Years)  (Range)  Median (Years)  (Range)  Median (Years)  (Range) 
Age at the time of onset  (0.5-46)  0.5  (0.2-6)  (0.5-7) 
Age at the time of diagnose  6.5  (2-54)  (0.5-15.5)  (2-25) 
Age at the time of enrolment  14  (2-56)  11  (2.5-29)  (0.6-29) 
Diagnostic delay  3.3  (0.5-39)  (0.17-15)  (0.8-18) 
Follow-up  4.5  (0.25-18)  7.5  (0.5-19)  (1-13) 

Patients received intravenous immunoglobulin for mean period of 5.2 years (range: 2-19 years). Twenty-one patients (34%) had received other products of blood such as packed red blood cells, platelet or fresh frozen plasma. The prevalence of blood product transfusion was not significantly different (P value > 0.05) in each type of PID (Table 3).

Table 3..

Liver involvement in antibody deficient patients.

Patients’ Medical History  CVID  XLA  Hyper IgM  Total 
  (38)  (19)  (5)  (62) 
Clinical signs of liver involvement  15 (40%)  2 (10.5%)  5 (100%)  22 (35.5%) 
Pathologic features of liver disease  6 (15.7%)  1 (5%)  1 (20%)  8 (13%) 
History of blood product transfusion  13 (34.2%)  7 (36.8%)  1 (20%)  21 (34%) 
Liver Disease

Among 62 studied patients, 22 patients (35.5%) had clinical features in favor of chronic liver disease, including hepatomegaly. These patients include five HIGM (100%), 15 CVID (40%) and two XLA (10.5%) patients (Table 3). Percutaneous liver biopsy was performed that revealed abnormalities in eight of them (13%) (Table 4).

Table 4..

Clinical features of primary antibody deficient patients with chronic liver disease.

No  Diagnosis  Age /Sex (years)  Physical Examination  Histologic Findings  Other accompanying morbidities and current status 
P1  CVID  20 / Female  Purpura, Clubbing, Hepatosplenomegaly  Chronic Active Hepatitis, Cirhosis  NLH, Anemia, Rise of ESR/ Alive 
P2  CVID  27 / Male  Ascitis Hepatosplenomegaly  Reactive Hepatitis, Cirhosis  Positive HCV PCR, Bronchiectasia/Alive 
P3  CVID  18 /Male  Clubbing Hepatosplenomegaly  Chronic Active Hepatitis  Ulcerative collitis/Died due to hepatic failure 
P4  CVID  17 / Male  Hepatosplenomegaly  Sclorising Cholangitis  ITP, Neutropenia, Esophageal Varices grade 2/ Died due to hepatic failure 
P5  CVID  7 / Male  Hepatosplenomegaly  Chronic Active Hepatitis  Alive 
P6  HIM  17 / Female  Clubbing Hepatosplenomegaly  Chronic Active Hepatitis  Evance Syndrome, IBD/Alive 
P7  XLA  24 / Male  Hepatosplenomegaly  Chronic Active Hepatitis  Dermatomyosit Like Syndrome/Died due to retroviral encephalitis 
P8  CVID  6 / Male  Hepatosplenomegaly  Not Given  CVA/ Alive 

NLH: Nodular lymphoid hyperplasia. ESR: Erythrocyte sedimentation rate. IBD: Inflamatory bowel disease. ITP: Immune-mediated thrombocytopenic purpura. CVA: Cerebrovasculare accident.

Inflammatory bowel diseases (P3, P6), other autoimmune diseases (P1, P4, P6, P7), and bronchiectasis (P2) were common in this group of patients, while other patients did not experience such manifestations (Table 4).

The presences of liver abscess, liver mass or any sign of fatty liver were excluded by abdominal ultra-sonography.

Laboratory Studies

Elevations of amino transaminases (ALT, AST) were found in 10 patients (16%). This rising was transient in four patients (whom were negative for HCV RNA). Two of them were considered as drug-induced hepatitis. The enzyme levels became normal after discontinuation of the drug (clarithromycin) and no other etiology was detected in them. Six patients had persistent (above six months) elevated levels of serum amino transaminases (mean for ALT: 159 IU/L and for AST: 109 IU/L) (Table 4).

HCV infection was detected only in one patient who had CVID and suffered from end stage liver disease (P2). All patients were negative for HBsAg.

In examination of stool, only one patient with HIGM due to CD40-ligand deficiency was positive for C. parvum. This patient had hydrops of gall bladder in ultrasonography but he was asymptomatic with normal liver enzymes. Sclerosing cholangitis ruled out using MRCP in this patient.

Further Details

In general, pathologically proved liver disease was found in eight out of 62 patients (13%) with median age of 15 years. All of them had abnormal clinical examination in favor of liver disease, six patients had persistent elevation of amino transaminases (ALT, AST) and two patients had normal level of liver enzymes. These later two patients (P2, P6) had history of increased level of amino transaminases (ALT, AST) since some years ago and had palmar erythema, clubbing and ascites due to chronic liver dysfunction in first clinical examination (Table 4).

Among the eight patients with proved liver diseases, seven patients underwent percutaneous liver biopsy. The remaining one patient declined liver biopsy. The microscopic evaluation of liver biopsies showed mild to moderate chronic active hepatitis in five patients, which were not compatible with any specific etiology. One patient (P4) had histological evidences of sclerosing cholangitis and died due to severe hepatic insufficiency. In remaining patient (P2) with HCV infection, liver biopsy had been performed four years before our study, and showed reactive hepatitis with fibrosis indicating liver cirrhosis. This patient developed esophageal varices grade n, end stage liver disease, and cachexia.

As it has been shown in table 4, the known causes of liver disease were hepatitis C infection (P2) and sclerosing cholangitis (P4). In remaining six patients, no etiology were found (75%). There was no meaningful relationship between liver involvement and type of primary antibody deficiency.

The cumulative survival within patients with primary antibody deficiency based on liver involvement is shown in figure 1. Among eight patients who complicated with liver disease, three (37.5%) died during their follow-up.

Figure 1.

Cumulative survival within patients with primary antibody deficiency divided based on liver involvement.

(0.04MB).
Discussion

The incidence of liver involvement in patients with primary immunodeficiency varies from 18% to 55%14,32 and its severity ranging from mild biochemical abnormalities to end-stage hepatic failure.14-16,23,35,36 In our current study, the prevalence of liver diseases in 62 patients with primary antibody deficiency was 13%, which supports previous studies.

Fiore M, et al.15 in 1998 studied 30 Italian children (> 16 years) with PID (T cell, B cell and combined immunodeficiency). Their study showed that 11 patients (36.8%) had liver disease including 10 patients with T-cell and one with B-cell (CVID) deficiency. Also in another study which was performed by an American group,16 among the 147 patients with PID (> 18 years), 35 patients (26%) were detected to have liver involvement. The most common type of PID was combined immunodeficiency syndrome (14 out of 35), in the reported study. All these data show that the involvement of liver in patients with T-cell and combined immunodeficiencies is more common and more severe comparing with primary antibody deficiencies.37

HCV infection was a major cause of liver disease in hypogammaglobulinemic patients in the past. Between February and July of 1994, 112 cases of hepatitis C infection associated with the use of infected IVIG were reported to the CDC,27 as well as some reports from Europe.25,32 Recent data clearly show that most immunoglobulin preparations are acceptably safe, at least with regard to HIV, HBV and HCV transmission,38 as we found only one patient infected with hepatitis C.

Our data provide evidence that a remarkable number of patients with primary antibody deficiency have liver disease unrelated to the common hepatotropic pathogens (Table 4).

Previous reports showed that sclerosing cholangitis (SC) is a common feature of liver involvement associated with immune disorders.23,24,39,40C. parvum had been implicated in the development of SC in HIV infection and in other immunocompromised patients, in particular, in those with X-linked HIGM syndrome.35,36 In our study, C. parvum infection was found in one patient. This patient had X-linked HIGM syndrome, was asymptomatic and had no laboratory and radiological evidence of sclerosing cholangitis and treated with azythromycin. The low incidence of C. parvum infection in our study could be due to geographical situations and good care of patients.

The rising of serum amino transaminases (ALT, AST) is characteristic of liver involvement. The level of this rising indicates the severity of hepatocellular injury.41 Based on results of our study and those from others,14-16,32,42 persistent elevation of liver enzymes in patients with primary antibody deficiency, above two times greater than normal, is an indicator of liver involvement and can be the first sign of an unknown progressive systemic disease. Chronic active hepatitis with unknown origin was the most common feature of liver injury in our series (75%). Because of high incidence of liver involvement, it is advised to perform a biochemical liver profile, including serum concentrations of amino transaminases must be performed at least twice yearly in all patients with primary antibody deficiency.43

The presence of autoantibodies like smooth muscle antibody (SMA) is usual in PID specially in T-cell deficiencies that can reflect dysregulation in immune system and may involve the liver.5,14,16,30,44 Triggering of autoimmune inflammatory processes by hepatotropic viruses is one possible mechanism by which such chronic liver disease may develop.14,44 Since in primary antibody deficiencies, production of antibodies is impaired, we cannot detect autoantibodies in these patients. High incidence of other co-morbidities such as bone marrow suppression, autoimmune cytopenias, inflammatory bowel diseases and dermatomyositis like syndrome can propose that a systemic autoimmune process is present.

More investigations are needed to determine etiology of this high prevalence of unexplained liver disease (75%) and unknown progressive systemic disease. Interestingly, the survival of PAD patients with liver involvement seems to be less than that of patients who do not have this complication. Application of preventive measures and beginning of timely therapy for this complication could lead to increased life span of PAD patients.

Other reports revealed that approximately 10 to 23% of adult patients with some types of primary immunodeficiency have unexplained liver diseases.14,15,32 Chronic active hepatitis is the most common pathologic feature of liver injury in our patients with primary antibody deficiency (five from seven patients). Whether this high prevalence of liver disease with unknown origin (75%) is the result of an unidentified hepatotropic virus or other mechanisms such as autoimmunity, is currently difficult to understand.

Acknowledgments

This study was supported by a grant from Tehran University of Medical Sciences and Immunology, Asthma and Allergy Research Institute.

The authors wish to thank all the patients, their families and the Iranian Primary Immunodeficiency Association (IPIA) for their kind collaboration in this research project. We are also grateful to Dr. Memar, Dr. Jannati, Dr. Arshi, Ms. Akbarzadeh, and Ms. Faridoni and the staff of the Department of Allergy and Clinical Immunology, Tehran University of Medical Sciences.

References
[1.]
Aghamohammadi A,, Moein M,, Farhoudi A,, Pourpak Z,, Rezaei N,, Abolmaali K,, et al.
Primary immunodeficiency in Iran: first report of the National Registry of PID in Children and Adults..
J Clin Immunol, 22 (2002), pp. 375--80
[2.]
Knerr V,, Grimbacher B..
Primary immunodeficiency registries..
Curr Opin Allergy Clin Immunol, 7 (2007), pp. 475--80
[3.]
Rezaei N,, Aghamohammadi A,, Moin M,, Pourpak Z,, Movahedi M,, Gharagozlou M,, et al.
Frequency and clinical manifestations of patients with primary immunodeficiency disorders in Iran: update from the Iranian Primary Immunodeficiency Registry..
J Clin Immunol, 26 (2006), pp. 519--32
[4.]
Notarangelo L,, Casanova JL,, Fischer A,, Puck J,, Rosen F,, Seger R,, Geha R..
Primary immunodeficiency diseases: An update..
Journal of Allergy & Clinical Immunology, 114 (2004), pp. 677--87
[5.]
Cunningham-Rundles C,, Bodian C..
Common variable immunodeficiency: clinical and immunological features of 248 patients..
Clin Immunol, 92 (1999), pp. 34--48
[6.]
Lederman HM,, Winkelstein JA..
X-linked agammaglobulinemia: an analysis of 96 patients..
Medicine (Baltimore), 64 (1985), pp. 145--56
[7.]
Aghamohammadi A,, Farhoudi A,, Moin M,, Rezaei N,, Kouhi A,, Pourpak Z,, et al.
Clinical and immunological features of 65 Iranian patients with common variable immunodeficiency..
Clin Diagn Lab Immunol, 12 (2005), pp. 825--32
[8.]
Moin M,, Aghamohammadi A,, Farhoudi A,, Pourpak Z,, Rezaei N,, Movahedi M,, et al.
X-linked agammaglobulinemia: a survey of 33 Iranian patients..
Immunol Invest, 33 (2004), pp. 81--93
[9.]
Hermaszewski RA,, Webster AD..
Primary hypogammaglobulinaemia: a survey of clinical manifestations and complications..
Q J Med, 86 (1993), pp. 31--42
[10.]
Farhoudi A,, Aghamohammadi A,, Moin M,, Rezaei N,, Pourpak Z,, Movahedi M,, et al.
Distribution of primary immunodeficiency disorders diagnosed in the Children’s Medical Center in Iran..
J Investig Allergol Clin Immunol, 15 (2005), pp. 177--82
[11.]
Aghamohammadi A,, Moazzami K,, Rezaei N,, Karimi A,, Movahedi M,, Gharagozlou M,, et al.
ENT manifestations in Iranian patients with primary antibody deficiencies..
J Laryngol Otol, 122 (2008), pp. 409--13
[12.]
Aghamohammadi A,, Parvaneh N,, Tirgari F,, Mahjoob F,, Movahedi M,, Gharagozlou M,, et al.
Lymphoma of mucosa-associated lymphoid tissue in common variable immunodeficiency..
Leuk Lymphoma, 47 (2006), pp. 343--6
[13.]
Aghamohammadi A,, Pouladi N,, Parvaneh N,, Yeganeh M,, Movahedi M,, Gharagolou M,, et al.
Mortality and morbidity in common variable immunodeficiency..
J Trop Pediatr, 53 (2007), pp. 32--8
[14.]
Bjoro K,, Haaland T,, Skaug K,, Froland SS..
The spectrum of hepatobiliary disease in primary hypogammaglobulinaemia..
J Intern Med, 245 (1999), pp. 517--24
[15.]
Fiore M,, Ammendola R,, Gaetaniello L,, De Felice C,, Iorio R,, Vegnente A,, et al.
Chronic unexplained liver disease in children with primary immunodeficiency syndromes..
J Clin Gastroenterol, 26 (1998), pp. 187--92
[16.]
Rodrigues F,, Davies EG,, Harrison P,, McLauchlin J,, Karani J,, Portmann B,, et al.
Liver disease in children with primary immunodeficiencies..
J Pediatr, 145 (2004), pp. 333--9
[17.]
Seymour B,, Miles J,, Haeney M..
Primary antibody deficiency and diagnostic delay..
J Clin Pathol, 58 (2005), pp. 546--7
[18.]
Khodadad A,, Aghamohammadi A,, Parvaneh N,, Rezaei N,, Mahjoob F,, Bashashati M,, et al.
Gastrointestinal manifestations in patients with common variable immunodeficiency..
Dig Dis Sci, 52 (2007), pp. 2977--83
[19.]
Rezaei N,, Aghamohammadi A,, Siadat SD,, Nejati M,, Ahmadi H,, Moin M,, et al.
Serum bactericidal antibody response to serogroup C polysaccharide meningococcal vaccination in children with primary antibody deficiencies..
Vaccine, 25 (2007), pp. 5308--14
[20.]
Aghamohammadi A,, Moin M,, Farhoudi A,, Rezaei N,, Pourpak Z,, Movahedi M,, et al.
Efficacy of intravenous immunoglobulin on the prevention of pneumonia in patients with agammaglobulinemia..
FEMS Immunol Med Microbiol, 40 (2004), pp. 113--8
[21.]
Busse Pj,, Razvi S,, Cunningham-Rundles C,, Cunningham-Rundles C..
Efficacy of intravenous immunoglobulin in the prevention of pneumonia in patients with common variable immunodeficiency..
J Allergy Clin Immunol, 109 (2002), pp. 1001--4
[22.]
Chapel HM..
Consensus on diagnosis and management of primary antibody deficiencies. Consensus Panel for the Diagnosis and Management of Primary Antibody Deficiencies..
[23.]
Davis JJ,, Heyman MB,, Ferrell L,, Kerner J,, Kerlan R, Jr.,, Thaler MM..
Sclerosing cholangitis associated with chronic cryptosporidiosis in a child with a congenital immunodeficiency disorder..
Am J Gastroenterol, 82 (1987), pp. 1196--202
[24.]
DiPalma JA,, Strobel CT,, Farrow JG..
Primary sclerosing cholangitis associated with hyperimmunoglobulin M immunodeficiency (dysgammaglobulinemia)..
Gastroenterology, 91 (1986), pp. 464--8
[25.]
Bjoro K,, Froland SS,, Yun Z,, Samdal HH,, Haaland T..
Hepatitis C infection in patients with primary hypogammaglobulinemia after treatment with contaminated immune globulin..
N Engl J Med, 331 (1994), pp. 1607--11
[26.]
Chapel HM,, Christie JM,, Peach V,, Chapman RW..
Five-year follow-up of patients with primary antibody deficiencies following an outbreak of acute hepatitis C..
Clin Immunol, 99 (2001), pp. 320--4
[27.]
Rossi G,, Tucci A,, Cariani E,, Ravaggi A,, Rossini A,, Radaeli E..
Outbreak of hepatitis C virus infection in patients with hematologic disorders treated with intravenous immunoglobulins: different prognosis according to the immune status..
Blood, 90 (1997), pp. 1309--14
[28.]
Yap PL,, McOmish F,, Webster AD,, Hammarstrom L,, Smith CI,, Bjorkander J,, et al.
Hepatitis C virus transmission by intravenous immunoglobulin..
J Hepatol, 21 (1994), pp. 455--60
[29.]
McLauchlin J,, Amar CF,, Pedraza-Diaz S,, Mieli-Vergani G,, Hadzic N,, Davies EG..
Polymerase chain reaction-based diagnosis of infection with Cryptosporidium in children with primary immunodeficiencies..
Pediatr Infect Dis J, 22 (2003), pp. 329--35
[30.]
Knight AK,, Cunningham-Rundles C..
Inflammatory and autoimmune complications of common variable immune deficiency..
Autoimmunity Reviews, 5 (2006), pp. 156--9
[31.]
Zelazko M,, Carneiro-Sampaio M,, Cornejo de Luigi M,, Garcia de Olarte D,, Porras Madrigal O,, Berron Perez R,, et al.
Primary immunodeficiency diseases in Latin America: first report from eight countries participating in the LAGID. Latin American Group for Primary Immunodeficiency Diseases..
J Clin Immunol, 18 (1998), pp. 161--6
[32.]
Webster AD,, Brown D,, Franz A,, Dusheiko G..
Prevalence of hepatitis C in patients with primary antibody deficiency..
Clin Exp Immunol, 103 (1996), pp. 5--7
[33.]
Okamoto H,, Sugiyama Y,, Okada S,, Kurai K,, Akahane Y,, Sugai Y,, et al.
Typing hepatitis C virus by polymerase chain reaction with type-specific primers: application to clinical surveys and tracing infectious sources..
J Gen Virol, 73 (1992), pp. 673--9
[34.]
Garson JA,, Ring C,, Tuke P,, Tedder RS..
Enhanced detection by PCR of hepatitis C virus RNA..
[35.]
Naveh Y,, Mendelsohn H,, Spira G,, Auslaender L,, Mandel H,, Berant M..
Primary sclerosing cholangitis associated with immunodeficiency..
Am J Dis Child, 137 (1983), pp. 114--7
[36.]
Levy J,, Espanol-Boren T,, Thomas C,, Fischer A,, Tovo P,, Bordigoni P,, et al.
Clinical spectrum of X-linked hyper-IgM syndrome..
J Pediatr, 131 (1997), pp. 47--54
[37.]
Rodrigues F,, Davies EG,, Harrison P,, McLauchlin J,, Karani J,, Portmann B,, et al.
Liver disease in children with primary immunodeficiencies..
J Pediatr, 145 (2004), pp. 333--9
[38.]
Quinti I,, Pierdominici M,, Marziali M,, Giovannetti A,, Donnanno S,, Chapel H,, et al.
European surveillance of immunoglobulin safety-results of initial survey of 1243 patients with primary immunodeficiencies in 16 countries..
Clin Immunol, 104 (2002), pp. 231--6
[39.]
Yoshioka R,, Sato Y,, Kogure A,, Ohira H,, Takagi T,, Kuroda M,, et al.
Association of primary sclerosing cholangitis, thymoma and hypogammaglobulinemia..
Liver, 15 (1995), pp. 53--5
[40.]
Gremse DA,, Bucuvalas JC,, Bongiovanni GL..
Papillary stenosis and sclerosing cholangitis in an immunodeficient child..
Gastroenterology, 96 (1989), pp. 1600--3
[41.]
Behrman RE,, Kliegman R,, Jenson HB..
Nelson textbook of pediatrics..
[42.]
Bjoro K,, Skaug K,, Haaland T,, Froland S.S..
Long-term outcome of chronic hepatitis C virus infection in primary hypo-gammaglobulinaemia..
Q J Med, 92 (1999), pp. 433--41
[43.]
Stiehm ER..
Human intravenous immunoglobulin in primary and secondary antibody deficiencies..
Pediatr Infect Dis J, 16 (1997), pp. 696--707
[44.]
Vento S,, Cainelli F,, Renzini C,, Concia E..
Autoimmune hepatitis type 2 induced by HCV and persisting after viral clearance..
Copyright © 2009. Fundación Clínica Médica Sur, A.C.
Descargar PDF
Opciones de artículo
es en pt

¿Es usted profesional sanitario apto para prescribir o dispensar medicamentos?

Are you a health professional able to prescribe or dispense drugs?

Você é um profissional de saúde habilitado a prescrever ou dispensar medicamentos

Quizás le interese:
10.1016/j.aohep.2023.101123
No mostrar más