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Rheumatology 2001; 40: 152-157
© 2001 British Society for Rheumatology

Human parvovirus B19 infection in patients with systemic lupus erythematosus

T.-C. Hsu1 and G. J. Tsay

Department of Medicine and Institutes of Immunology and
1 Medicine, Chung Shan Medical and Dental College, Taichung, Taiwan


   Abstract
Top
 Abstract
Introduction
 Materials and methods
 Results
 Discussion
 References
 
Objective. The clinical significance of the presence of B19 DNA in patients with SLE was studied.

Methods. Sera from 72 patients with systemic lupus erythematosus (SLE), 23 patients with rheumatoid arthritis (RA), 18 patients with Sjögren's syndrome (SS), eight patients with Raynaud's phenomenon (RP), five patients with primary biliary cirrhosis (PBC), five patients with polymyositis (PM), four patients with erythema infectiosum (EI) and 22 normal controls were examined for parvovirus B19 (B19) infection by serological assays, nested PCR and Southern blotting.

Results. Parvovirus B19 DNA was detected in 17 of 72 patients with SLE and in three of four patients with EI, but not in patients with other systemic rheumatic diseases. Of the 17 patients with B19 DNA, only one had IgG anti-B19 antibody and two had IgM anti-B19 antibodies, whereas IgG and IgM anti-B19 antibodies were detected in 27 (49.1%) and 21 (38.2%) of 55 SLE patients without B19 DNA respectively. All sera from the patients with EI contained both IgG and IgM anti-B19 antibodies. B19 DNA was found more commonly in sera from SLE patients without anti-B19 antibodies than in those with anti-B19 antibodies (P<0.05).

Conclusions. B19 infection in patients with SLE may be due to lack of anti-B19 antibodies because of either the immunocompromised nature of the host or the use of immunosuppressive drugs. There was a higher prevalence of hypocomplementaemia and RP in patients with parvovirus B19 viraemia than in those without parvovirus B19 viraemia.

KEY WORDS: Human parvovirus B19, Systemic lupus erythematosus, Nested PCR, Hypocomplementaemia, Raynaud's phenomenon.


   Introduction
Top
 Abstract
 Introduction
Materials and methods
 Results
 Discussion
 References
 
Human parvovirus B19 (B19) was discovered in the UK in 1975 [1] and has been associated with a variety of clinical manifestations, including rash, thrombocytopenia, leukopenia, fetal wastage, hypocomplementaemia, autoimmune haemolytic anaemia, arthritis and vasculitis [2–6]. It is the causative agent of erythema infectiosum (EI). In addition, B19 infection can be associated with elevated levels of antinuclear antibody, anti-double-stranded DNA antibody, antineutrophil cytoplasmic antigens and anti-cardiolipin [7]. B19 is a small, non-enveloped virus containing a single-stranded DNA of 5600 nucleotides and composed of two capsid proteins, VP1 (781 amino acids) and VP2 (554 amino acids), and a non-structural protein, NS1 [8–10]. It targets early erythroid progenitor cells. It requires rapidly dividing cells in order to replicate. The cellular receptor is the P antigen (globoside, a glycosphingolipid), expressed in most individuals on mature erythrocytes and other cells [11]. B19 infection is found world-wide in persons of all ages. Most people become infected at some time during their life, up to 15% of individuals developing infection between 1 and 5 yr of age, 15–60% between the ages of 5 and 19 yr, and 30–60% in adulthood [12–13].

The detection of anti-VP1 and anti-VP2 antibodies is the basis for the diagnosis of acute or past B19 virus infections. The dominant humoral immune response is to VP2 during early convalescence and to VP1 during late convalescence. Anti-VP1 and anti-VP2 antibodies play a major role in limiting B19 infection in man [14]. Antibodies against NS1 may have utility as an indicator of chronic or persistent forms of B19 virus infection [15].

The association of B19 infection with autoimmune diseases, including systemic lupus erythematosus (SLE), rheumatoid arthritis (RA), Sjögren's syndrome (SS), primary biliary cirrhosis (PBC) and polymyositis (PM), has been suggested [5, 6, 16–19], although the exact relationship between the infection and these disorders is not understood. Recently, it has been suggested that B19 exacerbates or even induces SLE [20–22]. There are striking analogies between the clinical features and haematological findings of SLE and those of B19 infection. It was the aim of this study to investigate the role and clinical significance of B19 infection in patients with SLE.


   Materials and methods
Top
 Abstract
 Introduction
 Materials and methods
Results
 Discussion
 References
 
Patients
One hundred and fifty-nine serum samples were tested for parvovirus B19 infection by DNA detection with the nested polymerase chain reaction (PCR). Serum samples were collected from four patients with EI, 72 patients with SLE, 23 with RA, 18 with SS, eight with Raynaud's phenomenon (RP), five with PM and five with PBC. Twenty-two normal, age- and sex-matched subjects were used as a control group. The treatment of SLE depended on the severity of the disease. The patients were treated more aggressively if the disease was active. Of the 72 SLE patients, 41 received either low-dose prednisolone treatment (<=15 mg daily) and/or hydroxychloroquine, 11 received moderate-dose prednisolone (16–40 mg daily) and azathioprine treatment, and 20 received moderate-dose prednisolone and/or cyclophosphamide treatment. All patients were followed up at Chung Shan Medical and Dental College Hospital, Taichung, Taiwan, and were diagnosed using the following criteria: SLE according to the 1982 revised criteria [23]; RA according to the 1987 American Rheumatism Association revised criteria [24]; SS according to the American College of Rheumatology criteria [25]; PM as described by Bohn and Peter [26]; and PBC as described by Williamson et al. [27].

DNA purification and PCR amplification
For amplification of B19 DNA by nested PCR [28], DNA was extracted using the QIA Amp kit (Qiagen, Hilden, Germany) as directed by the manufacturer. In the first round of amplification, 0.2 µM of nucleotide primers corresponding to nucleotides 2381–2400 (B19SI) and 2781–2800 (B19ASI) (5'-CCTTTTCTGTGCTAACCTGC-3' and 5'-CCCAGGCTTGTGTAAGTCTT-3' respectively) were used. Two microlitres of each sample was used in a 50 µl reaction containing 5 µl of 10x buffer (500 mM Tris–HCl, pH 8.7, 50 mM NH4Cl, 20 mM MgCl2, 400 mM KCl, 1% Triton X-100), 4 µl of 25 mM dNTP, 1 unit of Tth DNA polymerase (AcuGen Systems, Boston, MA, USA) and 36 µl water. The reaction was overlaid with mineral oil. After an initial denaturation step of 5 min at 94°C, 38 cycles were performed at 94°C for 45 s, 54°C for 45 s and 72°C for 1 min. After the first round of amplification, 2 µl of the first PCR product was added to the second-round PCR mixture containing 2 µM of each oligonucleotide primer corresponding to nucleotides 2429–2448 (B19SII) and 2730–2751 (B19ASII) (5'-AAAGCTTTGTAGATTATGAG-3' and 5'-GGTTCTGCATGACTGCTATGG-3' respectively). Then 25 cycles of amplification were performed using the cycling parameters described. Subsequently, the nested PCR products of size 322 base pairs (bp) were confirmed on 1% agarose gel. Negative controls were also included in each PCR reaction. The nested PCR was used as it eliminates non-specific background and thus gives a clearer final product. Because of the high sensitivity of the nested PCR reaction used, stringent precautions were taken to avoid the risk of false-positive results.

Restriction mapping
One hundred microlitres of the nested PCR products of the B19-positive samples was analysed by the restriction endonucleases AluI and AcsI. The samples were loaded on a 1% TAE (Tris-acetate/EDTA) gel in TAE buffer for electrophoresis. The DNA fragments were cut and purified with the Qiagen PCR purification kit according to the manufacturer's instructions. Aliquots containing 1 µg of PCR products were digested with AluI (AluI site 2432, 2496, 2552) or AcsI (AcsI site 2894, 2517) with 10 units of enzyme for 4 h, and were separated on a 5% acrylamide gel. After electrophoresis, the DNA fragment was stained with ethidium bromide and excised under UV light.

Southern blot analysis. The procedure was as described by Sambrok et al. [29]. The PCR products were electrophoresed on a 1.5% TAE gel in TAE buffer. After electrophoresis, the DNA was transferred to a nylon membrane by capillary blotting. The gel was pretreated with an alkaline solution (0.2 N NaOH and 0.6 M NaCl) for 30 min and treated with Tris buffer (1.0 M Tris, pH 7.4, and 0.6 M NaCl) for another 30 min. Prehybridization was performed by treating the membrane with 5x Denhardt's solution, 100 µg/ml fragmented salmon sperm DNA and 20 µg/ml polyvinylpyrrolidone (Sigma) and 6x SSC (0.9 M NaCl and 0.09 M sodium citrate) at 55°C for 5 h. The solution was replaced with a fresh hybridization solution of 5x Denhardt's solution, 6x SSC, 100 µg/ml fragmented salmon sperm DNA and 0.5% sodium dodecyl sulphate (SDS) containing 4x105 c.p.m./ml of [32P]ATP end-labelled B19SIII oligonucleotide probe (5'-CAGACTTAGAGCTTATTCAAATAT-3'). After 12 h of hybridization at 55°C with rotation, the nylon membrane was washed five times with 2x SSC solution containing 1% SDS at 55°C for 30 min and five times with 0.5x SSC solution containing 1% SDS at 60°C for 30 min. The membrane was air-dried and exposed on Kodak x-AR film overnight at -70°C.

Detection of B19 IgM and IgG antibodies
The B19 IgM antibody (Parvoscan-B19TMIgM, Euro-Diagnostica, Ideon, Sweden) and B19 IgG antibody (Parvoscreen-B19TMIgG, Euro-Diagnostica) [30] were analysed by ELISA (enzyme-linked immunosorbent assay) against B19 VP1 and VP2 structural proteins according to the manufacturer's instructions.

Statistics
Statistical analysis was done with the {chi}2 test.


   Results
Top
 Abstract
 Introduction
 Materials and methods
 Results
Discussion
 References
 
Parvovirus B19 DNA was identified in patients with EI and SLE
We used nested PCR to test for the presence of B19 DNA in the blood of patients with a variety of autoimmune diseases, including SLE, RA, SS, RP, PBC, PM and EI. B19 DNA was detected in five of six serum samples from four patients with EI and 17 of 72 SLE serum samples. As shown in Fig. 1Go, lanes 3–4, 9 and 16–17 were positive for B19 DNA with the 322 bp nested PCR products. Table 1Go shows a summary of data from patients with B19 DNA identified by PCR. Only sera from patients with SLE and EI were found to have B19 DNA. None of the patients with RA, RP, SS, PM or PBC and none of the normal controls was found to have B19 DNA. Anti-parvovirus B19 IgG and IgM were detected in only one (5.9%) and two (11.8%) of 17 serum samples from SLE patients with B19 DNA respectively, whereas anti-parvovirus B19 IgG and IgM were detected in 27 (49.1%) and 21 (38.2%) of 55 serum samples from SLE patients without B19 DNA respectively. Parvovirus B19 DNA was found more often in SLE patients without anti-B19 IgG and IgM than in those with anti-B19 IgG and IgM antibodies (P<0.05).



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  		FIG. 1. Agarose gel electrophoresis of parvovirus B19 DNA sequences encoding 322 bp of viral structural protein (VP1 unique region) and the non-structural protein NS1 amplified from serum by nested PCR. DNA bands were visualized by staining the gel with ethidium bromide. Positive samples showed the expected molecular size of the 322 bp PCR product indicated on the right. Lane 1, 100 bp DNA molecular weight markers; lanes 2–5, patients with EI; lanes 6–7, normal controls; lanes 8–17, patients with SLE.

 

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  		TABLE 1. Summary of data for patients with B19 DNA

 
The structures of the B19 DNA fragments generated by nested PCR were analysed by the use of the restriction endonucleases AluI and AcsI. The sizes of the enzyme cleavage products for AluI were 56, 63, 123 and 199 bp and those for AcsI were 33, 55, 88 and 234 bp (Fig. 2Go). For the confirmation of these 22 positive samples with B19 DNA by nested PCR, southern blot analysis was employed. The B19SIII oligonucleotide probe, which anneals at nucleotides 2541–2564 for B19 and is known to be an important epitope region [31–33], was end-labelled with [32P]ATP and hybridized with the nylon membrane containing the PCR products. The results of southern blotting showed that the 22 samples were all B19-positive (Fig. 3BGo). As shown in Fig. 3AGo and B, lanes 2–12 were positive for 322 bp PCR products.



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  		FIG. 2. Restriction mapping of parvovirus B19 positive samples. Digested DNA was analysed on 5% acrylamide gels. Lanes 1 and 9, 20 bp DNA molecular weight marker; lanes 2–4, DNA digested with AluI; lanes 5–7, DNA digested with AcsI; lane 8, control for the 322 bp PCR product without endonuclease.

 


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  		FIG. 3. Southern blot analysis of the 322 bp PCR product of B19 DNA from serum samples of patients with EI or SLE. (A) Agarose gel electrophoresis of the 322 bp product of nested PCR. (B) Southern blot of DNA fragments. Lane 1, {phi}X174 RF DNA/HaeIII fragments of DNA marker; lanes 2–6, patients with EI; lanes 7–13, patients with SLE. Lane 13 is the negative control without DNA fragments.

 

Clinical significance of parvovirus B19 infection in patients with SLE
The relationship between the presence of B19 DNA and clinical manifestations of SLE was studied. As shown in Table 2Go, the prevalence of hypocomplementaemia was higher in patients with B19 viraemia. No correlation could be found between the presence of B19 DNA and other clinical manifestations of SLE.


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  		TABLE 2. Clinical manifestations of SLE patients with and without B19 DNA by nested PCR

 


   Discussion
Top
 Abstract
 Introduction
 Materials and methods
 Results
 Discussion
References
 
The relationship of parvovirus B19 infection with SLE is an issue of interest. There are striking similarities between B19 infection and SLE. It is difficult to differentiate B19 infection from SLE clinically. The occurrence of parvovirus B19 infection in adults has been documented in some patients with systemic autoimmune diseases [5, 6, 16–19]. Parvovirus B19 may be accompanied by a transient subclinical state of autoimmunity [22] and may mimic or exacerbate SLE [6, 21]. It may be implicated in the development of SLE as well as other chronic arthropathies [5, 22]. In our study, parvovirus B19 DNA was detected in 17 (24%) patients with SLE by PCR and was confirmed by Southern blotting. B19 DNA was not found in sera from patients with other autoimmune diseases, including RA, SS, PBC and PM. However, the presence of B19 DNA in patients with SLE may not be causative. It may rather reflect a superimposed B19 infection in patients with SLE due to lack of antibodies against B19. In this study, the prevalence of IgG and IgM anti-B19 antibodies in sera from SLE patients with B19 DNA was much lower than in patients without B19 DNA (P<0.05). Kurtzman et al. [14, 34] demonstrated that the production of antibody to the B19 capsid protein plays a major role in limiting parvovirus infection in man. It has also been reported that, in the immunocompetent host, the production of B19-specific antibodies results in clearance of the viraemia within a few days, whereas in immunocompromised patients the virus persists [14, 34–35]. The appearance of B19-specific neutralizing antibodies might alter the course of viral infection. The persistence of infection with parvovirus B19 in our patients with SLE may have been due to lack of antibodies against parvovirus B19 because the host was immunocompromised or because of the use of immunosuppressive agents.

The restriction mapping of nested PCR product is a simple and sensitive method of detecting B19 infection that is suitable for clinical use. The typical profiles of AluI and AcsI cleavage products with four different DNA fragments (Fig. 2Go) are both easily identified for the confirmation of B19 infection. The method gives consistent results and can be used instead of nucleotide sequencing to confirm B19 infection.

As B19 DNA was detected only in patients with SLE or EI, its clinical significance was studied further. Hypocomplementaemia and RP were significantly more common in patients with B19 viraemia than in those without B19 DNA. Parvovirus B19 infection may have exacerbated the clinical course of SLE. However, there was no apparent association between the presence of B19 DNA and other clinical manifestations, such as skin rash, arthritis and proteinuria, in patients with SLE. Recently, cytomegalovirus infection has been found to be a highly significant risk factor for RP [36]. Viral infection may affect the course of SLE, leading to specific clinical subsets. These preliminary findings require confirmation in order to elucidate the significance of the presence of B19 DNA in SLE.


   Acknowledgments
 
This study was supported by a grant NSC 89–2314-B040–009 from the National Science Council of Taiwan.


   Notes
 
Correspondence to: G. J. Tsay, Department of Medicine and Institute of Immunology, Chung Shan Medical and Dental College, 110 Sec. 1, Chien Kuo N. Road, Taichung 402, Taiwan. Back


   References
Top
 Abstract
 Introduction
 Materials and methods
 Results
 Discussion
 References
 

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Submitted 24 May 2000; Accepted 2 September 2000


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