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treated with elbasvir&#47;grazoprevir in December 2017&#44; achieving SVR&#46; Six months after achieving undetectable viraemia&#44; she began to experience xerophthalmia&#44; xerostomia and parotitis&#44; for which she began follow-up by rheumatology&#46; Blood tests showed&#58; hypergammaglobulinaemia &#40;polyclonal IgG&#41;&#44; positive ANA &#40;titre 1&#47;640&#41;&#44; negative anti-RO antibodies &#40;anti-Ro&#41; and anti-La antibodies &#40;anti-LA&#41;&#44; rheumatoid factor &#40;RF&#41; 55<span class="elsevierStyleHsp" style=""></span>mg&#47;dl &#40;0&#8211;40&#41;&#59; serum creatinine &#40;sCr&#41; 0&#46;87<span class="elsevierStyleHsp" style=""></span>mg&#47;dl&#59; basic urine negative for proteins and red blood cells&#46; With these abnormalities&#44; she was diagnosed with SS&#44; as she did not meet the criteria for primary Sj&#246;gren&#39;s syndrome due to negative anti-Ro and anti-La&#44; and previous HCV infection&#46;</p><p id="par0015" class="elsevierStylePara elsevierViewall">In January 2020&#44; the patient began to experience purpuric skin lesions on her lower limbs associated with type III or mixed positive cryoglobulins &#40;polyclonal IgG and polyclonal IgM&#41;&#44; without prior testing having been performed&#59; her RF had risen &#40;130 IU&#47;mL&#41; and renal function remained normal &#40;sCr 0&#46;87<span class="elsevierStyleHsp" style=""></span>mg&#47;dl&#41;&#44; along with a basic urine sample with no abnormalities&#46; Skin biopsy was inconclusive&#46; However&#44; based on the rest of results&#44; it was treated as type III or mixed cryoglobulinaemic vasculitis with skin involvement and she was started on oral prednisone &#40;0&#46;5<span class="elsevierStyleHsp" style=""></span>mg&#47;kg&#47;day&#41;&#46;</p><p id="par0020" class="elsevierStylePara elsevierViewall">In May of that same year&#44; she was admitted for a respiratory infection&#44; documenting simultaneously a clinical and biochemical nephrotic syndrome &#40;sCr 1&#46;35<span class="elsevierStyleHsp" style=""></span>mg&#47;dl&#59; 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1</a>A and B&#41;&#46; Using the silver technique&#44; double contour images in the capillary loops &#40;<a class="elsevierStyleCrossRef" href="#fig0005">Fig&#46; 1</a>C&#41;&#46; Immunofluorescence showed capillary positivity for IgG &#40;&#43;&#43;&#43;&#41; in a coarse granular pattern and with a subendothelial and mesangial location &#40;<a class="elsevierStyleCrossRef" href="#fig0005">Fig&#46; 1</a>D&#41;&#46; All of this is consistent with a pattern of membranoproliferative glomerulonephritis &#40;MPGN&#41; mediated by immune complexes&#46;</p><elsevierMultimedia ident="fig0005"></elsevierMultimedia><p id="par0025" class="elsevierStylePara elsevierViewall">Although there was no sample for electron microscopy and no thrombi or fibrinoid necrosis were found&#44; the rest corresponded to type III MCV with skin and kidney involvement in the form of MPGN&#44; probably related to past HCV infection&#46; A lymphoproliferative syndrome was ruled out by computed tomography&#44; and the HCV viral load was always negative&#46; The patient was given rituximab &#40;500<span class="elsevierStyleHsp" style=""></span>mg x 2 doses 15 days apart&#41; and steroid therapy in a tapering regimen&#46; After three months she was in complete remission&#58; sCr 0&#46;8<span class="elsevierStyleHsp" style=""></span>mg&#47;dl&#59; albumin 4&#46;2<span class="elsevierStyleHsp" style=""></span>g&#47;dl&#59; C3 66&#46;90<span class="elsevierStyleHsp" style=""></span>mg&#47;dl &#40;normal&#41;&#59; C4 5&#46;40<span class="elsevierStyleHsp" style=""></span>mg&#47;dl &#40;normal&#41;&#59; negative cryoglobulins&#46; Urinalysis with 24<span class="elsevierStyleHsp" style=""></span>-h urinary protein of 294<span class="elsevierStyleHsp" style=""></span>mg&#47;g and normal sediment&#46; She has remained stable over the subsequent 18 months of follow-up&#44; receiving maintenance doses of rituximab &#40;500<span class="elsevierStyleHsp" style=""></span>mg&#41; every six months since then&#46;</p><p id="par0030" class="elsevierStylePara elsevierViewall">The development of new DAA against HCV has represented a paradigm shift in the treatment of this infection&#46;<a class="elsevierStyleCrossRef" href="#bib0005"><span class="elsevierStyleSup">1</span></a> They are clearly effective in eradicating the virus&#44; with SVR rates close to 99&#37;&#46; Despite this&#44; the effectiveness in controlling some EH manifestations is not so evident&#46;<a class="elsevierStyleCrossRef" href="#bib0005"><span class="elsevierStyleSup">1</span></a></p><p id="par0035" class="elsevierStylePara elsevierViewall">MCV is the most common EH manifestation&#46;<a class="elsevierStyleCrossRef" href="#bib0010"><span class="elsevierStyleSup">2</span></a> Typically&#44; those associated with hepatitis C virus infection are type II and&#47;or type III cryoglobulinaemia&#44; also known as mixed cryoglobulinaemias&#46;<a class="elsevierStyleCrossRef" href="#bib0015"><span class="elsevierStyleSup">3</span></a> Some 70&#8211;90&#37; are associated with HCV infection&#46;<a class="elsevierStyleCrossRef" href="#bib0010"><span class="elsevierStyleSup">2</span></a> In our case&#44; it was a type III mixed cryoglobulinaemia because it was formed by polyclonal IgG and IgM&#44; with rheumatoid activity&#46;</p><p id="par0040" class="elsevierStylePara elsevierViewall">The renal involvement usually associated with MCV due to hepatitis C virus is MPGN&#46;<a class="elsevierStyleCrossRef" href="#bib0015"><span class="elsevierStyleSup">3</span></a> DAA have highly variable clinical and immunological response rates on MCV &#40;64&#37;&#8211;96&#37; and 48&#37;&#8211;89&#37;&#44; respectively&#41;&#46;<a class="elsevierStyleCrossRef" href="#bib0020"><span class="elsevierStyleSup">4</span></a> Furthermore&#44; some authors have suggested that the use of DAA alone could be insufficient in controlling renal manifestations and cryoglobulinaemic vasculitis&#46;<a class="elsevierStyleCrossRef" href="#bib0020"><span class="elsevierStyleSup">4</span></a> Recent publications have reflected persistence of MCV with or without renal involvement despite SVR with DAA&#46;<a class="elsevierStyleCrossRefs" href="#bib0025"><span class="elsevierStyleSup">5&#8211;8</span></a> In these patients&#44; the use of immunosuppressive treatment such as rituximab can be effective in controlling the disease&#46;<a class="elsevierStyleCrossRef" href="#bib0045"><span class="elsevierStyleSup">9</span></a> In our case&#44; what makes it unusual is that the manifestations appeared after SVR&#46; Prior to treatment with DAA&#44; no EH involvement had been documented&#46; To the best of our knowledge&#44; there are few published cases similar to ours&#46;</p><p id="par0045" class="elsevierStylePara elsevierViewall">The mechanism by which patients with eradicated HCV infection can develop EH manifestations after treatment with DAA is not fully understood&#46; HCV infection causes different immune system regulation abnormalities&#46; One well-known theory is that HCV &#34;settles&#34; inside the cell it infects&#44; thereby avoiding attack by the immune system&#46;<a class="elsevierStyleCrossRef" href="#bib0050"><span class="elsevierStyleSup">10</span></a> HCV acts on the usual cellular DNA repair mechanisms&#44; producing an increase in unrepaired DNA alterations that are associated with greater genomic instability&#44; increasing the risk of development of neoplasia and dysfunction of the immune system&#46;<a class="elsevierStyleCrossRefs" href="#bib0050"><span class="elsevierStyleSup">10&#44;11</span></a> Among other factors&#44; this would cause the abnormal activation of B lymphocytes and their monoclonal expansion&#44; which would give rise to the formation of cryoglobulins responsible for MCV&#46;<a class="elsevierStyleCrossRef" href="#bib0055"><span class="elsevierStyleSup">11</span></a> Some studies have found that patients who achieved clinical remission of MCV after the use of DAA have shown a decrease in activated B lymphocytes and an increase in regulatory T lymphocytes&#46;<a class="elsevierStyleCrossRef" href="#bib0060"><span class="elsevierStyleSup">12</span></a> Other authors&#44; such as Hegazy et al&#46;&#44; have found that patients with HCV infection treated with DAA have a higher concentration of B lymphocyte activation factors &#40;BAFF and APRIL&#41; during the first 12 months after receiving treatment&#46;<a class="elsevierStyleCrossRef" href="#bib0065"><span class="elsevierStyleSup">13</span></a> This could lead to hyperactivity of B lymphocytes after the use of DAA&#44; which could explain the appearance of autoimmune manifestations after treatment&#46;</p><p id="par0050" class="elsevierStylePara elsevierViewall">Lastly&#44; contrary to what might have happened with the immunomodulatory effect of interferon&#44; free regimens of this drug could lose this anti-inflammatory effect&#44; and not be sufficient in all cases to control EH manifestations&#46;<a class="elsevierStyleCrossRef" href="#bib0065"><span class="elsevierStyleSup">13</span></a></p><p id="par0055" class="elsevierStylePara elsevierViewall">In conclusion&#44; DAA improve hepatic morbidity and mortality rates in almost all cases&#46; The exact mechanism behind the development of autoimmune manifestations that appear once SVR is achieved with these drugs is unknown&#46; Therefore&#44; in the first few months after treatment with DAA&#44; it is important to closely monitor for autoimmune manifestations as&#44; if they do appear&#44; they may require additional immunosuppressive therapy&#46;</p><span id="sec0005" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0005">Funding</span><p id="par0060" class="elsevierStylePara elsevierViewall">The authors declare that they have not received any funding for publishing this article&#46;</p></span><span id="sec0010" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0010">Conflicts of interest</span><p id="par0065" class="elsevierStylePara elsevierViewall">The authors declare that they have no conflicts of interest&#46;</p></span></span>"
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Letter to the Editor
Cryoglobulinemic vasculitis and membranoproliferative glomerulonephritis in a patient with cured virus C infection
Vasculitis crioglobulinémica y glomerulonefritis membranoproliferativa en paciente con infección por virus C curada
Ester Casillas Sagradoa, Candela Moliz Cordóna,
Corresponding author
candelamoliz@gmail.com

Corresponding author.
, Ana Sainz Gonzálezb, Vanessa Lopes Martína, Milagros Fernández Lucasa, Javier Villacorta Péreza
a Servicio de Nefrología, Hospital Universitario Ramón y Cajal, Madrid, Spain
b Servicio de Anatomía Patológica, Hospital Universitario Ramón y Cajal, Madrid, Spain
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    "textoCompleto" => "<span class="elsevierStyleSections"><p id="par0005" class="elsevierStylePara elsevierViewall">The development of new direct-acting antivirals &#40;DAA&#41; for the treatment of hepatitis C virus &#40;HCV&#41; has been a revolution in the control of this infection&#44; achieving sustained virological response &#40;SVR&#41; rates close to 99&#37;&#46;<a class="elsevierStyleCrossRefs" href="#bib0005"><span class="elsevierStyleSup">1&#8211;4</span></a> Some extrahepatic &#40;EH&#41; manifestations associated with this infection may persist or recur after achieving SVR with DAA&#46;<a class="elsevierStyleCrossRef" href="#bib0020"><span class="elsevierStyleSup">4</span></a> Few cases have been reported of the development of new EH manifestations after achieving SVR&#46; We present a case of mixed cryoglobulinaemic vasculitis &#40;MCV&#41; and membranoproliferative glomerulonephritis&#44; accompanied by sicca syndrome &#40;SS&#41;&#44; which manifested 28 months after achieving SVR with DAA&#46;</p><p id="par0010" class="elsevierStylePara elsevierViewall">This patient was a 70-year-old woman with HCV infection without liver or EH involvement&#44; treated with elbasvir&#47;grazoprevir in December 2017&#44; achieving SVR&#46; Six months after achieving undetectable viraemia&#44; she began to experience xerophthalmia&#44; xerostomia and parotitis&#44; for which she began follow-up by rheumatology&#46; Blood tests showed&#58; hypergammaglobulinaemia &#40;polyclonal IgG&#41;&#44; positive ANA &#40;titre 1&#47;640&#41;&#44; negative anti-RO antibodies &#40;anti-Ro&#41; and anti-La antibodies &#40;anti-LA&#41;&#44; rheumatoid factor &#40;RF&#41; 55<span class="elsevierStyleHsp" style=""></span>mg&#47;dl &#40;0&#8211;40&#41;&#59; serum creatinine &#40;sCr&#41; 0&#46;87<span class="elsevierStyleHsp" style=""></span>mg&#47;dl&#59; basic urine negative for proteins and red blood cells&#46; With these abnormalities&#44; she was diagnosed with SS&#44; as she did not meet the criteria for primary Sj&#246;gren&#39;s syndrome due to negative anti-Ro and anti-La&#44; and previous HCV infection&#46;</p><p id="par0015" class="elsevierStylePara elsevierViewall">In January 2020&#44; the patient began to experience purpuric skin lesions on her lower limbs associated with type III or mixed positive cryoglobulins &#40;polyclonal IgG and polyclonal IgM&#41;&#44; without prior testing having been performed&#59; her RF had risen &#40;130 IU&#47;mL&#41; and renal function remained normal &#40;sCr 0&#46;87<span class="elsevierStyleHsp" style=""></span>mg&#47;dl&#41;&#44; along with a basic urine sample with no abnormalities&#46; Skin biopsy was inconclusive&#46; However&#44; based on the rest of results&#44; it was treated as type III or mixed cryoglobulinaemic vasculitis with skin involvement and she was started on oral prednisone &#40;0&#46;5<span class="elsevierStyleHsp" style=""></span>mg&#47;kg&#47;day&#41;&#46;</p><p id="par0020" class="elsevierStylePara elsevierViewall">In May of that same year&#44; she was admitted for a respiratory infection&#44; documenting simultaneously a clinical and biochemical nephrotic syndrome &#40;sCr 1&#46;35<span class="elsevierStyleHsp" style=""></span>mg&#47;dl&#59; urea 55<span class="elsevierStyleHsp" style=""></span>mg&#47;dl&#59; albumin 3&#46;2<span class="elsevierStyleHsp" style=""></span>g&#47;dl&#59; cholesterol 275<span class="elsevierStyleHsp" style=""></span>mg&#47;dl&#59; 24<span class="elsevierStyleHsp" style=""></span>-h urinary protein 5&#44;900<span class="elsevierStyleHsp" style=""></span>mg&#47;24<span class="elsevierStyleHsp" style=""></span>h&#59; urinary sediment with 5&#8211;10 dysmorphic red blood cells&#47;field&#44; and hypocomplementaemia with C3 of 47&#46;80<span class="elsevierStyleHsp" style=""></span>mg&#47;dl and C4 of 2&#46;20<span class="elsevierStyleHsp" style=""></span>mg&#47;dl&#41;&#46; The rest of the autoimmunity study was negative &#40;negative antiPLA2R&#44; ANCA and proteins&#41;&#46; Kidney biopsy showed 18 glomeruli&#44; all of them hypertrophic with lobulated morphology and occlusion of vascular lumens by inflammatory cells&#44; mesangial expansion with mesangial hypercellularity &#40;<a class="elsevierStyleCrossRef" href="#fig0005">Fig&#46; 1</a>A and B&#41;&#46; Using the silver technique&#44; double contour images in the capillary loops &#40;<a class="elsevierStyleCrossRef" href="#fig0005">Fig&#46; 1</a>C&#41;&#46; Immunofluorescence showed capillary positivity for IgG &#40;&#43;&#43;&#43;&#41; in a coarse granular pattern and with a subendothelial and mesangial location &#40;<a class="elsevierStyleCrossRef" href="#fig0005">Fig&#46; 1</a>D&#41;&#46; All of this is consistent with a pattern of membranoproliferative glomerulonephritis &#40;MPGN&#41; mediated by immune complexes&#46;</p><elsevierMultimedia ident="fig0005"></elsevierMultimedia><p id="par0025" class="elsevierStylePara elsevierViewall">Although there was no sample for electron microscopy and no thrombi or fibrinoid necrosis were found&#44; the rest corresponded to type III MCV with skin and kidney involvement in the form of MPGN&#44; probably related to past HCV infection&#46; A lymphoproliferative syndrome was ruled out by computed tomography&#44; and the HCV viral load was always negative&#46; The patient was given rituximab &#40;500<span class="elsevierStyleHsp" style=""></span>mg x 2 doses 15 days apart&#41; and steroid therapy in a tapering regimen&#46; After three months she was in complete remission&#58; sCr 0&#46;8<span class="elsevierStyleHsp" style=""></span>mg&#47;dl&#59; albumin 4&#46;2<span class="elsevierStyleHsp" style=""></span>g&#47;dl&#59; C3 66&#46;90<span class="elsevierStyleHsp" style=""></span>mg&#47;dl &#40;normal&#41;&#59; C4 5&#46;40<span class="elsevierStyleHsp" style=""></span>mg&#47;dl &#40;normal&#41;&#59; negative cryoglobulins&#46; Urinalysis with 24<span class="elsevierStyleHsp" style=""></span>-h urinary protein of 294<span class="elsevierStyleHsp" style=""></span>mg&#47;g and normal sediment&#46; She has remained stable over the subsequent 18 months of follow-up&#44; receiving maintenance doses of rituximab &#40;500<span class="elsevierStyleHsp" style=""></span>mg&#41; every six months since then&#46;</p><p id="par0030" class="elsevierStylePara elsevierViewall">The development of new DAA against HCV has represented a paradigm shift in the treatment of this infection&#46;<a class="elsevierStyleCrossRef" href="#bib0005"><span class="elsevierStyleSup">1</span></a> They are clearly effective in eradicating the virus&#44; with SVR rates close to 99&#37;&#46; Despite this&#44; the effectiveness in controlling some EH manifestations is not so evident&#46;<a class="elsevierStyleCrossRef" href="#bib0005"><span class="elsevierStyleSup">1</span></a></p><p id="par0035" class="elsevierStylePara elsevierViewall">MCV is the most common EH manifestation&#46;<a class="elsevierStyleCrossRef" href="#bib0010"><span class="elsevierStyleSup">2</span></a> Typically&#44; those associated with hepatitis C virus infection are type II and&#47;or type III cryoglobulinaemia&#44; also known as mixed cryoglobulinaemias&#46;<a class="elsevierStyleCrossRef" href="#bib0015"><span class="elsevierStyleSup">3</span></a> Some 70&#8211;90&#37; are associated with HCV infection&#46;<a class="elsevierStyleCrossRef" href="#bib0010"><span class="elsevierStyleSup">2</span></a> In our case&#44; it was a type III mixed cryoglobulinaemia because it was formed by polyclonal IgG and IgM&#44; with rheumatoid activity&#46;</p><p id="par0040" class="elsevierStylePara elsevierViewall">The renal involvement usually associated with MCV due to hepatitis C virus is MPGN&#46;<a class="elsevierStyleCrossRef" href="#bib0015"><span class="elsevierStyleSup">3</span></a> DAA have highly variable clinical and immunological response rates on MCV &#40;64&#37;&#8211;96&#37; and 48&#37;&#8211;89&#37;&#44; respectively&#41;&#46;<a class="elsevierStyleCrossRef" href="#bib0020"><span class="elsevierStyleSup">4</span></a> Furthermore&#44; some authors have suggested that the use of DAA alone could be insufficient in controlling renal manifestations and cryoglobulinaemic vasculitis&#46;<a class="elsevierStyleCrossRef" href="#bib0020"><span class="elsevierStyleSup">4</span></a> Recent publications have reflected persistence of MCV with or without renal involvement despite SVR with DAA&#46;<a class="elsevierStyleCrossRefs" href="#bib0025"><span class="elsevierStyleSup">5&#8211;8</span></a> In these patients&#44; the use of immunosuppressive treatment such as rituximab can be effective in controlling the disease&#46;<a class="elsevierStyleCrossRef" href="#bib0045"><span class="elsevierStyleSup">9</span></a> In our case&#44; what makes it unusual is that the manifestations appeared after SVR&#46; Prior to treatment with DAA&#44; no EH involvement had been documented&#46; To the best of our knowledge&#44; there are few published cases similar to ours&#46;</p><p id="par0045" class="elsevierStylePara elsevierViewall">The mechanism by which patients with eradicated HCV infection can develop EH manifestations after treatment with DAA is not fully understood&#46; HCV infection causes different immune system regulation abnormalities&#46; One well-known theory is that HCV &#34;settles&#34; inside the cell it infects&#44; thereby avoiding attack by the immune system&#46;<a class="elsevierStyleCrossRef" href="#bib0050"><span class="elsevierStyleSup">10</span></a> HCV acts on the usual cellular DNA repair mechanisms&#44; producing an increase in unrepaired DNA alterations that are associated with greater genomic instability&#44; increasing the risk of development of neoplasia and dysfunction of the immune system&#46;<a class="elsevierStyleCrossRefs" href="#bib0050"><span class="elsevierStyleSup">10&#44;11</span></a> Among other factors&#44; this would cause the abnormal activation of B lymphocytes and their monoclonal expansion&#44; which would give rise to the formation of cryoglobulins responsible for MCV&#46;<a class="elsevierStyleCrossRef" href="#bib0055"><span class="elsevierStyleSup">11</span></a> Some studies have found that patients who achieved clinical remission of MCV after the use of DAA have shown a decrease in activated B lymphocytes and an increase in regulatory T lymphocytes&#46;<a class="elsevierStyleCrossRef" href="#bib0060"><span class="elsevierStyleSup">12</span></a> Other authors&#44; such as Hegazy et al&#46;&#44; have found that patients with HCV infection treated with DAA have a higher concentration of B lymphocyte activation factors &#40;BAFF and APRIL&#41; during the first 12 months after receiving treatment&#46;<a class="elsevierStyleCrossRef" href="#bib0065"><span class="elsevierStyleSup">13</span></a> This could lead to hyperactivity of B lymphocytes after the use of DAA&#44; which could explain the appearance of autoimmune manifestations after treatment&#46;</p><p id="par0050" class="elsevierStylePara elsevierViewall">Lastly&#44; contrary to what might have happened with the immunomodulatory effect of interferon&#44; free regimens of this drug could lose this anti-inflammatory effect&#44; and not be sufficient in all cases to control EH manifestations&#46;<a class="elsevierStyleCrossRef" href="#bib0065"><span class="elsevierStyleSup">13</span></a></p><p id="par0055" class="elsevierStylePara elsevierViewall">In conclusion&#44; DAA improve hepatic morbidity and mortality rates in almost all cases&#46; The exact mechanism behind the development of autoimmune manifestations that appear once SVR is achieved with these drugs is unknown&#46; Therefore&#44; in the first few months after treatment with DAA&#44; it is important to closely monitor for autoimmune manifestations as&#44; if they do appear&#44; they may require additional immunosuppressive therapy&#46;</p><span id="sec0005" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0005">Funding</span><p id="par0060" class="elsevierStylePara elsevierViewall">The authors declare that they have not received any funding for publishing this article&#46;</p></span><span id="sec0010" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0010">Conflicts of interest</span><p id="par0065" class="elsevierStylePara elsevierViewall">The authors declare that they have no conflicts of interest&#46;</p></span></span>"
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          "en" => "<p id="spar0005" class="elsevierStyleSimplePara elsevierViewall">&#40;A&#41; H&#38;E&#58; 20&#215;&#46; Glomerulus with lobulated morphology&#44; mesangial expansion due to matrix and mesangial and endocapillary proliferation&#46; &#40;B&#41; PAS 20&#215;&#58; PAS positive mesangial expansion&#44; with increased cellularity&#46; &#40;C&#41; Methenamine silver 64&#215;&#46; Images of double contours in the glomerular capillary loops &#40;red arrows&#41;&#46; &#40;D&#41; Direct immunofluorescence &#40;DIF&#41; IgG 20&#215;&#46; Intense deposit &#40;3&#43;&#41; in a coarse granular pattern and with a subendothelial and mesangial location for IgG&#46;</p>"
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ISSN: 20132514
Original language: English
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