Biopsy Proven Non-Amyloid Glomerular Diseases in Patients
With Familial Mediterranean Fever
Can
H¨¹zmeli, Ayşe Şeker Koçkara, Ferhan Candan, Mansur
Kayataş
Can H¨¹zmeli, Ayşe Şeker
Koçkara, Ferhan Candan, Mansur Kayataş, Department of Nephrology, Cumhuriyet University Hospital, Sivas, Turkey
Correspondence to: Ayşe Şeker Koçkara,
Department of Nephrology, Cumhuriyet
University Hospital, Sivas, Turkey.
Email: drayse14@hotmail.com
Telephone: +5325680187
Received: March 26,
2015
Revised: May 27, 2015
Accepted: May 31, 2015
Published online: June 26, 2015
ABSTRACT
AIM: Kidney involvement is the most
serious organ involvement of Familial Mediterranean Fever (FMF), while the most
common cause is AA type amyloidosis with serum amyloid AA deposition. However,
vasculitis and other types of glomerulonephritis (GN) also have been reported.
With this study we evaluated biopsy proven non-amyloid glomerular diseases in
patients with FMF.
Methods: At our
Nephrology clinic, total 950 patients followed by diagnosis of FMF have been
evaluated. Nine patients who had positive proteinuria ( >500 mg/day) but had
negative amyloidosis in the tissue biopsy were made renal biopsy.
Results: Nine patients
underwent a renal biopsy, two patients were found to have IgA nephropathy
(IGAN), three mesangioproliferative glomerulonephritis (MsPGN), three
membranous glomerulonephritis (MGN) and one had immune complex
glomerulonephritis. Two patients with IGAN and one patient with MGN with
non-nephrotic proteinuria exhibited significant improvement with colchicine and
angiotensin receptor blocker (ARB) therapy. Other patients were treated with
colchicine, an ARB and immunosuppressive drugs. Upon evaluation for the FMF
gene mutation, different mutations have been found for the same
glomerulonephritis type.
Conclusions: Other glomerular
causes also must be investigated alongside amyloidosis in the case of kidney
involvement in FMF patients. While patients with IGAN and other
glomerulonephrities with non-nephrotic proteinuria can respond well to
colchicine treatment, patients with more aggressive kidney involvement may
require immunosuppressive therapy. Further studies are needed for revealing the
relationship between FMF gene mutation and non-amyloid glomerular diseases.
© 2015 ACT. All
rights reserved.
Key words: Familial Mediterranean fever; Nonamyloidotic
proteinuria; Glomerulonephritis
H¨¹zmeli C, Koçkara
AS, Candan F, Kayataş M. Biopsy Proven Non-Amyloid Glomerular Diseases in
Patients With Familial Mediterranean Fever. Journal of
Nephrology Research 2015; 1(1): 34-39 Available from: URL: http://www.ghrnet.org/index.php/jnr/article/view/1045
INTRODUCTION
Familial Mediterranean Fever (FMF) is an inflammatory disease with an
autosomal recessive inheritance pattern characterized by fever, pain associated
with episodes of serositis and synovitis and skin lesions. It is common among
Sephardic Jews, Turks, Arabs and Armenians from the Mediterranean Sea region[1].
A field study of Özen et al. recently revealed its prevalence in Turkey as
1:1075[2]. Mutations of the MEFV gene, on the short arm of
chromosome 16, codes for pyrin or marenostrin proteins is responsible for the
disease. The MEFV mutation is found in less than 70% of patients diagnosed with
FMF. Four mutations have been defined in 85% of patients from the mentioned 4
ethnic groups (M694V, M680I, M694I V726A)[3-5].
AA type
amyloidosis is the result of serum amyloid A protein deposition in tissues. It
is the best understood and the most serious reason for kidney failure in
patients with FMF. In a report from Turkey, amyloidosis rates among FMF
patients were found to be 7%[6]. There is no publication proving an
increase of glomerulonephritis among FMF patients. Kidney involvement of FMF
may occur due to vasculitis. But, other cases of glomerulonephritis
(crescentic, rapidly progressing glomerulonephritis, mesangial IgA nephropathy,
IgM nephropathy, diffuse proliferative glomerulonephritis) have also been
reported in patients with FMF[7-9]. We hereby present nine FMF
patients with biopsy proven glomerulonephritis, who have been followed by the
Nephrology Department of Cumhuriyet University.
Materials
and Methods
Patient
selection
950 FMF patients who had been followed by the Nephrology Department of
our university between 2004 to 2013 were evaluated. The diagnosis of FMF was
made according to the Tel Hashomer criteria[10]:
Major Criteria: 1. Recurrent
febrile episodes accompanied by peritonitis, pleuritis, or synovitis; 2.
Amyloidosis of AA-type without predisposing disease; 3. Favorable response to
continuous colchicine treatment
Minor Criteria: 1. Recurrent
febrile episodes; 2. Erysipelas-like erythema; 3. Positive history of FMF in a
first-degree relative
Definite Diagnosis: 2 major
criteria or 1 major and 2 minor criteria
Probable Diagnosis: 1 major and 1
minor criterion
During
follow-up encounters, proteinuria was assessed by a 24 hour urine collection in
patients with FMF. Patients with proteinuria levels exceeding 500 mg/day were
further assessed for amyloidosis by rectal or gum biopsies. The Congo red
method was used to detect amyloid in tissue sections. Amyloid was identified as
the AA type on immunohistochemical testing with the use of monoclonal
antibodies specific to SAA. ANA, anti-ds DNA, ANCA, anti GBM, complements,
anti-HIV and anti-hepatitis B and C antibodies also have been measured in
patients with proteinuria more than 500 mg/day. Kidney biopsies were performed
in nine patients with more than 500 mg/day proteinuria and tissue biopsies
negative for amyloidosis.
Exclusion criteria were: malignancy, SLE and systemic vasculitis, use
of immunosuppressive drugs, chronic renal failure and liver cirrhosis.
Genetic
Analysis
DNA was isolated from peripheral blood leukocytes by standard
procedures and amplified with sequence-specific primers using the polymerase
chain reaction (PCR) technique. Depending on the laboratory, denaturing
gradient gel electrophoresis, PCR/RFLP, amplification of refractory mutation
system, and DNA sequencing methods were used to screen for MEFV gene mutations.
Results
950 patients were followed by our nephrology team and tissue biopsies
were performed for patients with proteinuria greater than 500 mg/day with 24
hour urine collection to investigate amyloidosis. Nine patients with a negative
tissue biopsy for amyloidosis underwent a kidney biopsy and were subsequently
diagnosed with glomerulonephritis. The diagnosis of two patients with IGAN,
three patients with MsPGN, three patients with MGN and one patient with immune
complex GN was made. Four of nine patients were diagnosed with FMF and had been
receiving colchicine therapy before biopsy. The other five patients were
diagnosed FMF and glomerulonephritis on the same date and thus had not yet
received any therapy. One patient with a high initial creatinine level
(creatinine clearance of 30 ml/minute) and kidney biopsy of MsPGN, did not
respond to colchicine, ARB and azathioprine treatment and later progressed to
being dialysis dependent. Another patient with a high creatinine level
(creatinine clearance of 40 mL/minute) was diagnosed with immune complex GN and
kidney function was restored with colchicine, ARB, prednisolone and
azathioprine treatment.
Clinical data
of the patients, results of the genetic analysis for FMF, biopsy findings, and
therapy for both glomerulopathy and FMF are summarized in Table 1
CASE 1
A 22 year-old female patient complained of episodes of knee and hip
joint pain for a year. Family history includes cousins with FMF. Results of
physical examination were within normal limits. Blood analysis revealed a
creatinine level of 0.7 mg/dL and urinalysis revealed hematuria and proteinuria
(++). A 24-hour urinary protein collection revealed 2.3 g/day. Serological
tests of hepatitis markers, ANA, Anti-dsDNA, p-ANCA, c-ANCA, anti-GBM
antibodies were all negative and C3 and C4 were within normal limits. FMF gene
analysis revealed a heterozygote M694V mutation. Renal biopsy found an increase
in mesangial cells and matrix, IGAN with IgA (+++) and C3(+++) and poor IgG
staining. Congo red was negative (Figure 1). Colchicine tablet 3¡Á0.5 mg/day and
valsartan 160 mg/day were administered. The patient reported improvement with
her joint pain. Follow-up after two months revealed a 24-hour urinary protein
level of 620 mg/day.
CASE 2
A 30 year-old female patient with recurrent episodes of abdominal,
chest and joint pain for 10 years was evaluated during an outpatient clinic
visit. Family history reveals that the patient¡¯s father has FMF and chronic
renal failure. Physical examination was within normal limits. Blood analysis
revealed a creatinine level of 0.81 mg/dL, urinalysis revealed proteinuria (+),
hematuria, and a 24 hour urinary protein collection of 960 mg/day. Serological
tests for hepatitis markers, ANA, Anti-ds DNA, p-ANCA, c-ANCA, Anti-GBM
antibodies were all negative and C3 and C4 were within normal limits. Renal
biopsy reported IGAN with a mild mesangial increase and proliferation, (+)
mesangial staining of glomeruli with IgG and IgM by immunofluorescence, (+++)
mesangial staining with IgA. Congo red was negative. Gene analysis for FMF
revealed heterozygote E148Q mutation. A colchicine tablet 3¡Á0.5 mg/day and
valsartan 160 mg were administered. The patient had no episodes following
colchicine treatment. The follow-up 24 hour urinary protein was 420 mg/day
after three months.
CASE 3
A 65 year-old male patient presented with complaints of swelling on his
feet and shortness of breath. Past medical history includes diabetes and
hypertension for last 20 years and coronary artery disease for a year. Upon
further investigation, we learned the patient has episodes of abdominal pain,
fever and joint pain for 40 years, which significantly have increased over the
last 20 years. He has children who have been diagnosed with FMF. Blood pressure
was 160/90 mm Hg, heart rate was 63 bpm, body temperature was 36.5 C. Rales
were auscultated upon pulmonary and the patient had pretibial edema
bilaterally. Blood analysis revealed BUN level 46 mg/dL (9-23), creatinine 5.1
mg/dL (0.9-1.3). Urinalysis revealed proteinuria (++++), hematuria, a 24 hour
urine total protein of 6.8 g/day and a creatinine clearance of 30 mL/minute.
Ophthalmologic examination for investigating diabetic retinopathy was negative
for retinopathy. A heterozygote E148Q mutation was discovered with FMF gene
analysis. Serological tests of hepatitis markers, ANA, Anti-ds DNA, p-ANCA,
c-ANCA, AntiGBM antibodies were all negative and C3 was low and C4 was within
normal limits. Renal biopsy showed an increase of mesangial matrix and cells,
consistent with MsPGN and negative for Congo red. Colchicine tablet 2¡Á0.5 mg/day,
azathioprine 2¡Á50 mg/day and
valsartan 160 mg/day were administered. The patient presented to the ER with
uremic symptoms two months later and underwent hemodialysis. During the
follow-up period, the patient was started on a hemodialysis program.
CASE 4
A 29 year-old female patient was diagnosed with FMF based on fever and
joint pain 7 years ago. She was on colchicine tablet 3¡Á0.5 mg/day. FMF
gene analysis revealed a heterozygote M680I mutation. Upon physical and
laboratory examination, her blood pressure was 120/80 mmHg, creatinine was 0.68
mg/dL, urinalysis revealed protein (+) and 24 hour urinary protein was 1.2
gr/day. Serological tests for hepatitis markers, ANA, Anti-ds DNA, p-ANCA,
c-ANCA, Anti-GBM antibodies were all negative and C4 was within normal limits
and C3 was low. Renal biopsy showed a mild increase in the mesangial matrix and
mesangial cellularity, C3 (++), focal mesangial deposition of IgG and IgM on
immunofluorescence. Congo red was negative and the diagnosis was reported to be
MsPGN. Azathioprine tablet 2x50 mg/day, prednisolone tablet 30 mg/day and
valsartan 160 mg/day were administered. The 24 hour urinary protein level was
179 mg/day at follow-up 3 months later.
CASE 5
A 55 year-old male patient who had been diagnosed with FMF ten years
previously presented to our clinic. Gene analysis for FMF revealed heterozygote
M694V and heterozygote M680I mutation. The patient was started on colchicine
tablet 3¡Á0.5 mg/day and
had no episodes since treatment began. Blood analysis of creatinine was 0.8
mg/dL, urinalysis of protein (+) and the 24 hour urinary protein was 1.4 g/day.
Serological tests of hepatitis markers were, ANA, Anti-ds DNA, p-ANCA, c-ANCA,
anti-GBM antibodies were all negative and C3 and C4 were within normal limits.
Renal biopsy found intermediate proliferation of mesangial cells, increase of
mesangial matrix and mesangial deposition of C3 (++), mesangial granular
deposition of IgM (+) at immunofluorescence staining and negative for congo red
staining, the diagnosis given was MsPGN. Azathioprine tablet 2¡Á50 mg/day,
prednisolone tablet 30 mg/day and Valsartan 160 mg/day were added to the
treatment plan. Urine protein level was 330 mg/day after 2 months of treatment.
CASE 6
A 32 year-old female patient who was diagnosed with FMF 4 years ago
presented to our clinic. FMF gene analysis revealed heterozygote E148Q. She
responded well to colchicine tablet 3¡Á0.5 mg/day treatment. Physical
examination findings were within normal limits. Upon laboratory blood analysis,
creatinine was 0.9 mg/dL and urinalysis revealed protein (+), 24 hour urinary
protein was 950 mg/day. Serological tests of hepatitis markers were, ANA,
Anti-ds DNA, p-ANCA, c-ANCA, anti-GBM antibodies were all negative and C3 and
C4 were within normal limits. Renal biopsy revealed thickening of the
glomerular basal membrane, moderate staining of basal membrane with C3 and IgM,
Congo red staining was negative and the diagnosis was reported as MGN.
Valsartan 160 mg/day was included in the treatment plan. The 24 hour urinary
protein level was 400 mg/day, measured two months after treatment had been
initiated.
CASE 7
A 37 year-old female patient presented to our clinic with complaints of
swelling of feet, joint pain and proteinuria. Past medical history includes
pulmonary embolism and deep vein thrombosis, subsequently the patient was being
treated with Warfarin. Physical examination findings were, blood pressure of
150/85 mmHg and pretibial edema. Upon laboratory investigation, creatinine
level was 0.7 mg/dL, urinalysis revealed proteinuria (+++), 24 hour urinary
protein was 8 g/day and creatinine clearance was 70 mL/minute. Serological
tests of hepatitis markers were negative, ANA, Anti-dsDNA, p-ANCA, c-ANCA,
anti-GBM antibodies were negative and C3 and C4 were within normal limits.
Mutations of heterozygote P369S and heterozygote M694V were found during FMF
gene analysis. Further, the patient has a known familial history of FMF. The
patient was diagnosed with FMF and prescribed colchicine 3¡Á0.5 mg/day. The
patient was subsequently followed up with a renal biopsy which revealed
thickening of the glomerular basal membrane, granular deposition of C3 and IgG
on glomerular basal membrane and negative for congo red staining; the diagnosis
was reported as MGN. Valsartan 160 mg/day, atorvastatin 20 mg/day, prednisolone
1 mg/kg and 1 g cyclophosphamide monthly treatment administered. The patient
received 6 sessions of cyclophosphamide, but did not responded well to the
treatment (24 hour urinary protein was 12 g/day). When the patient did not
respond to cyclophosphamide treatment, cyclosporine was administered as 200
mg/day. At follow-up visit after three months, 24 hour urinary protein was 197
mg/day.
CASE 8
A 46 year-old patient with a diagnosis of FMF since she was 13 and has
been treated with colchicine 3x0.5 mg/day, presented to our clinic for routine
outpatient follow-up. Several children of this patient have been diagnosed with
FMF. Gene analysis of the patient resulted V726A mutation. Physical examination
revealed a blood pressure of 160/100 mmHg and pretibial edema. Blood analysis
revealed creatinine of 0.25 mg/dL, urinalysis revealed proteinuria (++) and 24
hour urinary protein was 13 g/day. Serological tests of hepatitis markers, ANA,
Anti-dsDNA, p-ANCA, c-ANCA, anti-GBM antibodies were all negative and C3 and C4
were within normal limits. Renal biopsy revealed thickening of the glomerular
basal membrane, granular deposition of C3 and IgG on glomerular basal membrane
and negative for congo red staining, the diagnosis was reported to be MGN.
Valsartan 160 mg/day, acetylsalicylate, atorvastatin 20 mg/day, 1 mg/kg/day
prednisolone and 9 sessions of cyclophosphamide treatment administered. 24 hour
urinary protein at follow-up was 288 mg/day. Azathioprine was included in the
treatment plan.
CASE 9
A 35 year-old male patient was referred to our outpatient clinic with
complaints of swollen feet,fever and joint pain episodes. Gene analysis for FMF
revealed an A744S mutation. Blood pressure was measured as 130/80 mmHg, other
physical examination findings were normal. Blood analysis revealed creatinine
to be 2.3 mg/dL and urinalysis revealed proteinuria (++), 24 hour urinary
protein was 3.4 g/day and creatinine clearance was 40 ml/minute. Serological
tests of hepatitis markers, ANA, Anti-ds DNA, p-ANCA, c-ANCA, anti-GBM
antibodies were all negative and C3 and C4 were within normal limits. Renal
biopsy revealed increase of mesangial cells, global sclerosis, interstitial
fibrosis, tubular atrophy, and mesangial focal staining with C3 and IgM the
diagnosis was reported as immune complex glomerulonephritis, chronic
tubulointerstitial glomerulonephritis and negative for congo red staining.
Valsartan 160 mg/day, prednisolone 30 mg/day, azathioprine 2¡Á50 mg/day and
colchicine tablet 2¡Á0.5 mg/day were administered. At follow-up two months later, the 24
hour urinary protein was 900 mg/day, creatinine was 1.2 mg/day and creatinine
clearance was 60 mL/minute.
Discussion
Proteinuria of FMF patients must make the clinician also consider
non-amyloid glomerular diseases (IgA nephropathy, IGAN, focal and diffuse
glomerulonephritis, MsPGN and rapidly progressing glomerulonephritis). In a
study conducted by a Turkish FMF working group, 2,436 FMF patients have been
evaluated for renal involvement[11]. From these patients, 12.9% had
amyloid deposition, 0.9% had PAN, 2.7% had HSP and 22 patients (0.8%) had non
amyloid glomerular disease. Six of these 22 patients had mesangiocapillary GN,
six of them had MsPGN, five of them had diffuse endocapillary proliferative GN,
one of them had focal glomerular sclerosis, one of them had MGN, one of them
had IGAN, two of them had PAN, four of these patients also had renal amyloiosis[11].
Eliakim et al investigated 106 FMF patients and found 22% of them had
non-amyloid kidney disorders (transient or permanent hematuria, recurrent acute
pyelonephritis, acute post streptococcal glomerulonephritis and other types of
glomerulonephritis)[12]. Kukuy et al describes findings in a
retrospective study that included all patients with FMF undergoing kidney
biopsy for proteinuria > 0.5 g/24 h. They found that among 25 FMF patients,
10 (40%) had nonamyloid kidney disease[13]. Said et al
conducted a study which evaluated renal biopsies of 15 FMF patients with
proteinuria and found amyloidosis in seven of them, MsPGN in six of them, RPGN
in two of them[8].
Studies have
found that vasculites such as polyarteritis nodosa (PAN) and Henoch-Schönlein
purpura (HSP) are more common in patients with FMF compared with the normal
population. Other than reports of HSP and PAN, there are no large
epidemiological studies suggesting that non-amyloid glomerular disease is more
frequent in FMF patients than in the general population[14].
We found MsPGN
in three of nine patients, for which we had kidney biopsies. Two of these
patients had been diagnosed with FMF previously and were receiving colchicine
treatment, in addition to that treatment, azathioprine and prednisolone were also
administered, their proteinuria improved. For the other patient with nephrotic
range proteinuria and impaired renal function, we administered colchicine and
azathioprine. The patient did not responded well to this treatment, upon
follow-up visit three months later, he presented with uremic symptoms and
oliguria; thus he was started on hemodialysis and enrolled in a routine
hemodialysis program. Çağdaş et al. showed that colchicine treatment for an FMF
case with a MsPGN diagnosis made upon renal biopsy provided a complete cure for
this patient [9]. Eroğlu E et al diagnosed a patient with FMF and MsPGN
and the patient responded well to colchicine treatment[15].
Two of our
cases had FMF with IGAN. Two cases had hematuria and non-nephrotic proteinuria,
they had no amyloid deposition. The patients were administered colchicine and
valsartan and but did not received immunosuppressive treatment. During the
follow-up period, we observed a significant decrease in the rate of episodes
and a decrease in proteinuria. Said et al. reported IgA nephropathy in two
patients with FMF in 1988, and noticed significant improvements at kidney
functions with colchicine treatment[16]. Rigante D et al, Gok
F et al, Ceri M et al and G¨¹ll¨¹ et al found IgA
nephropathy with FMF, and these patients responded well response to colchicine
treatment[17-20]. Koukoui L et al. reported a patient with IgA
nephropathy and a carrier of a mutation in the FMF gene (MEFV), in whom
continuous colchicine treatment induced remission[21].
We observed
MGN with three of our FMF patients. Two of these patients were already having
colchicine treatment with FMF diagnosis. One of these patients had
non-nephrotic proteinuria, a decrease at proteinuria only established by ARB
and colchicine. Two other cases with MGN had hypertension and nephrotic
proteinuria, these patients received immunosuppressive treatment. One patient
did not respond to cyclophosphamide treatment, so cyclosporine was administered
and proteinuria improved three months later. Proteinuria of another case
improved with cyclophosphamide. Ceri et al. reported that a patient who was
diagnosed with FMF and MGN initially presented with 2.5 gr/day proteinuria and
with colchicine treatment proteinuria decreased 50% after six months and the patient
was completely cured after 12 months[22].
Immunologic
mechanisms have an important role on FMF pathogenesis. The MEFV gene is
expressed in mature neutrophils and codes pyrin which suppresses inflammation.
Mutated pyrin activates inflammatory cytokines. Increased inflammatory response
of patients with FMF usually facilitates immunogenic glomerular damage.
Colchicine is the most frequently used drug for FMF associated
glomeruloinephritis. It is thought to affect chemotaxis by its influence on
microtubules, thus it limits migration of leucocytes to the inflammatory area.
In addition to that, with its antioxidant effect, it is effective in causing
the remission of proteinuria for patients with MsPGN, IGAN and IgM nephropathy[8,23].
However, this treatment is not effective for patients with FMF and diffuse
proliferative glomerulonephritis. In this case, prednisolone, cyclophosphamide
or azathioprine might be included in the treatment plan[8]. In a
recently published study, a kidney biopsy was performed in 12 patients with FMF
and nephrotic-range proteinuria. It was found amyloidosis in 50% (6/12), focal
segmental glomerulosclerosis (FSGS) in 41.7% (5/12), and MPGN in 8.3% (1/12).
With colchicine and angiotensin converting enzyme inhibitors, a marked improvement
was seen in patients with amyloidosis, but no improvement was seen in patients
with FSGS[24].
Akpolat T et
al have suggested that colchicine prevents glomerular disease, and that the
irregular use of this drug triggers GN attacks[25]. In our study,
four of nine patients were diagnosed as FMF and were receiving regular
colchicine before biopsy. Four patients using regular colchicine, two were
found to have MsPGN and two were found to have MGN. These findings are
inconsistent with other publications that suggest a protective role of regular
colchicine for GN[25].
Homozygosity
for the M694V mutation is a major risk factor for renal amyloidosis in FMF
patients[14]. The role of mutations other than M694V for non-amyloid
glomerular disease is unknown. Our study revealed different mutations in the
same type of glomerulonephritis (Table 1). Further studies are needed to
evaluate an association between mutations and glomerulonephritis types in FMF.
Conclusion
In patients with FMF, glomerulonephritis must be considered as a cause
of non-amyloid renal involvement and kidney biopsies must be obtained. Good
responses may be achieved with colchicine for patients with mild kidney
involvement GN such as IGAN or MsPGN. But in cases of patients with nephrotic range
proteinuria and more severe kidney involvement, immunosuppressive therapy must
be included in the treatment plan. Further studies are needed for assessment of
the relationship between type of glomerulonephritis and FMF gene mutation.
CONFLICT OF INTERESTS
The authors declare no conflict of interest.
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Peer reviewers: Gabriela E. Garcia, Associate
Professor, Department of Medicine, University of Colorado Denver, 12700 East
19th Avenue, MS C281, Aurora, CO 80045, USA; Velibor Tasic, MD, PhD, Professor,
Department of Pediatric Nephrology, University Children¡¯s Hospital, 17
Vodnjanska, 1ooo Skopje, Macedonia.
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