Introduction
For patients with relapsing-remitting multiple sclerosis (RRMS), interferon-beta (IFN) is a well-established first-line therapy that is still commonly administered.
Thrombotic microangiopathy (TMA), a group of microvascular disorders with diminished organ perfusion and hemolytic anemia, is a rare yet serious side effect that can arise years after starting IFN therapy [1].
Thrombotic thrombocytopenic purpura (TTP) and hemolytic uremic syndrome (HUS) are the two most common diseases associated with TMA. Ischemia in the brain and other organs is caused by systemic microvascular aggregation of platelets in TTP. In HUS, platelet-fibrin thrombi mostly occlude the renal circulation [2].
TTP is specifically caused by a severe deficiency in ADAMTS13 while HUS is mostly due to a Shiga toxin producing-Escherichia Coli infection. In 10% of the cases, excessive complement activation and membrane attack complex deposits contribute to atypical HUS (aHUS) when one or more regulators of the alternative route of the complement (factor H, factor I, C4b-binding protein, complement receptor 1, CD46) are dysregulated [3,4].
We report herein, a TMA case due to acquired complement factor I deficiency in a patient receiving interferon-beta (IFNβ) for multiple sclerosis.
It’s worth mentioning that there’s relatively little experience with TMA associated with interferon. Particularly those involving immunological testing and complement system study, underscoring the need of reporting such cases today.
Case report
A 28-year-old man was diagnosed with RRMS in 2007. Subcutaneous IFNβ 44 μg was commenced three times a week in 2017. He had no other medical conditions and received no other treatment.
In July 2020, he was admitted to the intensive care unit for a status epilepticus associated with severe arterial hypertension and then transferred to the Nephrology department for management of malignant arterial hypertension with acute renal failure. On examination, he did not present any neurological disorder but had very unbalanced blood pressure under triple therapy. Urine dipstick showed proteinuria +++ and hematuria +++. Biological investigations showed hemolytic anemia (hemoglobin at 9.7 g/dL, elevated LDH
level at 3N, low haptoglobin level < 58.3, elevated reticulocyte count, and presence of schistocytes at 4%), normal platelet count at 165 G/L, renal failure (creatininemia at 146 µmol/L, and urea at 9.1 mmol/L) and hypokalemia at 3 mmol/L. Urinary analysis revealed proteinuria of glomerular origin (7g/day).
Initial immunological investigations showed no complement activation (C3 at 1.08g/l and C4 at 0.32 g/l), undetectable antiphospholipid antibodies (assays for anti-b2-glycoprotein 1 and anticardiolipin antibodies were negative and there was no lupus anticoagulant), negative antinuclear antibodies, negative anti-glomerular basement membrane and positive anti-neutrophil cytoplasmic antibodies (40, N< 20) with no specificity.
This clinical-biological presentation strongly evoked aHUS complicating IFNβ. In addition to treatment discontinuation, the patient received methylprednisolone of 10 mg/kg intravenous for 3 consecutive days switched to oral corticosteroid therapy of 0.5 mg / Kg/day and received supportive treatment including plasma exchange.
Despite the achievement of seven sessions of plasma exchange, the renal failure rapidly worsened and the patient required hemodialysis. A kidney biopsy was therefore indicated and was performed three days after stopping the plasma exchange sessions with a normal hemostasis assessment.
The renal puncture biopsy showed acute and chronic vascular and glomerular TMA (mesangiolysis, reduction of the lumen of the glomerular capillaries, fibrinoid necrosis, mesangial fibrosis, and onion bulb appearance of vessels) with IgG and fibrinogen deposits in the immunofluorescence study (Fig 1, 2&3). The biopsy was complicated by the progressive constitution of a perirenal hematoma leading to a state of hemorrhagic shock which required embolization of two distal arteries.
The patient subsequently benefited from five other plasma exchange sessions permitting the regression of the hemolytic process. However, there was no renal recovery and the patient remained hemodialysis-dependent.
Far from plasma exchanges, we explored the complement system. The results were received lately while the hemolytic process was controlled by standard treatment and showed a decrease in complement factor I: 26,83 mg/l (32,3-87,5). The other proteins of the alternate complement pathway (factor B, factor H, and MCP) as well as the ADAMTS13 activity were within the normal range.
Given the absence of recurrence of hemolysis, no other treatment with rituximab, initially mentioned, was initiated.
At follow-up 6 months later, the patient had not regained kidney function and the complement factor I rate was still low. He remained on hemodialysis and was still taking three antihypertensive treatments.
Two years after the initial diagnosis, he did not experience hematological relapse and remained dependent on hemodialysis. His blood pressure has normalized without antihypertensive treatment and he was desiring cadaveric kidney transplantation. The exploration of the complement system was therefore redone and the activity of factor I was this time normal at 70% (70-100%).