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Treatment of Mitochondrial Neurogastrointestinal Encephalomyopathy with Dialysis

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Treatment of Mitochondrial Neurogastrointestinal Encephalomyopathy with Dialysis OBSERVATION Treatment of Mitochondrial Neurogastrointestinal Encephalomyopathy With Dialysis Haluˆk Yavuz, MD; Ahmet O¨ zel, MD; Mette Christensen, MSc; Ernst Christensen, PhD; Marianne Schwartz, PhD; Mithat Elmaci, MD; John Vissing, MD, PhD Objective: To study the effect of continuous ambula- Results: Dialysis stopped vomiting and reduced ab- tory peritoneal dialysis on nucleoside levels and clinical dominal pain, and the patient gained 5 kg in weight and course in a patient with mitochondrial neurogastroin- started to menstruate again. Symptoms returned if dialy- testinal encephalomyopathy (MNGIE). sis was paused. Dialysis did not affect plasma nucleoside levels. Patient: We studied a patient with genetically verified MNGIE, who prior to treatment had lost weight progres- Conclusions: This study shows an unambiguous clini- sively, developed amenorrhea, vomited multiple times cal benefit of peritoneal dialysis on gastrointestinal daily, and had abdominal pain. symptoms in MNGIE. Dialysis did not affect nucleoside levels, indicating elevated thymidine and deoxyuridine Intervention: The patient was treated with peritoneal levels are not solely responsible for the pathogenesis of dialysis for 3 years, and the effect on symptoms and MNGIE. plasma concentrations of thymidine and deoxyuridine were monitored. Arch Neurol. 2007;64:435-438 ITOCHONDRIAL NEURO- treatment for the condition is still lack- gastrointestinal en- ing. In this study, we report the use of con- cephalomyopathy tinuous ambulatory peritoneal dialysis (MNGIE) is a rare au- (CAPD) as a treatment for MNGIE. tosomal recessive mul- tisystem disorder characterized by exter- M REPORT OF A CASE nal ophthalmoplegia, gastrointestinal dysmotility and pain, cachexia, periph- eral neuropathy, and leukoencephalopa- A girl with consanguineous parents pre- thy. The disease is caused by mutations in sented with episodic vomiting and epigas- the gene encoding thymidine phosphory- tric pain at age 15 years. She was cachec- lase (ECGF1).1 Thymidine phosphory- tic (weight, 28 kg; height, 154 cm) and had lase is a cytosolic enzyme that regulates a low blood pressure (85/65 mm Hg). The pyrimidine nucleoside levels by phospho- patient had generalized muscle weakness rolytic catabolism of deoxyuridine and and atrophy, mild bilateral ophthalmople- Author Affiliations: thymidine to uracil and thymine and gia and ptosis, and absent tendon re- Department of Pediatrics, 2-deoxy-D-ribose 1-phosphate. ECGF1 flexes in the lower extremities. Meram Medical Faculty, Selcuk mutations cause severe loss of enzyme Plasma lactate levels were slightly University, Konya, Turkey function in patients with MNGIE, result- elevated (18.4 mg/dL [2.04 mmol/L]; ref- (Drs Yavuz, O¨ zel, and Elmaci); ing in very high concentrations of the erence range, 3-12 mg/dL [0.33-1.33 Neuromuscular Research Unit, nucleosides, thymidine, and deoxyuri- mmol/L). Radiography after barium Department of Neurology dine in extracellular fluids.1,2 Altered thy- ingestion showed an excess of gastric (Dr Vissing), and Department of midine and deoxyuridine metabolism has fluid and gastroptosis (Figure 1), but Clinical Genetics, National University Hospital, been proposed to destabilize mitochon- the intestinal passage appeared normal Rigshospitalet, Copenhagen, drial DNA (mtDNA) by interfering with on imaging. Electrophysiological studies 2 Denmark (Ms M. Christensen mtDNA repair and replication. revealed diffuse, mixed sensorimotor and Drs E. Christensen and Despite significant progress in the mo- polyneuropathy. Brainstem auditory Schwartz). lecular characterization of this disease, evoked potential study results were nor- (REPRINTED) ARCH NEUROL / VOL 64, MAR 2007 WWW.ARCHNEUROL.COM 435 ©2007 American Medical Association. All rights reserved. Downloaded From: https://jamanetwork.com/ on 09/28/2021 The patient was treated with intravenous fluids, dom- peridone, and metiamide with good effect on the eme- sis, but in the following year, vomiting got worse, so that she always vomited after meals. After a vomiting epi- sode, the patient developed a generalized tonic-clonic sei- zure. At that time (age 16 years), hemodialysis began 3 times weekly via first femoral, then brachial, catheters. After 2 months of hemodialysis, treatment was shifted to CAPD because CAPD can be performed continu- ously, is better tolerated by most patients, and can be per- formed outside the hospital. Continuous ambulatory peri- toneal dialysis is performed with 1200 mL of 1.5% glucose dialysis fluid every 3 hours. The procedure of emptying and refilling the peritoneum with dialysis fluid takes 10 minutes and is performed by the patient. At the time of publication, the patient had been treated with CAPD for 3 years. Only a few CAPD-related problems occurred dur- ing this period (leaking dialysis fluid from the catheter, 1 episode of mild peritonitis, and occasional right shoul- der pain). Magnetic resonance imaging and visual evoked potential and brainstem auditory evoked potential studies were repeated after 2 years of CAPD. Plasma levels of thymidine and deoxyuridine were measured before, during, and after 1 hemodialysis and 4 CAPD Figure 1. Contrast radiograph demonstrating marked gastroptosis. treatments. Thymidine and deoxyuridine levels were also measured in dialysis fluid during 3 CAPD treat- ments. Samples were injected into a high-performance liquid chromatograph (Alliance model 2690; Waters Corporation, Milford, Mass) equipped with a photodi- ode array detector (model 996; Waters Corporation) operating at 254 nm and recording UV-visible absorp- tion spectra (200-400 nm). All compounds were iden- tified by their retention times and by comparison of their absorption spectra with those of commercially available products. GENETIC AND METABOLIC FINDINGS Sequencing of ECGF1 revealed homozygosity for a pre- viously described splice-site mutation (IVS9-1GϾA),1 con- firming the diagnosis of MNGIE. The parents and an asymptomatic sister of the proband were heterozygous for this mutation. Thymidine and deoxyuridine levels were decreased by hemodialysis from 13 and 22 µmol/L before dialysis to 7 and 9 µmol/L after. Continuous ambulatory perito- neal dialysis, however, had no measurable effect on nucleoside levels (Figure 3), and the levels of these metabolites were elevated 100-fold or more compared Figure 2. T2-weighted brain magnetic resonance image of the patient, with concentrations found in healthy subjects (ie, demonstrating diffusely increased signal in the periventricular white matter. Ͻ0.05 µmol/L). Concentrations of the nucleosides in the dialysate were on average one third of plasma levels mal, but visual evoked potential studies showed pro- (Figure 3), and it can be calculated that approximately longed P100 latency. T2-weighted brain magnetic reso- 100 µmol of both thymidine and deoxyuridine were nance imaging showed increased signal affecting the removed daily by dialysis. Thymine and uracil were not periventricular white matter of the frontoparieto- detected in plasma or dialysate at any time. Plasma lac- occipital regions (Figure 2). On suspicion of MNGIE, tate levels ranged between 33 mg/dL [3.66 mmol/L] and we measured plasma thymidine and deoxyuridine levels 52 mg/dL [5.77 mmol/L] during the course of CAPD and sequenced all introns and exons of ECGF1, using treatment and were only decreased by 17% on average methods previously described.3 after each dialysis session. (REPRINTED) ARCH NEUROL / VOL 64, MAR 2007 WWW.ARCHNEUROL.COM 436 ©2007 American Medical Association. All rights reserved. Downloaded From: https://jamanetwork.com/ on 09/28/2021 EFFECT OF DIALYSIS ON SYMPTOMS AND SIGNS Before CAPD End of CAPD During CAPD CAPD Dialysate Before hemodialysis, the patient vomited after every meal. 40 Hemodialysis reduced the frequency of vomiting to once every 2 to 3 days. Continuous ambulatory peritoneal dialysis stopped 30 vomiting completely. If the quantity of dialysis fluid was decreased or dialysis was missed, typically because of a long period of sleeping, the patient consistently devel- 20 oped nausea, weakness, and vomiting. Epigastric pain al- most disappeared with the treatment, and the anorexia Micromoles per Liter she had before dialysis treatment improved markedly, so 10 that parenteral food supplementation has not been needed. After starting CAPD, her weight increased by 5 kg to 33 0 kg, and she started to menstruate again. Her height re- Thymidine Level Deoxyuridine Level mained unchanged. Her blood pressure also increased with treatment to on average 100/65 mm Hg. Despite the Figure 3. Mean±SE plasma levels of thymidine and deoxyuridine (n=4) progressive nature of the disease, the patient is able to before, during, and after continuous ambulatory peritoneal dialysis (CAPD) climb stairs more easily and walk longer distances than and their mean±SE concentrations in dialysate (n=3) at the end of dialysis. she could 3 years ago before treatment. The level of oph- thalmoplegia, the absent tendon reflexes, and findings on brain magnetic resonance imaging and results of vi- High extracellular concentrations of thymidine and de- sual evoked potential and brainstem auditory evoked po- oxyuridine have been proposed to induce nucleoside pool tential studies after 2 years of CAPD treatment did not imbalance in mitochondria that compromise mtDNA rep- change. lication and repair, resulting in a progressive develop- ment of deletions, point mutations, and depletion of mtDNA.2,9 Possible therapies for MNGIE could there- COMMENT fore be enzyme replacement
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