Uncommon early-onset neuropathy in diabetic patients
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1 J Neurol (1998) 245 : Springer-Verlag 1998 ORIGINAL COMMUNICATION G. Said A. Bigo A. Améri J.-P. Gayno F. Elgrably P. Chanson G. Slama Uncommon early-onset neuropathy in diabetic patients Received: 29 November 1996 Received in revised form: 4 September 1997 Accepted: 10 Oktober 1997 G. Said ( ) Service de Neurologie, Hôpital de Bicétre, F Le Kremlin BicÍtre, France Tel.: Fax: A. Bigo Centre Hospitalier de Versailles, France A. Améri Service de Neurologie, Centre Hospitalier de Meaux, France J.-P. Gayno Centre Hospitalier de St Germain en Laye, France F. Elgrably G. Slama Service de Diabétologie, Hôtel Dieu de Paris, France P. Chanson Service d Endocrinologie, Hôpital de Bicétre, France Abstract An acute neuropathy rarely occurs early in the course of diabetes mellitus. Five cases are described of adult patients who developed a peripheral neuropathy at the time or shortly after the onset or discovery of diabetes mellitus. Patient 1, an 80- year-old woman who developed a subacute tetraparesis with proximal and distal muscle weakness with normal cranial nerves, proved to have insulin-requiring diabetes mellitus. In the other patients, all men aged years, symptomatic neuropathy occurred simultaneously (patient 2) or 1 6 months after the onset of insulin-dependent diabetes mellitus (IDDM) (patients 3 5). Patients 2 and 3 developed a symptomatic multifocal neuropathy; patients 4 and 5, a painful distal symmetrical sensory polyneuropathy (DSSP) shortly after beginning treatment with insulin. Nerve biopsy showed active axonal lesions in patients 2 and 5 and mixed axonal and demyelinating lesions in the others, with severe axon loss in patients 4 and 5. Vasculitic lesions were found in patient 2, who improved without additional treatment. Neurological examination remained unchanged after 2 years in patients 3 5. Although a coincidence cannot be excluded for patients 1 3, whose neuropathy was not of the pattern commonly found in diabetes, it is suggested that acute disequilibrium in the diabetic status may facilitate the occurrence of a variety of neuropathies. Alternatively, the autoimmune process which led to IDDM may also trigger an autoimmune neuropathy with vasculitis (patient 2) or demyelinative nerve lesions. Only the distal symmetrical sensory polyneuropathy with severe axonal lesions observed in patients 4 and 5 seems directly related to diabetes mellitus. In spite of their occurrence shortly after beginning insulin therapy, the role of treatment with insulin in the onset is uncertain. Key words Peripheral neuropathy Diabetes mellitus Neuropathology Introduction Neuropathy is an important disability factor in diabetic patients and its incidence increases with the duration of diabetes, poor glycaemic control [1] and the age of the patient [2, 3]. Although cardiovascular autonomic function tests can be impaired in newly diagnosed patients with insulin-dependent diabetes mellitus (IDDM) [4], symptomatic neuropathy is uncommon at this stage [reviews in 5, 6]. In some patients, however, other factors are likely to play a role, since severe sensory and autonomic diabetic polyneuropathy may occur early in the course of IDDM, especially in young adults [7]. To illustrate the different patterns of acute neuropathy observed early in the course of IDDM, we report the clinicopathological findings in
2 62 Table 1 Clinical and biological characteristics at onset of neuropathy in diabetic patients with acute early onset polyneuropathy Patient Height (cm), Treatment Haemoglobin Fasting glucose Renal function Retinopathy [Sex, age weight (kg) A 1C (normal: (mmol/l) (normal: (years)] 3 5%) mmol/l) Patient None Serum creatinine: 60 µm/l No F, Patient None Serum creatinine: 62 µm/l No M, Patient Insulin Serum creatinine: 81 µm/l No M, Patient Insulin Serum creatinine: 80 µm/l, No (angiography) M, microalbuminuria-24 mg/24 h Patient Insulin Serum creatinine: 10 µm/l No (angiography) M, five patients who developed neuropathies at the time or shortly after the onset or discovery of diabetes mellitus, and discuss the respective responsibility of diabetes and superimposed factors in the occurrence of these neuropathies. Patients and methods Patients Five diabetic patients were referred to our centre between 1988 and 1993 for evaluation of a neuropathy of early onset. In two patients, the diabetes and neuropathy occurred or were discovered at the same time. All patients were Caucasians and had normal dietary habits. All patients, except patient 2, were under treatment with insulin at the time of neurological investigation, but glycaemic control was poor in all. Causes of neuropathy other than diabetes, including familial, toxic, drug abuse, nutritional, metabolic, dysglobulinaemic, amyloid, inflammatory and paraneoplastic disorders, were carefully excluded by appropriate studies. Patient 2 was later found to have an active hepatitis C virus. All patients had studies of glycaemic control, measurements of glycated haemoglobin (HbA1C) and renal function, ophthalmological examination by a senior ophthalmologist, and routine electrophysiological studies. Retinal angiography was performed in patients 4 and 5 (Table 1). Neurological examination included muscle and tendon reflex testing and evaluation of light touch, pinprick, vibratory and temperature sensation at +4 C and +40 C, and position sense to explore the functions of different subpopulations of axons. Cardiovascular autonomic function was assessed by measurements of the variation in blood pressure and pulse rate in the recumbent and standing positions, and the variation in heart-rate responses to postural change, to the Valsalva manoeuvre and to deep breathing. Neuropathy was the only complication of diabetes in these patients. The clinical data are summarised in Tables 2 and 3. Patient 1 developed a severe quadriparesis within a few weeks, without sensory symptoms. She was negative for a number of antibodies, including to that against Campylobacter jejuni. Electrophysiological testings suggested a mixed axonal and demyelinative polyneuropathy. No conduction block was disclosed. Patient 2 acutely developed a multifocal sensory and motor neuropathy affecting the peroneal nerve on both sides. At the same time, he experienced symptoms related to hyperglycaemia and was found to be diabetic and treated with insulin. He then entered the diabetic honeymoon phase during which insulin was stopped. He was referred for a nerve biopsy 2 months after the onset of neuropathy. Electrophysiological testing showed signs of a mild axonal neuropathy of the peroneal nerve. The patient had mild alterations of liver functions of unknown origin at the time of onset of diabetes. Liver changes were later related to a hepatitis C virus infection. Patient 3 developed a multifocal neuropathy which coincided with beginning treatment with insulin. Patient 4 manifested a polyuro-polydypsic syndrome at the age of 23 years. Two years before, his blood glucose was normal on routine examination. He rapidly lost weight and started to complain of weakness, cramps, burning pains in all four limbs extremities and contact dysaesthesiae. He had no manifestation of autonomic disturbances. Patient 5 developed a polyuro-polydypsic syndrome owing to IDDM at the age of 34 and started to complain of distal numbness in the feet with tingling and pins and needles sensations. He had no manifestations of autonomic dysfunction. The biopsy was performed 4 months after the first symptoms. Follow-up Patient 1 was treated with insulin and received intravenous immunoglobulins and then corticosteroids. She started to recover gradually after 1 year. In patient 2, no residual signs or symptoms of neuropathy were present 3 years after the onset. His general condition deteriorated 7 years later owing to the development of a carcinoma of the liver. No relapse of neuropathy occurred. In patient 3, symptoms improved after a few weeks but signs remained unchanged after 2 years. Patient 4 became pain free after intravenous administration of imipramine at a dose of 100 mg/day for 12 days followed by oral administration of the same dose for 1 year. He remains pain free after 3 years. Patient 5 s neurological condition seems stable after 3 years of follow-up. Morphological study Methods After informed consent, the superficial peroneal nerve and the adjacent peroneus brevis muscle were sampled in patients 1 3, who had a predominant involvement in this nerve territory. The sural nerve was biopsied under local anaesthesia at the ankle level in patients 4 and 5 (see method in [7]).
3 63 Table 2 Neurological findings in diabetic patients with acute early onset polyneuropathy Patient Duration of diabetes at onset of Motor deficit Sensory findings Tendon reflexes Cerebrospinal Follow-up [Sex, age neurological manifestations fluid (years)] Patient 1 Simultaneous discovery of proximal Severe weakness Slight decrease in perception Abolished 0.56 g/l; No improvement F, 80 and distal weakness of all four limbs Strength from 1/5 to of vibrations in distal limbs no cell after 1 year and diabetes 3/5 normal cranial nerves Patient 2 Simultaneous onset of IDDM, Strength at 3/5 in the Numbness without sensory Decreased patellar Normal Recovery within M, 24 paraesthesia and weakness in one leg, right peroneal nerve deficit upon examination and ankle reflexes 4 months then in both territory, 4/5 on the left side Patient 3 Massive loss of weight, sleepiness, Normal strength Decreased vibratory sensation Loss of ankle jerks Normal Neuropathic M, 32 discovery of hyperglycaemia treated over the left foot; hypaesthesia symptoms by insulin. A few weeks later, numbness to pinprick over the antero- disappeared of the posterior and lateral aspects of lateral aspect of the legs and spontaneously, the left leg, then of the right feet signs unchanged Patient 4 A few weeks after the onset of IDDM, Normal strength Distal symmetrical tempera- Normal tendon NA Improvement of M, 23 muscle wasting and painful paraesthesia ture and pain sensory loss of reflexes pain with tricyclic the lower limbs, gloves, an- antidepressants terior aspects of the trunk. i.v.; clinically sta- Normal position sense and ble after 2 years vibratory sensations Patient 5 Paraesthesia of the toes, 2 weeks after Decreased strength stocking hypaesthesia Ankle reflexes NA Clinically stable M, 34 beginningtreatment with insulin of extensor hallucis affecting all modalities of abolished; patellar after 2 years brevis and peroneus sensation normal muscles (4/5) on both sides
4 64 Table 3 Results of electrophysiological and morphological investigations in diabetic patients with acute early-onset polyneuropathy (CMAP compound muscle action potential a, CV conduction velocity, MCV motor conduction velocity b, DL distal latency c, SAP sensory action potential d ) Electrophysiology Teased fibre preparations Fibres percent Density of nerve fibres per mm 2 of endoneurial area Early stages Late stages Segmental Normal of axonal de- of axonal de- demyelina- fibres Myelinated Unmyelinated generation generation tion and/or fibres fibres remyelination Control values < 1 < 1 < 1 > ± ± 4700 Patient 1 Sural nerves: no detectable SAP; peroneal nerve: MCV (left) and 19 m/s; DL: 6.8 (left) and 7 ms (right) Patient 2 Sural nerve: amplitude 15 µv, CV 50 m/s; right peroneal nerve: CMAP 2.5 mv, MCV 42 m/s; left peroneal nerve: High proportion of CMAP 8 mv. CV 48 m/s regenerating fibres Patient 3 Left sural nerve: SAP µv, 24.1 m/s; right peroneal nerve: MCV 31.1 m/s, CMAP 7.3 mv, DL 7.5 ms; right Long demyeliposterior tibial nerve: MCV 28.3 m/s, DL 10 ms, CMAP nated segments 14.8 mv; left median nerve: MCV 43.3 m/s, CMAP 20.2 mv Patient 4 Right sural nerve: SAP: 6.5 µv, CV 27.2 m/s; right peroneal nerve: DL 6.6 ms, CMAP 6 mv; left side: DL 4.4 ms, MCV: 24.8 m/s, CMAP 7 mv Patient 5 Right sural nerve: SAP 6 µv, 35.5 m/s; right peroneal nerve: MCV 18.5 m/s, DL 7.1 ms, CMAP 0.5 mv; right median nerve: MCV 42 m/s, DL 3.7 ms, CMAP 6 mv, F wave latency 35.9 ms a CMAP normal values: > 4 mv c DL normal values: < 5 ms b MCV normal values: > 45 m/s d SAP normal values: > 10 µv
5 65 Fig. 1 Histological appearance of the biopsy specimens of the superficial peroneal nerve and of the sural nerves of diabetic patients with different patterns of acute polyneuropathy of early onset. 1-µm-thick cross sections of nerve specimens. Thionin blue staining. Top left Shows several fibres undergoing axonal degeneration (A) in patient 1. M Denotes a macrophage filled with myelin debris. Top right Illustrates the lesions encountered in patient 3 who had a multifocal demyelinative neuropathy. The density of myelinated fibres is preserved. Note the presence of a demyelinated axon (D) and two regenerating axons (R) in the same Schwann cell. Bottom left and right Illustrate the lesions encountered in patient 2 who had a multifocal axonal neuropathy. At bottom left note the epineurial artery (Ar) surrounded by a few mononuclear cells. This vessel was occluded on serial sections, as was the perineurial vessel (V). In the endoneurium, note the presence of degenerating axons (A). Bottom right Fibres undergoing axonal degeneration (A) and regenerating axons (R) not myelinated yet Results The results of the clinical examination are given in Tables 1 3. Patient 1 had a subacute, predominantly motor polyneuropathy affecting all four limbs, without cranial nerve involvement or marked cerebrospinal fluid (CSF) abnormality. Electrophysiological tests suggested a mixed axonal and demyelinating polyneuropathy. Morphological findings showed an ongoing axonal process of recent onset associated with a high proportion of demyelinated fibres, without inflammatory infiltration (Figs. 1, 2). Patient 2 had a multifocal, axonal neuropathy with electrophysiological features of axonal lesions. Morphological examination of the nerve specimen demonstrated non-progressive axonal lesions of recent onset and early signs of axonal regeneration. All affected fibres were at a late stage of axonal degeneration. The density of myeli-
6 66 nated fibres was reduced to 2320 per mm 2. A small epineurial artery was surrounded by mononuclear cells and, on serial sections, the lumen of a perineurial blood vessel was occluded by cells (Fig. 1). On electron microscopic examination, the unmyelinated fibres had a normal appearance and density per mm 2. In patient 3, the density of fibres, both myelinated and unmyelinated, was within the normal range. There was an increased proportion of lympho-monocytic cells in the endoneurium. On teased fibre preparation, there was a high proportion of demyelinated-remyelinated fibres, in agreement with decreased nerve conduction velocity. In patients 4 and 5, the density of myelinated fibres was decreased, and on teased fibre preparations, fibres at different stages of axonal degeneration were isolated, including fibres that had started to degenerate only days before performance of the nerve biopsy, as shown by the amount of myelin debris. These findings indicate that the degenerative process was still progressing. On electron microscopic examination, the density of unmyelinated fibres was decreased in both patients, but more severely in patient 5. No inflammatory infiltrate or blood vessel abnormality was found in patients 4 and 5. Discussion Fig. 2 A C Teased fibre preparations. A Patient 1: group of teased fibres, one of which is demyelinated and remyelinated (a), while the other two are undergoing axonal degeneration. B Patient 4: in this group of fibres, fibre a is demyelinated and remyelinated, fibre b is at a late stage of Wallerian degeneration and fibre c is at an early stage of Wallerian degeneration. C Patient 3: this panel shows consecutive segments of a fibre from patient 3 who had a multifocal demyelinative neuropathy. The fibre shown is demyelinated between a b, d e, f g, i k, n o and p q. Paranodal demyelination is present around nodes of Ranvier c, l and m. The fibre is thinly remyelinated between nodes k and node n The patients included in this series represent a heterogeneous group illustrating different patterns of acute polyneuropathy encountered very early in the course of IDDM. In diabetic neuropathy, the duration of diabetes prior to the onset of the neurological symptoms may vary from several weeks to several years [8], yet the average duration of the diabetes prior to the onset of clinical neuropathy was 5.9 years in Jordan s series of 120 cases [9]. In 28 of them, however, diabetes had been present for 1 year or less. As emphasised by Pirart and Coërs [10], early complications of diabetes are usually seen in association with old age, poor control or a long period of unrecognised diabetes, which was the case in the 82 patients with early neuropathy that they observed, and especially in the 13 patients with severe neuropathy. Although this is certainly common in patients with non-iddm (NIDDM), which may remain undetected until the occurrence of symptomatic complications, it is unlikely in patients with IDDM, and well-documented morphological studies of cases of very early onset diabetic neuropathy in patients with IDDM are not available. The pattern of neuropathy observed in patients 1 3 is unusual in diabetes. In patient 1, a severe, predominantly motor, mixed axonal and demyelinative polyneuropathy [11], led to the discovery of diabetes, which required treatment with insulin in patient 1. In patient 2, mononeuritis multiplex occurred at the onset of IDDM, in keeping with occlusion of epineurial and perineurial blood vessels demonstrated on serial sections of the nerve specimen. This patient had been examined a year earlier for hepatitis, which was later found to be caused by a hepatitis C virus and may have played a role in the occurrence of vasculitis. The simultaneous onset of the neuropathy and of IDDM may suggest a common immunological mechanism for both conditions. Patient 3 developed a multifocal inflammatory demyelinative neuropathy at the onset of IDDM, which may also result from an autoimmune mechanism. In contrast, patients 4 and 5 developed a distal symmetrical sensory polyneuropathy, which is the most common pattern of diabetic neuropathy, except for the very early onset in these two patients. Patient 4 presented manifestations comparable with those termed acute painful diabetic neuropathy in male patients [12] or diabetic cachexia [13], yet our patient was neither cachectic nor
7 67 Fig. 3 Patient 5: electron micrographs of thin section of the nerve specimen to illustrate degeneration of unmyelinated fibres. Top panel shows the presence of many pockets of collagen (C), which occupy spaces left empty by degenerated unmyelinated fibres. (B) remnants of basement membrane. Bottom: note a degenerating unmyelinated fibre (D), and the presence of many Schwann cell processes devoid of axons. U denotes an unmyelinated fibre. Uranyl acetate and lead citrate. Bar = 1 µm impotent and was already being treated with insulin. He improved after intravenous administration of imipramine and remains pain free after 3 years. However, considering the already considerable loss of axons, the long-term prognosis looks poor in both patients. Patients 3, 4 and 5 experienced the first neuropathic symptoms shortly after beginning treatment with insulin. Precipitation of sensory neuropathy following the start of treatment with insulin [14] or tight glycaemic control [15] have been observed, but careful study of a nerve biopsy specimen of a patient whose pain increased after the establishment of tight glycaemic control showed no active nerve lesion [15]. In addition, most patients improve in spite of continuation of treatment with insulin, which makes the role of insulin questionable in precipitating a pre-existing neuropathy. In conclusion, symptomatic peripheral neuropathy occasionally occurs very early in the course of IDDM, either as a consequence of severe diabetic disequilibrium or owing to other factors, possibly of autoimmune origin. In all cases, a cause other than diabetes must be carefully excluded by appropriate investigations.
8 68 References 1. The Diabetic Control and Complications Trial Research Group (1993) The effect of intensive treatment of diabetes on the development and progression of long-term complications in insulin-dependent diabetes mellitus. N Engl J Med 329: Pirart J (1978) Diabetes mellitus and its degenerative complications: a prospective study of 4400 patients observed between 1947 and Diabetes Care 1: & Harris M, Eastman R, Cowie C (1993) Symptoms of sensory neuropathy in adults with NIDDM in the U.S. population. Diabetes Care 16: Ziegler D, Gries FA, Spüler M, Lessmann F (1992) Diabetic Cardiovascular Autonomic Neuropathy Multicenter Study Group. J Diabetes Complications 6: Thomas PK, Tomlinson DR (1993) Diabetic and hypoglycaemic neuropathy. In: Dyck PJ, Thomas PK (eds) Peripheral neuropathy. Saunders, Philadelphia, pp Said G (1996) Diabetic neuropathy: an update. J Neurol 243: Said G, Goulon-Goeau C, Slama G, Tchobroutsky G (1992) Severe earlyonset polyneuropathy in insulin-dependent diabetes mellitus a clinical and pathological study. N Engl J Med 326: Goodman JI, Baumoel S, Frankel L, Marcus LJ, Wassermann S (1953) The diabetic neuropathies. Thomas, Springfield, Ill 9. Jordan WR (1936) Neuritic manifestations in diabetes mellitus. Arch Intern Med 57: Pirart J, Coërs CH (1971) Diabetic neuropathy a critical appraisal. Excerpta Medica Foundation Diabetes 1971: Cornblath D, Drachman DB, Griffin JW (1987) Demyelinating motor neuropathy in patients with diabetic polyneuropathy. Ann Neurol 22: Archer AG, Watkins PJ, Thomas PK, et al (1983) The natural history of acute painful neuropathy in diabetes mellitus. J Neurol Neurosurg Psychiatry 46: Ellenberg M (1974) Diabetic neuropathic cachexia. Diabetes 23: Caravati CM (1933) Insulin neuritis: a case report. Va Med Mon 59: Llewelyn JG, Thomas PK, Fonseca V, et al (1986) Acute painful diabetic neuropathy precipitated by strict glycaemic control. Acta Neuropathol 72:
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