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Diabetes & Metabolism
Vol 27, N° 4  - septembre 2001
p. 496
Doi : DM-09-2001-27-4-1262-3636-101019-ART10
Original articles

Prevalence and risk factors of clinical diabetic polyneuropathy in a portuguese primary health care population
 

A.P. Barbosa [1], J.L. Medina [1], E.P. Ramos [2], H.P. Barros And The DPN In Porto Study Group [2],  [3]
[1] Endocrinology Department, São João Hospital, Porto Medical School, Porto, Portugal.
[2] Epidemiology Department, Porto Medical School, Porto, Portugal.
[3] The DNP (Diabetic Polyneuropathy) in Porto Study Group consisted of the following participants: D.M. Moura, Paranhos Primary Health Care Center; B. Vilas-Boas, Aldoar Primary Health Care Center; A.M. Silva, Aldoar Primary Health Care Center; I.A. Pereira, Carvalhosa Primary Health Care Center; J.A. Frey-Ramos, Carvalhosa Primary Health Care Center; M.F. Lima, Carvalhosa Primary Health Care Center; M.R. Lima, Aldoar Primary Health Care Center.

Abstract
Objective

Distal symmetrical polyneuropathy in diabetics (DPN) has a variable prevalence around 30 % and increases the risk for foot ulcers and amputations. We aimed at evaluating the prevalence of clinical DPN and associated risk factors in patients followed in primary care centers.

Material and methods

101 type 2 diabetics were evaluated and 8 were excluded due to the presence of other causes of neuropathy. The remaining 93 had a mean age of 65.4 ± 10.1 years and a mean diabetes duration of 10.1 ± 11.1 years, 60.2 % were women and 39.8 % men. DPN was defined as the presence of both altered sensitivities and reflexes, regardless of symptoms.

Results

Seventy-two (80 %) patients had symptoms of polyneuropathy, but DPN was present only in 29 (32.2 %). Calluses (37.8 %) and trophic skin (74.4 %) and nail (75.6 %) changes were found in both feet. There was a significant positive association of DPN with age (69.0 ± 9.1 vs 63.3 ± 9.9 years, p = 0.01), disease duration (15.7 ± 13.5 vs 7.2 ± 8.8 years, p = 0.001), feet skin changes (38.8 vs 13.0 %, p = 0.04) and myocardial infarction/ischemia (14.8 vs 1.7 %, p = 0.03).

Conclusions

This sample of diabetic patients cared by family doctors presented a high prevalence of DPN. Aging, disease duration, the presence of feet skin changes and myocardial infarction/ischemia are factors that increase the prevalence of the disease. Primary care doctors awareness of the problem might help to decrease the associated morbidity.

Abstract
Prévalence et facteurs de risque de la neuropathie diabétique clinique dans une population portugaise suivie en ville.
Objectif

La prévalence de la polyneuropathie symétrique distale chez le diabétique est variable, autour de 30 %, et augmente le risque de troubles trophiques du pied et d'amputations. Notre but était d'évaluer la prévalence de la ND clinique et des facteurs de risque associés chez des patients suivis en centres de soins de proximité.

Materiel et méthodes

101 diabétiques de type 2 ont été évalués et 8 ont été exclus en raison d'une neuropathie d'une autre origine. Les 93 restants avaient un âge de 65,4 ± 10.1 ans et une durée moyenne de diabète de 10,1 ± 11.1 ans, 60,2 % étaient des femmes. La ND était définie par la présence d'une altération des sensibilités et des réflexes, quels que soient les symptômes.

Résultats

Soixante douze (80 %) patients avaient des symptômes de polyneuropathie, mais la ND n'était présente que chez 29 (32,2 %). Les callosités (37,8 %) et les troubles trophiques de la peau (74,4 %) et des ongles (75,6 %) étaint notés dans les deux pieds. Il y avait une association significative positive entre ND et âge (69,0 ± 9,1 vs 63,3 ± 9,9 ans, p = 0,01), durée du diabète (15,7 ± 13,5 vs 7,2 ± 8,8 ans, p = 0.001), modifications cutanées des pieds (38,8 vs 13,0 %, p = 0,04) et infarctus/ischémie myocardique (14,8 vs 1,7 %, p = 0,03).

Conclusions

Cet échantillon de diabétiques gérés par leur médecin généraliste présente une forte prévalence de ND. L'âge, la durée du diabète, la présence de modifications cutanées des pieds et d'infarctus/ischémie myocardique sont des facteurs qui en augmente la prévalence. La prise de conscience par les médecins généralistes de ce problème peut aider à en diminuer la morbidité associée.


Mots clés : neuropathie diabétique. , facteurs de risque.

Keywords: diabetic neuropathy. , risk factors.


RESEARCH DESIGN AND METHODS

Diabetic peripheral neuropathy (DPN) is one of the most common chronic complications of diabetes, sometimes the initial manifestation of type 2 patients. Although its prevalence varies widely according to classification criteria and patient selection, it is usually present in about 30 % of people with the disease [ [1]]. Clinical neuropathy at diagnosis is observed in 7.5 % of type 2 diabetics, increasing to more than 50 % after 25 years of disease duration [ [2], [3]]. Distal symmetrical sensorimotor polyneuropathy is the most common form of diabetic neuropathy, with an estimated prevalence of 70 % of all symmetrical diabetic polyneuropathies [ [4]]. Although it sometimes surges as a painful syndrome, most frequently it progresses insidiously and symptomless but with sensory loss, predisposing to callus formation that can fissure, infect and ulcerate [ [5], [6]]. Sixty percent of diabetics with ulcers have dominant peripheral neuropathy while 20 % have dominant arterial disease and 20 % have a combination of both [ [7]]. The morbidity of this condition is very high, being responsible for a great number of visits and long time occupied hospital beds, ending many times in lower extremity amputations. About 50-70 % of all nontraumatic lower extremity amputations is due to diabetes [ [8]]. The rate of lower limb amputation is 15 times higher in diabetics [ [9]]. At least half of these are believed to be preventable, and primary care physicians play a major role through potential therapeutic interventions namely regular foot surveillance and patient education. So, there is a need for early diagnosis of DPN in primary care in order to decrease the associated morbidity and mortality.

Our study aimed to evaluate the prevalence of clinical DPN and associated risk factors using a sample of primary care diabetic patients of the north of Portugal.

The study was performed from June 1998 to April 1999 in 3 primary health care centers in Porto, a major town in the north of Portugal. Family doctors recruited all their diabetic patients, explained the nature of the study and obtained informed consent. One hundred and one type 2 caucasian diabetic patients were studied and 8 were excluded due to the presence of diseases potentially causing neuropathy namely traumatic surgery of the foot, rheumatoid arthritis, cerebral vascular disease, vitamin B12 deficiency, hypothyroidism, hyperthyroidism and Parkinson disease. We excluded 3 patients from data analysis because of absent pulses.

The clinical history was recorded by the patient's family doctor and the same endocrinologist performed the physical examination including the neurological one. The clinical history comprised information on diagnosis, chronic complications including previous ulcer/amputation of the lower limbs, type of treatment and symptoms of autonomic and peripheral somatic neuropathy according to the symptoms questionnaire proposed by Dyck [ [10], [11], [12], [13]]. The presence of hypertension, lower-extremity arterial disease, other chronic diseases and medication in the last year including minerals and vitamins were also recorded. Angina and intermittent claudication were evaluated using Rose's questionnaire [ [14]] and the presence of myocardial infarction/ischemia was evaluated by the analysis of the electrocardiogram.

Pressure, pain, cold, vibration and joint position sensitivities were evaluated in both feet bilaterally. Femoral, popliteal, tibial posterior and dorsal pedal pulses and knee and ankle tendon reflexes (with Tromner hammer and using reinforcement) were also evaluated bilaterally. For pressure perception, the Semmes-Weinstein monofilament (10 gram) was used in 10 areas of the foot (9 in the plant and 1 in the dorsum) according to the Bell's sensory testing technique [ [15], [16]]. For vibration perception, a 128-Hz graduated tuning fork (Rydel-Seiffer) was used at the first metatarsal head and in both malleolus. It was recorded the value in a scale from 0 to 8 for which the patient losted vibration perception and values < 4 and <= 2 were considered, respectively, diminished and absent vibration [ [17], [18], [19]]. For pain and cold perceptions, a disposable dressmaker's pin and a cube of ice tested in 4 areas in the plant and 1 in the dorsum were used. For joint position perception, the response to the movement of the first toe was tested with immobilization of the proximal joint. Feet inspection included the skin status (color, thickness, dryness, cracking, trophic changes), the nail status (color, thickness, trophic changes) and the presence of deformity (claw and hammer toes, pes cavus and planus, halux valgus, Charcot's foot), edema, infection (including interdigital fungal), ulceration, calluses and blistering. The muscle strength was also evaluated clinically, considering the finger spread, the great toe extension and the ankle dorsiflexion.

The physical examination included anthropometric measures and the evaluation of postural hypotension. We defined distal symmetrical sensorimotor polyneuropathy (DPN) as the presence of both altered (diminished or absent) sensitivities and absent reflexes bilaterally, with or without symptoms of peripheral somatic neuropathy including burning, shooting or stabbing pains, pins and needles, numbness or deadness based on the staging of diabetic peripheral neuropathy described by Boulton AJM

et al.

[ [1]].

Laboratory studies included hemogram, venous blood glucose, hemoglobin A1c, uric acid, renal, thyroid and liver tests, lipids, microalbuminuria and vitamin B12.

Alcohol and smoking habits were recorded as self-reported. Patients were considered current drinkers if they had at least 1 glass/week, occasional drinkers if < 1 glass/week and ex-drinkers if they had stop drinking at least 6 months ago. They were considered smokers if they smoked at least once a day, occasional smokers if less than once a day and ex-smokers if they had stop smoking at least 6 months ago.

Subjects were considered hypertensive if on medication or had systolic blood pressure >= 140 mmHg and/or diastolic blood pressure >= 90 mmHg.

Statistical analysis: quantitative variables were expressed as mean ± SD and were compared using Student's

t

test. Proportions were compared using the chi-square test with a correction for continuity or the Fisher's exact test. P values < 0.05 were considered statistically significant.

RESULTS

The main characteristics of the evaluated 93 patients (37 (39.8 %) men and 56 (60.2 %) nonpregnant women) are presented in Table I

.

Women had a mean age of 65.2 ± 9.8 and men 65.2 ± 10.6 years. Most patients, 67.7 % were married. Mean education was 4.6 ± 3.2 years and 11 (11.8 %) patients were illiterate. Fifty-three (57.6 %) patients were retired and 16 (17 %) were household women. The diabetes was treated in 32.3 % of patients only with diet or physical exercise, in 61 (65.6 %) with oral antidiabetics and in 2 (2.1 %) with insulin.

Family history of diabetes was present in the parents in 35 (37.6 %) and in the brothers and sisters in 43 (46.2 %) patients.

There were no patients on dialysis. Only one patient had undergone vascular surgery of the lower limbs, but there were no cases of previous amputation, and 7 (7.5 %) patients had previous history of lower-extremity callus or ulceration. Ten (11.0 %) patients had previous history of angina, 6 (6.7 %) had electrocardiographic evidence of myocardial infarction/ischemia and 68.8 % patients were hypertensive.

Women had a mean height of 154.3 ± 6.7 cm and men 167.1 ± 7.0 cm.

We excluded 3 patients because of absent pulses. The symptoms of neuropathy and the physical examination are described in Table II

.

There were no cases of muscle atrophy nor changes in muscle strength. Edema was present in the dorsum of one or both feet in 11.1 % of patients. Foot deformity was detected in 36.7 %.

Means of hemoglobin A1c were 8.3 ± 1.9 and 68.5 % of the patients had it >= 7 %, HDL was <= 0.9/1.15 mmol/l (35/45 mg/dl) in 28.9 %, 20.2 % had triglycerides >= 2.3 mmol/l (200 mg/dl) and LDL was > 2.6 mmol/l (100 mg/dl) in 93.3 %. Microalbuminuria was negative (< 30 mg/dl) in 58.3 %, positive in 41.7 % and > 300 mg/24 h in 3.6 % of patients.

When we compared the patients with DPN with the patients without DPN, we found a significant positive association with age (p = 0.011), with disease duration (p = 0.001), with skin changes (p = 0.043) and with myocardial infarction/ischemia (p = 0.032). There was a non significant positive association of DPN with hypertension. There were negative associations but non significant with calluses, nail changes, smoking, alcohol intake, hemoglobin A1c >= 7 %, microalbuminuria, HDL <= 0.9/1.15 mmol/l, LDL > 2.6 mmol/l and triglycerides >= 2.3 mmol/l.

There were no associations of DPN with height or BMI in both sexes, even when analysed separately. Males had more prevalent DPN than females but it was not significant (Table III)

.

DISCUSSION

We used simple clinical criteria to define neuropathy without referring to electrodiagnostic studies. To our knowledge, this is the first epidemiological study that reports the prevalence and associated risk factors of DPN in Portugal. Although the sample is relatively small, it reflects a primary care diabetic population of the north of the country. We found a prevalence of DPN of 32.2 %, similar to those previously reported in other populations [ [1]]. Veglio examined the prevalence of diabetic neuropathy in Italy using the questionnaire, the neurological examination, the vibration sensation and 2 cardiovascular tests and found a prevalence of asymptomatic and symptomatic neuropathy of 7.2 and 21.3 %, respectively [ [20]]. Fedele in a multicenter study in Italy found a prevalence of 32.3 % using the diabetic neuropathy index [ [21]]. Adler in a prospective diabetic foot study found that 20 % of patients developed neuropathy [ [22]]. Also in England, Walters [ [23]] and Young [ [24]] using clinical criteria found prevalences of 16.3 % and 28.5 %, respectively. In a recent study, Cabezas-Cerrato found a prevalence of clinical DPN in Spain of 22.7 % [ [25]]. Nevertheless, in comparison with these 3 later larger studies which included hospital patients, in whom active complications are usually followed, the prevalence we found is very high.

Although the majority of patients with DPN progress insidiously and without symptoms, in our study symptoms were present in 80 % patients, mostly non-painful, such as numbness and pins and needles.

In our study, we found significant positive associations with age and disease duration, two largely correlated factors. Thus, aging is a possible confounding factor of the association of DPN with the duration of diabetes.

Height has been previously described as a risk factor, probably because it is a marker of neuronal length, so longer neurons are at greater risk for metabolic and/or ischemic injuries [ [26]], but we found no association of DPN with stature.

Hypertension has also been described as an independent predictive factor of DPN in IDDM patients [ [27]] and has been associated with symptoms of sensory neuropathy in NIDDM patients [ [28]]. In our study, despite the existence of a positive association of DPN with hypertension, it was not significant, probably because of the small number of patients.

Young

et al.

demonstrated that the presence of peripheral neuropathy increased the risk for foot ulceration nearly sevenfold, with an annual incidence of first foot ulceration of 4.9 % [ [29]], but Abbott

et al.

found an annual incidence of first foot ulceration in diabetics with significant peripheral neuropathy of 7.2 % [ [30]]. In prospective studies, the three main independent predictors for foot ulceration have been shown to be absent ankle tendon reflex, impaired monofilament pressure sensation and impaired vibration sensation [ [26], [31]]. The inability of a patient to feel the 10g monofilament has been shown to predict lower-extremity ulceration, so it means a loss of the protective sensation in the foot and implies a closer clinical surveillance [ [32], [33]]. Although the majority of our patients had normal pressure and vibration sensations, 31.8 % had distal pressure sensation diminished and in 7.1 % it was absent, while 9.0 % had distal vibration sensation diminished and it was absent in 9.0 %. So, these 2 were the most affected sensitivities in our patients. The ankle tendon reflex was absent in almost half of our patients (40.4 %).

It is also known that the risk of ulcers and lower-limb amputations is increased in males, in patients who have a diabetes duration of 10 or more years, who have poor glycemic control or have cardiovascular, retinal or renal complications [ [34]]. In our study, males had a higher prevalence of DPN than females, but it was not statistically significant. Already in 1979, Pirart [ [2]] found a male predominance and, more recently, Walters [ [23]] found that in type 2 diabetics, more men than women had neuropathy. However, Cabezas-Cerrato [ [25]] and Young [ [24]] found no difference in the DPN rate according to sexes.

In some studies, a previous history of ulceration was the most important predictive factor of subsequent ulceration. Also, plantar calluses were strong predictors for foot ulcers and ulcers recurred only at the site of callus [ [35]]. In our study, only 7.5 % of patients had history of previous callus or ulcer in the feet, there were 2.2 % of cases of blistering but we did not find any ulcers. However, we found a high prevalence of calluses. This high prevalence of calluses and low prevalence of more important complications such as ulcers, probably represents the reality of a primary care center because patients with complications tend to be monitored at the hospital.

Besides neuropathy being one of the most common causes leading to ulceration, minor trauma and foot deformity were also identified as frequent component causes for lower extremity ulceration [ [36]]. In our study, there was a relatively high incidence of deformity, the pes cavus and the halux valgus being the most frequent deformities. Despite the high incidence of skin and nail changes, there were no cases of interdigital fungal infection or ulcers.

In summary, our study showed a high prevalence of DPN and found that age, disease duration, skin changes in feet and myocardial infarction/ischemia are factors associated with DPN and can help identify patients at risk. Also, when symptoms of DPN develop, it should be promptly evaluated. So, an increased awareness by primary care physicians of the high prevalence of DPN and associated risk factors can lead to early therapeutic intervention and prevention of later neuropathic complications such as infection and foot ulcers, allowing a decrease in patient morbidity.Acknowledgements

This study was supported by the Ministry of Health Grant n

o

147/97. The authors acknowledge the collaboration of Dr. A.M. Aroso (North Regional Health Administration; ) and of Drs. A.A. Carneiro (Paranhos and Carvalhosa Primary Health Care Centers- Porto-Portugal. ), M.F. Stanislau

2

and J.L. Catarino

2

. The authors also acknowledge the assistance of Drs. I. Escudeiro

1

and M.P. Silva

1

and of all the nurse staff of the Primary Health Care Centers.

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