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Prevalence of sensorimotor polyneuropathy in the feet at the moment of diabetes mellitus diagnosis^*
(Portuguese PDF version)

Jorge Ricardo de Souza Lira¹, Aldemar Araújo Castro², Guilherme Benjamin Brandão Pitta³, Luiz Francisco Poli de Figueiredo⁴, Valter Mário Moreira Lage⁵, Fausto Miranda Jr.⁶

1. Master's degree student, Vascular, Cardiac, Thoracic Surgery and Anesthesiology, Universidade Federal de São Paulo - Escola Paulista de Medicina (UNIFESP/EPM), São Paulo, SP, Brazil.
2. Master. Assistant professor, Methodology of Scientific Research, Department of Social Medicine, Fundação Universitária de Ciências da Saúde de Alagoas (UNCISAL), Maceió, AL, Brazil.
3. PhD. Associate professor, Surgical Clinic, Department of Surgery, Fundação Universitária de Ciências da Saúde de Alagoas (UNCISAL), Maceió, AL, Brazil.
4. Professor, Surgical Technique and Experimental Surgery, Department of Surgery, Universidade Federal de São Paulo - Escola Paulista de Medicina (UNIFESP/EPM), São Paulo, SP, Brazil.
5. Neurologist, Hospital Regional de Garanhuns D. Moura, Secretary of Health of the State of Pernambuco, Garanhuns, PE, Brazil.
6. Adjunct professor, Vascular Surgery, Department of Surgery, Universidade Federal de São Paulo - Escola Paulista de Medicina (UNIFESP/EPM), São Paulo, SP, Brazil.

* Study performed at the Hospital Regional de Garanhuns, PE, Brazil.

Correspondence:
Jorge Ricardo de Souza Lira
Av. Agamenon Magalhães, 413, Centro
CEP 55290-086 - Garanhuns, PE, Brazil
Phone: +55 (87) 3761.2454
E-mail: jorgelira@bluenet.com.br

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ABSTRACT

Objective: To determine the prevalence of distal sensorimotor polyneuropathy in adults, at the moment of type 2 diabetes mellitus diagnosis.

Method: 113 patients, 70 female (61.9%) and 43 male (38.1%), age varying from 40 to 65 years old, were selected from a total of 2,412 individuals consecutively receiving outpatient care at the Hospital Regional de Garanhuns, from February 2002 to October 2003, where they were submitted to the first diabetes mellitus diagnosis, and later to distal sensorimotor polyneuropathy, through three neurological tests: Ankle jerk reflex, vibration sense with a 128-Hz tuning fork, and plantar tactile sensitivity to the 10-g monofilament. Age, gender, origin, fasting glucose, and neurological tests were analyzed, with which a definite diagnosis was given.

Results: Fasting glucose varied from 126 mg/dl to 440 mg/dl, with an average of 188.1 ± 65.5 mg/dl, with a significant prevalence of concentrations from 170 mg/dl to 319 mg/dl in men. Neurological alterations were diagnosed in 29 patients, corresponding to a prevalence of 25.7% (CI 95% 18.25-34.31%). 23 patients (79.3%) had uni- or bilateral flexor plantar areflexia, 12 (41.4%) had hypopallesthesia, and eight (27.5%) had absence of tactile sensitivity of the foot. There were 10 cases (34.5%) with more than one neurological alteration.

Conclusions: The prevalence of sensorimotor polyneuropathy at the moment of diabetes mellitus diagnosis in the rural area of Pernambuco is three times higher than in developed countries, and it should be considered a major public health problem.

Key-words: diabetes mellitus, diabetic polyneuropathy, neurological exam.

J Vasc Br 2005;4(1):22-6

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Diabetes mellitus (DM) is a multisystemic disease capable of causing several complications, of which the most feared is the lower limb amputation. Regarding this, sensorimotor neuropathy is essentially important, due to the fact that its chronicity and progression will inexorably lead the patent with DM to suffer from diabetic foot, increasing the risk of amputation. The probability of amputation is 15 times higher in individuals with DM than in the non-diabetic population.^1,2

Early diagnosis and a strict control of DM will lead to a delay in the occurrence of the diabetic neuropathy, which is the most predominant complication of this disease, corresponding to more than 50% of all its complications.³ The neuropathy provokes sensorimotor alterations. These induce to the formation of ulcerations that get easily infected, almost always requiring radical treatments. The knowledge of such fact can significantly reduce the incidence of lower limb amputations in diabetic patients, which, according to Brem et al.,⁴ reach more than 82,000 every year only in the United States of America.

The aim of this study is to determine the prevalence of sensorimotor polyneuropathy in the feet of adults from the rural area of Pernambuco, at the moment of DM diagnosis.

PATIENTS AND METHOD

This survey was approved by the ethics committee of the Fundação Universitária de Ciências da Saúde de Alagoas. All patients signed a consent form.

This is a prospective, transversal study, which was performed at the Angiology outpatient clinic of the Hospital Regional de Garanhuns, in the southern rural area of the state of Pernambuco, Brazil. It is a secondary-level, public hospital that serves an estimated population of 500,000 inhabitants from 23 towns in the nearby region.

In order to obtain the size of the estimated sample, 2,412 individuals performed a fasting glucose test, which was assessed from February 2002 to October 2003 in our outpatient clinic, from where we obtained the sample of 113 new cases of DM, later tested to detect the diabetic polyneuropathy.

All consecutive individuals who arrived at the outpatient clinic were included, respecting the following criteria:

• not having a previous diagnosis of DM, including gestational DM for women;
  
• having fasting glucose equal or higher than 126 mg/dl, measured by the researcher.
  

Exclusion criteria were: patients with less than 40 years old or more than 65 years old, those who denied submitting to the physical examination for the survey of sensorimotor characteristics, mentally disabled, amputated of both lower limbs, and patients with peripheral neuropathies of other etiologies previously diagnosed.

The diagnosis of distal sensorimotor polyneuropathy in the new diabetic patients was confirmed by three simple semeiological tests: plantar flexor reflex, vibration sense, and plantar tactile sensitivity. All individuals with glucose level equal or higher than 126 mg/dl meeting the inclusion criteria were assessed, independent from gender or race. Neurological tests were performed at the same time by the researcher and by Dr. Valter Mário Moreira Laje, a hospital neurologist and associate researcher. In order to do this, we used a neurological hammer with a rubber percussive extremity, Semmes-Weinstein nylon monofilament, approximately 5-cm long and with a 10-g pressure when pushed against the skin (developed by the Hansen's Disease Center in Carville, Louisiana),⁵ and a metal tuning fork with a 128-Hz vibratory frequency.

With the patient in a supine position, we inspected both feet and the presence of lesions, according to topography of the foot and laterality of lower limb, which were recorded in our own form. Next, percussion of the Achilles tendon with a neurological hammer was performed. The patient was considered neuropath when there was an absence in the plantar flexor reflex, being recorded the laterality of the ankle.

Afterwards, the vibration sense test was performed, which consists of placing the vibrating 128-Hz tuning fork on the anteroposterior homolateral iliac crest, warning the patients that this vibratory perception should be considered the standard. After a new vibration, the tuning fork was placed on the patella, and the patient was asked to compare both vibrations, informing the intensity of the patella, which was recorded in the form. The same process was repeated, placing the tuning fork on the extreme distal portion of the hallux, whose perception was also compared to the homolateral iliac crest. The vibration sense was classified as normal, when the patient identified a similar sensitivity on the patella and hallux, according to laterality of the assessed lower limb, comparing to that of the homolateral iliac crest; and altered, indicating neuropathy, when the patient reported a reduction or abolition of the vibration sense on any of the assessed topographies.

The plantar tactile sensitivity test was performed with a 10-g monofilament making a 2-second pressure on the plantar surface of the first, third, and fifth metatarsal heads, until the filament bended at 60 degrees. The patient was asked to inform sensitivity without looking at the feet, and results were recorded in the form. The process was repeated on the digital pulp of the first, third, and fifth toes. It was classified as present, when the patient reported sensitivity in all assessed regions, or absent, characterizing neuropathy, when there was a reference of insensitivity in any topography.⁶

To analyze the results, we used the descriptive statistical parameters of the distribution of absolute and relative frequencies, mean, standard deviation, and median. Inferential statistical tests used were the Student's t test for two medians, qui-square test for contingency analysis, all at a significance level (alfa) equal to 0.05.

RESULTS

In the 113 type 2 diabetic patients studied, ages varied from 40 to 65 years old, with mean of 54.2 years old (SD 7.2) (Table 1). Of these, 70 individuals (61.9%) were female, with mean age group of 54.0 year old (SD 7.7) and 43 male (38.1%), with mean age of 54.3 years old (SD 6.3). Means did not differ statistically (p = 0.69).

Table 1 - Distribution of the 113 patients with type 2 diabetes according to age group - Hospital Regional de Garanhuns, February 2002/October 2003

Age (years old)	Frequency	Percentage
40-44	17	15.0
45-49	15	13.3
50-54	32	28.3
55-59	18	15.9
60-64	23	20.4
65-69	8	7.1
Total	113	100.0

 

Regarding origin, 89 patients (78.8%) lived in the urban area of Garanhuns, eight (7.1%) in the urban areas of the 23 towns that form the southern rural area of the state of Pernambuco, Brazil, four (3.5%) outside the rural area of Garanhuns, and 12 (10.6%) in rural areas of other towns from this geographic region.

In the 113 type 2 diabetic patients, fasting glucose varied from 126 mg/dl to 440 mg/dl, with a mean of 188.1 mg/dl (SD 65.5), and a median of 160 mg/dl.

Among these individuals, we found 20 with at least one sign of distal sensorimotor polyneuropathy. Of these, 79.4% (23/29) had absence of plantar flexor reflex, 41.4% (12/29) had an impairment of the vibration sense, and 27.6% (8/29) had absence of tactile sensitivity of the toes.

Considering the sensorimotor polyneuropathy of each patient, 19 cases with only one involvement were diagnosed (65.5% of 29 patients with neurological alterations). Of these, 48.3% (14/29) with Achilles areflexia, and 17.2% (5/29) with hypopallesthesia. 10 patients had more than one neurological alteration (34.5% of 29 patients with neurological alterations). Of these, 13.8% (4/29) with Achilles areflexia + hypopallesthesia and plantar insensitivity; 6.9% (2/29) with Achilles areflexia and hypopallesthesia; 10.3% (3/29) with Achilles areflexia associated to plantar insensitivity, and 3.4% (1/29) with hypopallesthesia and plantar insensitivity.

226 lower limbs were assessed, distributed according to gender and laterality of lower limb (Table 2). There was a prevalence of sensorimotor polyneuropathy at the moment of DM diagnosis of 25.7% (29/113) (CI 95%, 18.25% to 34.31%) of patients from the southern rural area of Pernambuco.

Table 2 - Distribution of abnormal results in neurological tests performed in 226 lower limbs of 113 patients - Hospital Regional de Garanhuns - February 2002/October 2003

Altered diagnostic test and laterality of lower limb	Gender				Total
	Male (n=43)		Female (n=70)
	n	%	n	%	n	%
Right plantar flexor reflex	7	16.3	11	15.7	18	15.9
Left plantar flexor reflex	10	23.2	13	18.6	23	20.4
Vibration sense in the right patella	-	-	3	4.3	3	2.6
Vibration sense in the left patella	-	-	3	4.3	3	2.6
Vibration sense in the right hallux	3	7.0	4	5.7	7	6.2
Vibration sense in the left hallux	3	7.0	5	7.1	8	7.1
Tactile sensitivity in the first right metatarsus	2	4.6	2	2.9	4	3.5
Tactile sensitivity in the first left metatarsus	2	4.6	2	2.9	4	3.5
Tactile sensitivity in the third right metatarsus	-	-	3	4.3	3	2.6
Tactile sensitivity in the third left metatarsus	1	2.3	1	1.4	2	1.8
Tactile sensitivity in the fifth right metatarsus	3	7.0	1	1.4	4	3.5
Tactile sensitivity in the fifth left metatarsus	2	4.6	1	1.4	3	2.6
Tactile sensitivity in the first right digital pulp	2	4.6	1	1.4	3	2.6
Tactile sensitivity in the first left digital pulp	2	4.6	2	2.9	4	3.5
Tactile sensitivity in the third right digital pulp	1	2.3	2	2.9	3	2.6
Tactile sensitivity in the third left digital pulp	1	2.3	2	2.9	3	2.6
Tactile sensitivity in the fifth right digital pulp	3	7.0	1	1.4	4	3.5
Tactile sensitivity in the fifth left digital pulp	2	4.6	1	1.4	3	3.5

 

DISCUSSION

The diabetic foot is extremely susceptible to the development of trophic foot lesions. Every effort should be made in order to prevent the occurrence of such lesions. The physician who carries out the initial assessment must have this knowledge.

Any foot lesion, such as a callus, a fissure in the heel, an interdigital mycosis must be faced as a potential trigger of limb loss or death.⁷

DM is the most frequent cause of amputations worldwide. In the United States, diabetic patients constitute 51% of total patients submitted to lower limb amputation. From 9% to 20% of these individuals will suffer a new amputation (ipsilateral or contralateral) during hospitalization or in the period of 12 months. It is estimated that 5 years after the first amputation, 28 to 51% will have the second limb amputated, and 2/3 will have died.⁸

Diaz,⁹ presented statistical data in which from the total of hospitalized patients with diabetic foot at the hospital José Maria Vargas, in Venezuela, 54.9% underwent some type of amputation. 67.85% were major amputations, and 32.14% were minor amputations. Alcântara,¹⁰ at the Hospital Universitário de Lima, Peru, reports that from the 206 patients hospitalized with diabetic foot, 61.16% were submitted to amputation. In Brazil, Spichler et al.,¹¹ in a study on major lower limb amputations due to peripheral arterial disease and DM, from 1999 to 2000, in Rio de Janeiro, showed that from a total of 3,820 major amputations performed from 1994 to 2000, 50.8% were due to DM and 49.2% due to peripheral arterial disease.

Foliaki¹² understands that there is clear evidence about the possibility of reducing the morbidity-mortality of DM, which will result in the reduction of the risk of its progression to diabetic neuropathy, through an early diagnosis not only of the DM, but mainly of such complication. DM prevention implies in the individuals' education. The best way to avoid a diabetic patient's mutilation is the early diagnosis of the neurological involvement of their limbs, which can be obtained by simple and low-cost tests. Such aspect motivated the present study, since we know that by establishing a basic protocol of peripheral neuropathy detection at the DM outpatient care, and identifying the feet with risk of ulceration, we will be reducing by half the incidence of amputations in our population. The diagnosis of 29 patients with distal sensorimotor polyneuropathy offered them the possibility to learn about basic foot care, reducing their risk of suffering from more serious complications caused by DM. Thus, it can be said that the present study accomplished its social purpose, since it allowed this knowledge to be spread.

In our survey in the southern rural area of the state of Pernambuco, the prevalence of sensorimotor polyneuropathy in the feet of recently diagnosed diabetic patients was 25.7%, corresponding to more than three times the values found by researchers in developed countries. Partanen¹³ in Finland and Pirart¹⁴ in Belgium, with 8.0 and 7.5%, respectively. Although some authors state that the distal sensorimotor polyneuropathy diagnosis should be made based on two or more neurological tests, the methodology of the present survey followed the standards set by the American Diabetes Association, which considers the alteration in a single test as a minimum criterion to make such diagnosis. Therefore, our study can be compared to the study made by Barreira et al.,¹⁵ who adopted the presence of at least one sign of involvement of the peripheral nervous system as a minimum criterion for the diagnosis of diabetic polyneuropathy.

We do not have the sophisticated equipment to make the electrophysiological or biothesiometer exam, in order to measure the threshold of vibration sense suggested by Lawrence et al.,¹⁶ and we believe that the verification of detectable and reproducible clinical signs is more reliable and easier to be reproduced by other researchers than the mere subjective report of symptoms like pain, paresthesia, fatigue, etc. The methodology used in the present survey was the following: choice of three clinical signs obtained through work-up with simple equipment. It could be quantified in Hertz by the tuning fork, in grams by the Semmes-Weinstein monofilament, and by the direct vision of the examiner in case of absence of plantar flexor reflex after percussion of the Achilles tendon with the neurological hammer.

The finding of 25.7% of patients with distal sensorimotor polyneuropathy is actually a concerning figure. If we compare the prevalence found by Partanen,13 which was 8% at the moment of diagnosis, 16.6% after 5 years, and 41.9% after 10 years of DM diagnosis, we can see that this percentage corresponds to the findings among patients suffering from DM for more than 5 years. Such fact leads to the conclusion that this population is exposed to the deleterious effects of hyperglycemia for a long time until the diagnosis is made. The percentage found is more than three times the expected value, which means that this region needs a more efficient health policy to diagnose DM earlier and reduce this index, thus avoiding unnecessary mutilations in individuals often at a productive age.

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