Journal of Internal Medicine 1994; 2 3 6 : 215-223

Limited joint mobility in type 1 diabetic patients: correlation to other diabetic complications

P. E. T. ARKKILA, I. M. KANTOLA & J. S. A. VIIKARI From the Department of Medicine, Turku University Hospital. Turku. Finland

Abstract. Arkkila PET, Kantola IM, Viikari JSA (Department of Medicine, Turku University Hospital, Turku, Finland). Limited joint mobility in type 1 diabetic patients : correlation to other diabetic complications.

Objectives. To examine the association between limited joint mobility (LJM) and complications of diabetes in adult patients with type 1 diabetes. Design. Cross-sectional study in diabetic patients and healthy controls. Setting. The study was performed at the department of medicine in Turku University Hospital (n = 103), a private diabetes outpatient clinic (n = 153) and the municipal health centre of Turku (n = 29), Finland. Subjects. We studied 285 diabetic patients [age (meanf SD): 33 .4k 10.0 years] and 288 healthy nondiabetic controls [age (meanf SD): 32.3 k9.21. Main outcome measures. The limitations of several joints were examined with a goniometer. The diabetic patients were assessed in terms of the following complications : background and proliferative retino- pathy, peripheral symmetrical polyneuropathy, auto- nomic neuropathy, impotence as well as clinical and incipient nephropathy ; serum lipid values were also

Intern Med 1994; 236: 215-223.

measured. Results. The prevalences of LJM were 58% and 14% in diabetic patients and in healthy controls, re- spectively. The diabetic patients with LJM had a 2.8- fold risk of proliferative retinopathy [9 5% confidence interval (CI): 1.1-7.31 and a 3.6-fold risk of nephro- pathy (95% CI: 1.4-9.3) compared to patients without LJM, when the confounding effect of the duration of diabetes was excluded. LJM was not related to metabolic control of diabetes, micro- albuminuria, autonomic neuropathy or impotence. The association between LJM and peripheral sym- metrical polyneuropathy was exclusively explained by the duration of diabetes. The correlation between LJM and serum total and low-density lipoprotein cholesterol was dependent on the association be- tween LJM and nephropathy. LJM did not relate to serum high-density lipoprotein cholesterol or tri- glyceride values. Conclusions. The diabetic patients with LJM had an increased risk of proliferative retinopathy and nephropathy compared to patients without LJM.

Keywords: Diabetic complications, limited joint mobility, type 1 diabetes.

Introduction Several abnormalities of the upper extremities have been described in diabetic patients. In 1957, Lund- baek reported stiff hands in four diabetic patients who had had diabetes for more than 20 years [l]. Diabetes is also associated with the carpal tunnel syndrome [2], flexor tenosynovitis [3] and peri- arthritis of the shoulder [4]. A syndrome of painless finger joint stiffness in diabetic patients was initially described in 19 74 [ 51. The stiffness usually begins in the metacarpophalangeal (MCP) and proximal inter-

phalangeal (PIP) joints of the fifth finger and extends medially, but larger joints can be involved also. This syndrome of limited joint mobility (LJM) is associated with the microvascular complications of diabetes [6-81 and may precede the development of micro- vascular diabetic complications. LJM might thus be useful for identifying patients at increased risk of microvasculopathy, although this remains to be proven in prospective studies [6, 91.

There are less data available on LJM in adult patients with type 1 diabetes. The purpose of this study was to examine more closely the association

215

216 P. E. T. ARKKILA et al.

between LJM and complications of diabetes in this LJM' was defined as hand deformity at rest or population. associated cervical spine involvement. The repro-

ducibility of this method was tested in 23 diabetic subjects by remeasuring the limitation of the joints by goniometer after 2-12 months. Eighteen subjects Study population

We evaluated 285 (138 men and 147 women) type 1 diabetic patients [age (meankSD): 33 .4k 10.0 years]. Patients attending the department of medicine in Turku University Hospital ( n = 103). a private diabetes outpatient clinic ( n = 153) and the mu- nicipal health centre of Turku (n = 29), Finland were invited to participate in the study; all were consecutive patients seen at these three outpatient clinics during 3 months in autumn 1991. The average age, diabetic control and duration of diabetes were similar in the patients from all three referral centres. A total of 288 nondiabetic subjects (hospital staff) [age (meankSD): 32.3k9.21 with no known musculoskeletal complications or other significant illness, including a history of hand injury or infection, served as controls.

Methods Limited joint mobility was assessed in both upper extremities by the method of Rosenbloom by one observer [6]. The patients were asked to place the palmar surfaces of the fingers in a praying position with the fingers fanned and the wrists maximally flexed. If the patient failed to achieve complete fanning of the fingers, the examiner attempted to extend the patient's fingers. The passive extension of the third and fifth metocarpo phalangeal (MP) and wrist joint was recorded bilaterally with a gonio- meter. The extension of the elbow and ankle joints was also examined. Normal extension was described as a minimum of 180" for the proximal inter- phalangeal (PIP) and distal interphalangeal (DIP) and a minimum of 60" for the MP. The wrist should extend to at least 70" and the elbow to at least 180". The lateral flexion of the cervical spine was tested by asking the patient to touch the ear to the shoulder.

Joint mobility was classified according to the following criteria : ' no LJM' includes equivocal and unilateral findings, or refers to simply a sense of resistance without limitation ; 'mild LJM' indicates involvement of one or two PIP, one large joint or only the MCP joints bilaterally: 'moderate LJM' refers to involvement of three or more PIP or one finger joint and one large joint bilaterally : severe

(six with no, six with mild, five with moderate and one with severe LJM) had the same result in both measurements. One subject with mild LJM was found to have no LJM, one without LJM was found to have mild LJM and three subjects with mild LJM were found to have moderate LJM in the remeasurement.

Dupuytren's contracture (DC) was defined as a visible and/or palpable thickening of the palmar fascia surrounding the flexor tendons of the fourth and fifth and also the second and third fingers.

The criteria for shoulder capsulitis were shoulder pain for at least 1 month, an inability to lie on the affected shoulder, and restricted active and passive shoulder joint movements in at least 3 planes.

All subjects gave a detailed history. Special em- phasis was placed on the age at the onset of diabetes, the duration of diabetes and insulin treatment. The weight and height were measured and the body mass index (BMI) was calculated from the formula BMI = weight (kg)/[height (m)]'. The occupation of subjects (manual or intellectual work) was recorded as was the history of injuries, operations or infections in the upper extremities.

The metabolic control of diabetes was evaluated by the annual average glycosylated haemoglobin A,, (GHbA,,) value, which had been determined one to five times a year over the past 5 years. GHbA,, was determined by fast protein liquid chromatography (Pharmacia. Uppsala, Sweden). Serum creatinine, cholesterol, high-density lipoprotein (HDL) choles- terol and triglyceride concentrations were measured with a fully automated analyser (Hitachi 704; Hitachi Ltd, Tokyo, Japan); a kinetic Jagffe method (Boehringer Mannheim GmbH, Mannheim, Ger- many) was used to determine serum creatinine, and enzymatic methods (Boehringer Mannheim GmbH) for the other blood chemistry values. HDL cholesterol was measured after polyethyleneglycol (final con- centration 10%) precipitation [ 101. The low-density lipoprotein (LDL) cholesterol values were calculated by the formula of Friedewald et al. [ l l ] . Twelve-hour nocturnal urine samples were collected from 207 subjects, each of whom was instructed in writing to avoid exercise; only light indoor walking was al- lowed. The urine volumes were measured and the albumin concentrations were analysed after centri-

LIMITED JOINT MOBILITY IN DIABETIC PATlENTS 217

fugation from dipstick-negative samples by nephelo- metry (Behring nephelometer analyser ; Behring, Marburg, Germany) [ 121. Microalbuminuria and macroalbuminuria were considered to be present when the urinary albumin excretion rate (UAE) exceeded 20 but was less than 201 pg min-’ and when the samples were dipstick-positive. Before establishing the presence of nephropathy-associated micro- or macroalbuminuria, other causes of al- buminuria such as physical exercise, intercurrent essential hypertension and urinary tract infection were carefully excluded.

The state of the retina was assessed by experienced ophthalmologists by fundoscopy after dilation of the pupils with a mydriatic agent. Retinopathy was classified as background or proliferative. Background retinopathy was characterized by microaneurysms, hard exudates, cotton-wool or soft exudates and retinal haemorrhages. Proliferative retinopathy was characterized by neovascularization, fibrous proli- ferations, vitreous haemorrhage obscuring the retina, phthisis bulbi, or enucleation secondary to a com- plication of diabetic retinopathy.

The specific symptoms of peripheral symmetrical polyneuropathy and autonomic neuropathy were pain, paraesthesia, tickling, muscle weakness, pos- tural hypotension and anhidrosis or hyperhidrosis (body, extremities and gustatory). Symptoms caused by hypo- or hyperglycaemia were excluded. The knee and ankle jerks and the vibration sensitivity over the lateral malleoles and in the styloid processes of radius (using a tune fork of 256 Hz) were tested. Patients were considered to have peripheral symmetrical polyneuropathy if they had typical symptoms and impaired vibratory sensibility or if ankle jerks were absent. The motor nerve conduction velocities of the deep peroneal nerves were analysed in 148 subjects by a physician who was blinded to the degree of LJM. The sensory nerve function of the superficial peroneal and sural nerves was tested. Heart rate variation was assessed in 122 subjects by measuring the standard deviation of R-R intervals in the supine position [13] and by calculating the difference between the maxi- mum and the minimum heart rates during deep breathing as described elsewhere [ 141. Patients were considered to have autonomic neuropathy if the heart rate variation was pathological or if they had anhidrosis or hyperhidrosis.

Erectile impotence was defined as the inability to initiate or maintain erection sufficient for satisfactory intercourse and was assessed by personal inquiry,

but no physical examination or additional studies were performed to determine the aetiology of im- potence.

The blood pressure was measured in the sitting position after a period of rest of at least 10 min: a mercury sphygmomanometer was used. The reading when the Vth Korotkoff sound disappeared was taken as the diastolic blood pressure. A subject was defined as having hypertension if he/she used antihypertensive drugs, had a systolic blood pressure greater than 159 mmHg or a diastolic blood pressure greater than 94 mmHg.

The presence of coronary heart disease, any history of myocardial infarction and cerebrovascular disease was recorded.

The smoking history was recorded. An exsmoker was defined as one who had smoked regularly at any time previously.

For statistical analyses, Pearson’s chi-squared test, the one-way analysis of variance (ANOVA) and multinomial polychotomous logistic regression were used [15].

Results

Prevalence of LJM

The overall prevalence of LJM was 58%. One hundred and nineteen subjects were classified as having no, 90 as having mild, 62 as having moderate and 1 4 as having severe joint limitation (Table 1). Only 1 4 out of 52 patients (27%) who had had diabetes for less than 5 years had LJM. The prevalence of LJM was 68% in the subgroup of subjects (1 55) whose diabetes had been diagnosed under the age of 15. LJM was present in 4 1 of 288 (14%) control subjects: all of these had only mild LJM.

The mean duration of diabetes was 18.3 years. LJM was significantly associated with the age of diabetic patients, the duration of diabetes and the age at onset of diabetes (P < 0,001). LJM was not associated with sex, height, weight, BMI or oc- cupation (Table 1). Dupuytren’s contracture was present in 14% of all the subjects and 75% of them had LJM also. LJM was significantly associated with Dupuytren’s contracture (P < 0.05). Ten per cent of the subjects had shoulder capsulitis and 67% of them also had LJM. However, there was no statistical association between LJM and shoulder capsulitis.

Nineteen per cent of the subjects had had some radiologically verified fracture in an upper extremity

218 P. E. T. ARKKILA et al.

Table 1 Characteristics of patients with type 1 diabetes mellitus by the severity of limited joint mobility (LJM)

Diabetic patients Diabetic patients Diabetic patients Diabetic patients without LJM with mild LJM with moderate LJM with severe LJM Total

Study group (n = 119; 41.8%) (II = 90; 31.6%) (n = 62: 21.8%) (n = 14: 4.9%) (n = 285: 100%)

Age (years) mean k SD 30.5 & 8.1 33 .7k 10.9' 37.1k11.0" 38 .6k6.7" 33 .4k 10.0 range 16-60 17-67 17-61 29-59 16-67

Sex

Height (cm) men (% of total) 42.9 53.3 53.2 42.9 48 .4

mean f SD 170 k 8.5 171 k 10.1 171k9 .6 1 6 7 k 8 . 2 170 k 9.3 range 153-190 14 7-1 9 3 152-190 156-1 8 5 147-193

Weight (kg) mean k SD 69 .4k10.5 71k12 .2 7 2 k 13.4 6 4 k 12.8 70k11 .9 range 50-99 47-102 51-116 43-91 43-1 16

BMI (kg m-')

Duration of DM (years) mean f SD 23 .9k3 .0 24 .1k3 .0 24 .7 f3 .2 22 .5k2 .9 24 .1k3.1

mean f SD 14 .0k8 .7 18.9 f 9.2" 23.5 k 8.6** 28.4f5.9** 18.3 k 9 . 7 range 1-48 3-44 4-47 19-37 1-48

mean k SD 8 . 1 k 1 . 5 7 .7k1 .2 8 .3+0.9 7.9 k 0 . 9 8 . 0 k 1 . 2 range 5.8-12.0 5.0-9.4 6.8-10.0 7.0-8.9 5.0-12.0

mean f SD 45.2 f 16.3 48.3 k 16.0 49.1 f 19.1 41 .5k 19.2 46.9 k 17.0

GHbA,, (%) (5 years)

Insulin dose (iu day-')

range 6-100 10-9 8 19-122 2 5-82 6-122 Nonsmokers (% of total) 68.9 65.2 62.9 57.1 65.8 Exsmokers (% of total) 5.0 4 .5 12.9 14.3 7.0 Smokers (% of total) 26.1 30.3 24.2 28.6 27.1

' P < 0.05. **f < 0.01, compared to diabetic patients without LJM.

and one subject had Charcot's joint in the right wrist. Nine patients had been operated on because of the carpal tunnel syndrome. Fourteen subjects had had palmar flexor tenosynovitis of the hand.

The mean levels of GHbA,, during the last 5 years did not differ significantly between the subject groups with different degrees of LJM, nor was there any statistically significant association between the total insulin dose per day and LJM (Table 1).

There was no association between smoking and the prevalence and severity of LJM. Twenty-seven per cent of the subjects were classified as smokers, 7% as exsmokers and 66% as nonsmokers (Table 1). The prevalence of LJM was 60, 70 and 56% in these groups, respectively.

Association of LJM and microvascular complications

Retinopathy. Sixty-five per cent of the diabetic patients had retinopathy (background or proliferative) and 68% of them had LJM. Forty-two per cent of the subjects without retinopathy, 60% of those with background and 85% of those with proliferative

retinopathy had LJM (Table 2). Ten out of fourteen subjects with severe LJM had proliferative retin- opathy (Fig. 1). The correlation between the degree of LJM and background and proliferative retinopathy was significant ( P < 0.001).

Albuminuria. Thirty-eight of 285 (1 3%) diabetic patients had nephropathy-associated macroalbumin- uria and 84% of them also had LJM, whereas 54% of those who had no macroalbuminuria had LJM (Table 2). The correlation between the degree of LJM and macroalbuminuria was significant (P < 0.001). Microalbuminuria was present in 45 of 207 (22%) diabetic subjects and 62% of them had LJM. The frequency of normo-, micro- and macroalbuminuria according to presence and severity of LJM is seen in Fig. 2. The mean duration of diabetes was 20.9 years for the patients who had microalbuminuria and 16.9 years for those who had no microalbuminuria; the mean GHbA,, values were 8.8 and 8.0%, respect- ively, in these groups of patients. Although the mean urinary albumin excretion rate (UAE) was higher in the groups of subjects with LJM compared to that in

LIMITED JOINT MOBILITY I N DIABETIC PATIENTS 219

Table 2 Age. duration of diabetes, GHbA,,. limited joint mobility (LJM) and complications of diabetes

Mean duration Mean age of diabetes GHbA,, (years k SD) (years k SD) (%I

Retinopathy normal 28.448.6 10.8k7.7 background 34.7k9.6 20.9k7.7 proliferative 39.1k9.5 26.1k6.9

no 32.2k9.7 17.5k9.7 Yes 35.8+10.2 23.4k7.5

no 32.5 f 9.4 16.8 f 9.3 Yes 35.1k11.4 20.2k10.2

Macroalbuminuria

Microalbuminuria

Peripheral symmetrical polyneuropathy no 30.3i8.6 yes 38.7k 10.2

no 31.5 k9.3 Yes 37.8k10.6

no 30.6+ 8.2 yes 46.6k10.5

no 31.6 + 9.5 Yes 38.6k9.8

Autonomic neuropathy

Impotence

Hypertension

History of myocardial infarction

no 32.8 49 .6 Yes 53.9 k 7.0

no 32.4k9.3 Yes 45.2 k 11.9

no 33.0k9.9 Yes 46.0k8.6

Coronary heart disease

Cerebrovascular disease

15.0 f 8.8 24.1 f 8.4

16.2k9.1 23.3k9.5

15.3 f 8.6 26.5 k9.2

16.3k9.4 24.5f7.7

17.9k9.4 34.3 f8.8

17.5 k 9.2 28.2 k 10.1

18.0k9.6 28.6f6.3

7.5k1.1 8.3k 1.4 7.9k1.2

8.1k1.6 8.3 f 1.3

8.0k 1.6 8.8+ 1.6

7.9k1.7 8.5k 1.3

7.8 k 1.2 8.5 k 1.4

7.8k1.3 8.4k6.5

8.1 k 1.3 8.3 k 1.5

8.0k1.3 8.9 k 0.5

8 . 0 k 1.3 8 .4k9 .1

S.O+ 1.3 9.3 * 0.0

Present Absent n (%I n

41 (42) 74 (60) 51 (85)

129 (54) 32 (84)

84 (52) 28 (62)

92 (51) 74 (72)

108 (55) 54 (66)

68 (60) 18 (78)

112 (52) 54 (76)

160 (58) 6 (86)

151 (57) 15 (71)

160 (58) 6 (75)

56 50 9

112 6

78 17

90 29

90 28

45 5

102 17

117 1

112 6

116 2

the subjects without LJM; there was no significant association between the degree of UAE and LJM (Fig. 3). Also, a correlation was not found between LJM (classed as no or yes or 14) and diabetic subjects with normo- or microalbuminuria (UAE 21- 200 pg min-'). The mean serum creatinine value (125 pmol L-') of the group of subjects with severe LJM was much higher than the value of the other groups (range 86-98 pmol L-'). However, there was no significant association between serum creatinine and LJM.

Neuropathy. Peripheral symmetrical polyneuropathy was found in 36% of the diabetic subjects and 72% of them had LJM. whereas only 51% of those without neuropathy had LJM (Table 2). There was a con- sistent association between peripheral symmetrical polyneuropathy and LJM (P < 0.001), and also a

pathological electromyography was related to LJM (P < 0.01). Autonomic neuropathy was found in 29% of the patients and 66% of them had LJM (Table 2). Seventy of the 122 patients tested for heart rate variation had LJM. There was no relation between the results in heart rate variation or autonomic neuropathy and LJM.

The prevalence of impotenze was 17% amongst the male diabetic subjects and 78% of them had LJM; 60% without impotence had LJM (Table 2). Joint limitation was mild in half of the impotent males with LJM and only one male had severe LJM and impotence. Impotence was associated with age, the duration of diabetes and autonomic neuropathy (P < 0.001), but not with the mean GHbA,, values or smoking. Impotence was significantly associated with shoulder capsulitis ( P < 0.001) and Dupuytren's contracture ( P < 0.05). When logistic regression

220 P. E. T. ARKKILA et al.

-119 -90 k 6 2 k 1 4

60

m XI .- 3 40 C

20 a

0 I 2 3 4

Fig. 1 Proportion of diabetic patients without retinopathy (a). with background retinopathy (69) and with proliferative retinopathy (a) according to the severity of LJM (1 = no: 2 = mild: 3 = moderate: 4 = severe).

-119

I

n=90

2

e 6 2 n=l4

i n

3 4

Fig. 2 Frequency of macro- (m), micro- (m) and normoalbuminuria (0) according to the severity of LJM (1 = no: 2 = mild: 3 = moderate: 4 = severe).

n=6

T -- 40 t rk38 I

I 2 3 4 WM

Fig. 3 Urinary albumin excretion rate (UAE) in 207 type 1 diabetic patients according to the severity of LJM (1 = no: 2 = mild: 3 = moderate: 4 = severe). Values are meansfSD.

Table 3 Relation between limited joint mobility (LJM) and diabetic complications: the confounding effect of diabetes duration was eliminated by multinomial polychotomous logistic regression analysis

Complica tion

95% Odds Confidence

P-value ratio interval

Retinopathy 0.025 background vs. normal 1.0 0.5-1.9 proliferative vs. normal 2.8 1.1-7.3

Nephropathy 0.018 microalbuminuria vs. normal 1.3 0.6-2.7 macroalbuminuria vs. normal 3.6 1.4-9.3

Peripheral symmetrical NS

Autonomic neuropathy NS polyneuropathy

analysis was used and the effect of the duration of diabetes was eliminated, these associations between upper extremity abnormalities and impotence dis- appeared.

Multinomial polychotomous logistic regression analysis. Because LJM is strongly associated with the duration of diabetes, it is to be expected that LJM correlates with the duration-dependent complications of diabetes such as retinopathy, nephropathy and neuropathy. Because retinopathy and albuminuria were divided into three categories, the associations between the complications of diabetes and LJM were studied by multinomial logistic models. To eliminate any confounding effect of the duration of diabetes, the duration was taken as a covariate. Patients with any degree of LJM had a 2.8-fold risk of having proliferative retinopathy and a 3.6-fold risk of having nephropathy-associated macroalbuminuria com- pared to patients without LJM: there was no as- sociation between background retinopathy or micro- albuminuria and LJM (Table 3). Neither was there any association between LJM and symmetrical per- ipheral neuropathy or autonomic neuropathy.

Dyslipidaemia, hypertension and cardiovascular disease. The mean serum cholesterol concentration was 4.7 mmol L-' in subjects without LJM, 4.8 mmol L-' with mild LJM, 5.5 mmol L-' with moderate LJM and 5.2 mmol L-' with severe LJM. The severity of LJM was related to the serum cholesterol (P < 0.001). Also, a significant correlation was found between LJM and LDL cholesterol values (P < 0.05). which varied from 2.9 mmol L-' in patients without LJM to 3.6 mmol L-' in patients with severe LJM. Subjects with nephropathy had higher total cholesterol, LDL

LIMITED JOINT MOBILITY IN DIABETIC PATIENTS 221

100

- 80 &

B

In c B 6 0 - L

._ S 40- a r

E 2 0 -

cholesterol and triglyceride values (P < 0.01) and lower HDL cholesterol values (P < 0.05) than sub- jects without nephropathy. The association between LJM and total and LDL cholesterol values disappeared when the confounding effect of the correlation between nephropathy and LJM was considered. Mean serum HDL cholesterol values were approximately the same in the four different groups (1.3-1.4 mmol L-'). Mean serum triglyceride values ranged from 1.0 to 1 .3 mmol L-'. No association between HDL cholesterol or triglycerides and LJM was found.

The prevalence of hypertension was 2 5%. Thirty- three per cent of the subjects with LJM, compared to 14% without LJM, had hypertension (P < 0.001). When the duration of diabetes or the age of patients was considered, the difference lost its significance. Twenty-one subjects had coronary heart disease and seven had had a myocardial infarction, but these were not related to LJM. Eight patients had cerebro- vascular disease and six of them had LJM (Table 2).

-

-

Discussion

Prevalence of LJM

Limited joint mobility was present in 58% of diabetic subjects in this study, which compares with the prevalence of 51 and 55% found in earlier studies [7, 161. Only Starkman et al. have reported results of LJM in equally large populations of type 1 diabetic subjects of the same age group [16] ; however, the method for assessing LJM was not as strict as the method used in this study. The prevalence of LJM is lower in children and adolescents because they have had diabetes for a shorter time than the subjects in this study [17. 181; it was confirmed that the prevalence of LJM increases with age and duration of diabetes [7, 191.

Diabetes control

No relationship of LJM to metabolic control of diabetes has been demonstrated in previous studies using either glycosylated haemoglobin levels or blood glucose concentrations [20-221. In this study, no correlation was seen either, although GHbA,, values for the previous 5 years were available. However. an association between control of diabetes and LJM cannot be completely excluded because no data were available of the control in the early years of diabetes.

15

Microvascular complications

The association between LJM and microvascular complications has been identified previously [6, 9 , 231. Rosenbloom et al. have shown that there is an 83% risk of microvascular complications after 16 years of diabetes in patients with LJM, in contrast to a risk of only 25% in patients without LJM [6]. In this study, 53% of the subjects with LJM and 22% without LJM had proliferative retinopathy and macroalbuminuria after an average of 1 6 years of diabetes. Fig. 4 shows that the proportion of diabetic subjects without proliferative retinopathy or rnacro- albuminuria, but with moderate or severe LJM, is much lower than that with no or mild LJM, but not before the duration of diabetes is more than 1 5 years.

Kennedy et al. selected 20 type 1 diabetic patients with, and 20 without LJM matched for duration of diabetes (mean f SEM: 2 1.5 f 1.7 years and 20.5 & 1.7 years, respectively) to study the cor- relation between LJM and retinopathy. Of the LJM group, 75% (versus 40% of the non-LJM group) had retinopathy, but the difference in prevalence of proliferative retinopathy was 70% with LJM and only 15% without LJM [9]. Rosenbloom et al. have shown in subjects with a shorter duration of diabetes that the association between LJM and retinopathy was not dependent on duration of diabetes [23]. They selected five diabetes duration categories and used a log-linear model for statistical analysis. In this study, polychotomous logistic regression analysis was used and it was found that adult type 1 diabetic subjects with LJM have about a threefold to fourfold risk of having proliferative retinopathy and nephropathy,

I I I I I

Dmdur 5-10 11-15 16-20 >20 01

< 5

Fig. 4 Proportion of diabetic subjects without proliferative retinopathy or macroalbuminuria in subjects with no (0). mild (0). moderate (m) or severe (0) limited joint mobility according to the duration of diabetes.

I M H 236

222 P. E. T. ARKKILA et al.

respectively, compared to patients without LJM when the confounding effect of the duration of diabetes is excluded.

The benefit of screening for microalbuminuria has now been well established as an early detector of nephropathy in patients with diabetes [24]. It has also been shown that even a slightly elevated UAE strongly predicts the development of proliferative retinopathy [25]. Because LJM may have an origin similar to that of microangiopathy, one would expect an association between microalbuminuria and LJM. However, this was not seen in this study, which can indicate that LJM is not of clinical value as a marker for subsequent microangiopathy as micro- albuminuria.

Kennedy et al. noted decreased nerve conduction velocity for ulnar and median nerves in older patients with LJM, corrected for duration of diabetes [26]. Beacom et al. established that peripheral neurological function is more impaired in diabetic patients with LJM. However, the duration of diabetes was longer (median 26 years) in their study [8]. Starkman et al. found a significant association between LJM and neuropathy in patients younger than 40 years old and who had had diabetes for less than 20 years [16]. However, the criteria for LJM and neuropathy were not as strict as in this study. When 110 type 1 diabetic patients of approximately the same age group as this study were examined using the same criteria for LJM and neuropathy. no correlation between LJM and neuropathy was found [27]. In this study, a significant correlation between LJM and peripheral symmetrical polyneuropathy was found, but this seemed to be as a result of the duration of diabetes.

There are no previous reports on the frequency of autonomic neuropathy amongst patients with LJM. This study did not show any association between autonomic neuropathy and LJM, although the pro- portional frequency was higher in the groups of moderate and severe LJM. The duration of diabetes and age of the diabetic subjects are higher in these groups.

Erectile impotence occurs on average in 50% of men with diabetes mellitus [28, 291. The low preva- lence (1 7%) in our study was most probably because the diagnosis was confirmed only by personal inquiry. As in other conditions, four major factors must be considered as potential contributors to diabetic im- potence : psychological, hormonal, neural and vas- cular. Also, LJM may be a vascularly related pheno- menon of ageing [30]. We studied the association

between impotence and LJM because it is possible that the same aetiological factors cause impotence and LJM. There was no association between im- potence and LJM or smoking, but we confirmed the dependence of impotence on the duration of diabetes and age. Impotent subjects had more pro- nounced autonomic neuropathy than nonaffected subjects. There was a significant association between impotence and shoulder capsulitis and Dupuytren’s contracture, but these associations were simply caused by a longer duration of diabetes.

Dyslipidaemia

According to Starkman & Brink, there is no cor- relation between fasting triglyceride or cholesterol values and LJM [31]. In a recent study, the angle of the MCP joints was significantly correlated with dyslipidaemia (high triglyceride and low HDL chol- esterol), but the confounding effect of diabetes duration or nephropathy was not excluded [32]. Type 1 diabetic patients with normal renal function and macroalbuminuria have several abnormalities of serum lipids and lipoproteins that probably pre- dispose to atherosclerosis [33]. In this study, LJM was associated with total serum cholesterol and LDL cholesterol values, but the relation seems to be dependent on the association between LJM and nephropathy. There was no significant correlation between LJM and serum HDL cholesterol or tri- glycerides. Six out of seven patients with myocardial infarction had LJM-the small number of patients does not allow any firm conclusions. This study does not support the concept that macrovascular disease is aetiologically related to LJM, especially as no correlation between HDL cholesterol or triglyceride and LJM was found. However, it should be remem- bered that, for example, the total concentration of LDL cholesterol may not reflect the true athero- genecity of LDL. which is modified by glycosylation in diabetic patients [34].

Conclusions This study shows that LJM is common in adult patients with type 1 diabetes and that it is associated with microvascular complications of diabetes, in- dependent of the duration and the control of diabetes. Although LJM is related to retinopathy and clinical nephropathy, LJM was not associated with micro- albuminuria. LJM is not related to autonomic neur- opathy and the relation to peripheral symmetrical

LIMITED J O I N T MOBILITY I N DIABETIC P A T I E N T S 2 2 3

neuropathy was simply due to the duration of diabetes. We also showed that the association be- tween LJM and serum total cholesterol and LDL cholesterol are a result of the association between LJM and nephropathy, and LJM as such is not related to HDL cholesterol or triglyceride values.

Acknowledgements This study was financially supported by a grant from the Research and Science Foundation of Farmos.

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Received 13 December 1993. accepted 7 February 1994.

Correspondence: Ilkka M. Kantola MD. Department of Medicine, Turku University Hospital, 20520 Turku. Finland.

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