Insensitivity, limited joint mobility, and plantar ulcers in patients with diabetes mellitus.

Insensitivity, Limited Joint Mobility, and Plantar Ulcers in Patients with Diabetes Mellitus Plantar ulcers in patients with diabetes mellitus (DM) are a significant problem. Levin reports that 20% of all diabetic patients entering the hospital are admitted because of foot problems. [1] These troublesome foot ulcers can become infected and lead to amputation. The National Commission on Diabetes reported that an estimated 5% to 15% of diabetic patients will require a lower extremity amputation at some point in their lives. [2] Most and Sinnock also report that 45% of all lower extremity amputations are in patients with DM and that diabetic patients have a risk rate 15 times higher than nondiabetic patients. [3] Given that the cost for total diabetic care in the United States is over $14 billion, the economic impact of foot problems is staggering. [1]

Many factors can contribute to plantar ulcers in diabetic patients, but the two major factors are believed to be angiopathy and neuropathy. Neuropathy is currently recognized as the primary factor leading to plantar ulceration. [1,4,5] Levin describes the sequence of ulceration secondary to neuropathy involving sensory, motor, and autonomic nerve fibers. [1] Sensory loss can allo painless trauma, and motor neuropathy can lead to muscle atrophy and foot deformity, which causes increased pressure on parts of the insensitive foot. [4h Autonomic neuropathy leads to decreased perspiration, which causes dry, cracking skin. Brand has long emphasized the role of decreased sensation and concurrent increased, repetitive mechanical pressures as principal causative factors in ulceration. [4] Several studies have reported successful healing of diabetic plantar ulcers in the presence of vascular disease through the use of total contact casting, [6-9] a method that reduces the mechanical pressure at the site of ulceration. [10]

Brand described the gradual decrease in sensation seen in diabetic patients and noted a certain "threshold" of insensitivity they reach that puts them at risk for ulceration. [4] Birke and Sims used Semmes-Weinstein (SW) monofilaments to define this threshold in a group of 72 patients with Hansen's disease and 28 patients with DM. They reported that 4.17, 5.07, and 6.10 monofilaments are "a reliable set of testing instruments at the 95% confidence interval" and that the 5.07 monofilament was the best indicator of "protective sensation." [11] Recently, Holewski et al confirmed the SW monofilament to be a reliable measurement tool and the 5.07 monofilament as a "risk discriminator" for ulceration. [12]

Numerous factors may increase local pressures on the insensitive foot and lead to ulceration. [4,13] In addition to obvious deformity, limited joint mobility (LJM) of the foot and ankle may decrease flexibility and increase susceptibility to ulcertation. Limited joint mobility has been well documented in the upper extremity of patients with insulin-dependent diabetes mellitus (IDDM) [14-16 and recently in the shoulders of patients with non-insulin-dependent diabetes mellitus (NIDDM). [17] Rosenbloom and others have documented thickening of periarticular connective tissue of the finger joints as a common finding in children and adults with IDDM. [14-16] There is growing evidence that the prolonged state of hyperglycemia and insulin deficiency causes a diffuse nonenzymatic glycosylation of a variety of tissues including periarticular connective tisse. [18] In addition, the skin around the joints has been described as thick, tight, and waxy. [14-16] Studies have shown relationships between early diabetic complications and LJM in the hands or upper extremities. [5,19] To date, very little information has demonstrated simlar LJM in the feet of diabetic patients. The only reference to LJM in the feet we could locate at the initial submission of this article was an article by Larsen and Holstein, who found 18 of 272 diabetic patients with skin lesions of the feet showing "rigidity of the toe," which they believed contributed to ulceration of the tip of the big toe. [20] Recent articles by Birke et al [21] and Delbridge et al [22] have also identified LJM in the metatarsophalangeal joint of the great toe and in the subtalar joint (STJ). These authors also hypothesize that LJM contributes to plantar ulceration.

Limited dorsiflexion (DF) could result in increased pressure on the forefoot, particularly during the late stance phase of gait. [23] Because the STJ has been described as important in the absorption of transverse rotation and impact of the lower extremity during gait, limitations in this joint could place increased stress on the plantar skin surface. [23]

The purpose of this study was to determine whether differences in sensation, ankle DF, and STJ motion exist between 1) diabetic patients with a history of plantar ulcer (DMW Group), 2) diabetic patients without a history of plantar ulcer (DMWO Group), and 3) a nondiabetic control group (NDC Group). The null hypothesis was that there would be no significant difference in sensation, DF, or STJ range of motion between the groups.

Method

Subjects

Subjects in the DMW and DMWO Groups were drawn consecutively from the outpatient physical therapy department at the Irene Walter Johnson Rehabilitation Institute and the Diabetic Foot Center at Washington University Medical School. The NDC Group was composed of various staff members and patients in the medical center and spouses of patients in the DMW and DMWO Groups. Criteria for inclusion in the DMW Group was that patients had been diagnosed with IDDM or NIDDM and at some time had experienced a plantar ulcer. Patients diagnosed with DM having no report of a plantar ulcer were placed in the DMWO Group. Subjects with no history of DM or plantar ulcer were placed in the NDC Group. Exclusion criteria for all groups were a history of rheumatoid arthritis or severe trauma to the foot or ankle.

Table 1 contains descriptive data for subjects participating in the study. Mean age across all groups was 60 [plus-or-minus] 11.3 years. There were 31 male and 39 female subjects. When the data were subjected to t and chi-square tests, no statistical difference was demonstrated between the groups in distribution of age or sex. Duration since diagnosis of DM was reported as 19 [plus-or-minus] 9 years for the DMW Group and 13 [plus-or-minus] 7 years for the DMWO Group (t = 2.4, p [is less than] .05). Two patients in the DMW Group were classified as having IDDM because they had an early age of onset (less than 35 years old) and were prone to developing ketoacidosis. Most of the remaining patients in the two diabetic groups received insulin therapy to improve glycemic control (at the discretion of their primary physician). All subjects consented to participate in the study, which was approved by the Human Studies Committee at Washington University Medical School.

Procedure

All measurements of DF, STJ ROM, and sensation were taken by the same two physical therapists (MJM or JED). The testers had extensive experience taking the measurements on diabetic patients and developing intertester consistency. Interrater reliability coefficients of these measures taken on a group of 31 patients with DM by the same testers were acceptable (Tab. 2). [24] In addition to the reliability coefficients, we calculated Pearson product-moment correlations (r) to determine standard error of the mean (SEM) (Tab. 2). All measurements were taken with the patient in the prone position with the foot and ankle overhanging the end of the table. Goniometric measurements were taken with a plastic goniometer with 6-in(1) arms and the scale marked in 2-degree increments. Passive DF was measured at the talocrural joint with the knee extended and the STJ in neutral (Fig. 1). [25] Passive STJ ROM was assessed by measuring maximal calcaneal inversion and eversion as described elsewhere. [25] One arm of the goniometer was aligned with the bisector of the distal one third of the lower leg, and one arm was aligned with the bisector of the calcaneus (Fig. 2). The examiner positioned the goniometer with one hand and maximally inverted or everted the calcaneus with the other.

Sensation at the plantar surface of the foot was measured using 4.17, 5.07, and 6.10 SW monofilaments similar to the method described by Birke and Sims (Fig. 3). [11] Sites for testing were 1) the first, third, and fifth toes and metatarsal heads; 2) the medial and lateral midfoot (at base of fifth metatarsal); and 3) the heel. The monofilament was pressed perpendicular to the surface of the skin with enough pressure to bend the monofilament. The higher the value of the monofilament, the more difficult it is to bend. Five to 10 trials were taken at each site, and the subjects needed to perceive 80% of the trials to be graded the monofilament value used in these trials at that site. If they were unable to sense at least 80% of the trials, they would be tested with the next higher monofilament. Subjects unable to sense 80% of the trials using the 6.10 monofilament were graded the value [ is greater than] 6.10. The highest perceived monofilament value was taken as the overall grade of the foot. Operational definitions of the level of sensation based on the perception of the given value of the SW monofilament are provided in Table 3.

Data Analysis

The following data were obtained bilaterally and analyzed between groups: sensation, DF, STJ ROM (total excursion), calcaneal inversion, calcaneal eversion, and side of the ulcer. Goniometric data were analyzed for differences between groups using one-way analyses of variance (ANOVAs). [26] If a significant F ratio was obtained, Tukey's post boc analyses were carried out to establish which groups were significantly different. We considered using a single two-by-three ANOVA but did not because 1) we considered the goniometric measures as separate, dependent measures and 2) we believed we would lose information (ie, left vs right, inversion and eversion vs STJ ROM) that clinicians may be interested in. Sensation measurements were analyzed using a Kruskal-Wallis orderedscale test. The alpha level for all comparisons was established at .05.

Results

Mean DF for the DMW, DMWO, and NDC groups was 2, 5, and 7 degrees, respectively. Mode values for sensation with Semmes-Weinstein monofilaments were 6.10, 5.07, and 4.17. Mean STJ ROM was 26, 31, and 35 degrees, respectively. A summary of the ANOVA results showed significant F ratios (p [is less than] .05) for all measurements (Tab. 4). Post boc analyses revealed significant differences between the DMW Group and the NDC Group in sensation and all ROM measurements. Significant differences between the DMW and DMWO Groups were noted in eversion, DF, and STJ ROM, all bilaterally. The only motion that was more limited for the DMWO Group compared with the NDC Group was eversion on the right side. In addition, results of the Kruskal-Wallis test showed significant differences in sensation between all groups (Tab. 5), with a clear trend for decreased sensation bilaterally across a continuum from NDC Group to DMWO Group to DMW Group. All patients in the DMW Group had severely decreased or absent sensation (values of 6.10 or [is greater than] 6.10 SW monofilament).

Discussion

There was no significant difference in the distribution of age or sex between the three groups. There was, however, a significant difference in duration of DM between the DMW and DMWO Groups (19 [plus-or-minus] 9 vs 13 [plus-or-minus] 7 years, p [is less than] .05). These results are consistent with the findings of Boulton et al [5] and Holewski et al [12] who reported duration of DM in groups of diabetic patients with and without plantar ulcers as 16 [plus-or-minus] 1 versus 10 [plus-or-minus] 1 years and 18 [plus-or-minus] 2 versus 9 [plus-or-minus] 1 years, respectively. Furthermore, these results suggest diabetic patients are increasingly susceptible to plantar ulcers with increasing duration of disease. It appears patients with DM for 16 to 19 years are particularly at risk, but certainly other factors contribute to ulceration because some patients have DM for more than 16 years without plantar ulceration (Tab. 1). The duration of DM may reflect the prolonged state of glucose nonhomeostasis, which plays a significant role in the development of serious diabetic complications including neuropathic plantar ulcers. [18]

We found a significant difference in the measurements of sensation with SW monofilament between all three groups (p [is less than] .05). Similar to the reports of Birke and Sims [11] and Holewski et al, [12] we found the 5.07 monofilament to be the best discriminator between the diabetic patients with ulceration and those without ulceration. No patients with ulceration in this study were able to sense the 5.07 monofilament in the region of their ulcer, although several were able to sense the 6.10 monofilament. We choose to grade the foot conservatively by assigning the highest monofilament size the patient can sense because sensation above 5.07 would put that portion of the foot, and therefore the whole foot, at risk. Because the tool is a good discriminator, relatively inexpensive, and shown to be reliable in the hands of different clinicians, [11,12,24] we believe the monofilament can be an excellent screening tool in the assessment of the diabetic foot.

Although foot deformities are common and rather obvious in many patients with DM, decreased ROM is more subtle. We found a significant difference between the amount of DF and STJ ROM between the DMW Group and the NDC Group (p [is less than] .05) but not between the DMWO Group and the NDC Group. Root et al report that 10 degrees of DF is required at the talocrural joint with the STJ in neutral for normal ambulation. [23] Less than 10 degrees of DF could increase the pressure under the forefoot, particularly when the tibia rolls over the foot during the late stance phase of gait. Increased pressure in this region is particularly important, given that most plantar ulcers occur under the forefoot. [6,11] Although the NDC Group also showed a mean DF of less than 10 degrees, they did not have plantar ulcers. Insensitivity appears to be the additional factor that must be coupled with LJM or foot deformity to produce a plantar ulcer.

The STJ is important in absorbing transverse rotation of the lower extremity during gait. [23] If this normal transverse rotation is not absorbed at the STJ (because of LJM), increased shear forces could result at the plantar surface of the skin. In the presence of insensitivity, these increased shear forces could contribute to ulceration, as seen in the DMW Group.

To further assess the hypothesis of LJM contributing to plantar ulcerations, we retrospectively compared the foot with the most LJM with the side of ulceration in the DMW Group. We operationally defined the foot with the most LJM in each patient using the decision tree shown in Figure 4. Using these criteria, we found that the side of greatest LJM matched the side of the ulcer in 79% of the patients. Using a binomial distribution, the probability of matching the side of greatest LJM with the side of the ulcer 79% of the time is less than .05. Again, a close association between LJM and plantar uclers is suggested.

Although patients with plantar ucleration had a greater incidence of insensitivity and LJM than patients without plantar ulcerations, we cannot conclude from the results of this study that insensitivity or LJM causes plantar ulcers. We theorize that LJM contributes to increased pressure on the insensitive plantar aspect of the foot, but we did not directly measure this pressure. Perhaps patients develop LJM as a result of the ulcer, subsequent edema, immobilization, or the reduced activity level the ulcer may impose on them. Although these factors may contribute to LJM in the feet, LJM and insensitivity (apart from ulceration) have been well documented as sequela of DM. [14-19] In addition, the DMWO Group showed no ulceration but significantly less sensation than the NDC Group. Based on the results of this study, we hypothesize that diabetic patients with sensation values greater than 5.07 (as measured with SW monofilament), DF less than 5 degrees, and STJ ROM less than 30 degrees are at greater risk for developing a plantar ulcer. A prospective longitudinal study that includes a good indicator of diabetic control should be undertaken to determine whether this hypothesis is true.

Structures potentially contributing to LJM include skin, muscle, tendon, ligament, joint capsule, and bony components. Retrospectively, we noted a lack of any solid end-feels. Therefore, it was our clinical impression that the LJM in the talocrural joint and the STJ was not of bony origin. In addition, the skin overlying the STJ appeared thick, tight, and waxy as described elsewhere with LJM. [14] Hence, the LJM appeared to be due to periarticular limitations (ie, muscle, tendon, joint capsule, ligament, skin), all potentially amenable to physical therapy intervention. Further research is needed to specifically identify the structures causing LJM and determine which physical therapy techniques are most successful in improving it.

Conclusions

Decreased sensation and LJM were seen more often in the DMW Group than in the NDC Group. No patients in the DMW Group were able to sense the 5.07 SW monofilament. In addition, plantar ulceration was most often seen on the foot showing the most LJM. We propose that a sensory examination with the SW monofilament is a good screening method for patients at risk of developing plantar ulcers, although joint motion of the feet should also be addressed. We believe those patients screened and found unable to sense the 5.07 monofilament on any portion of the plantar aspect of the foot or showing less than 5 degrees of DF or less than 30 degrees of sTJ ROM should be provided with appropriate treatment including education in foot protection methods, accommodative footwear, and mobility exercises.

(*1) in = 2,54 cm.

References

[1] Levin ME: The Diabetic Foot, ed 4. Philadelphia, PA, C V Mosby Co, 1988, pp ix-50

[2] Report of the National Commission on Diabetes, Volume 3, Part 2. US Dept of Health, Education and Welfare Publication No NIH 77-1022. Washington, DC, US Government Printing Office, 1975

[3] Most RS, Sinnock P: The epidemiology of lower extremity amputation in diabetic individuals. Diabetes Care 6:87-91, 1983

[4] Brand PW: The diabetic foot. In Ellenberg M, Rifkin H (eds): Diabetes Mellitus: Theory and Practice, ed 3. New Hyde Park, NY, Medical Examination Publishing Co Inc, 1983, pp 829-849

[5] Boulton AJ, Kubrusly DB, Bowker JH, et al: Impaired vibratory perception and diabetic foot ulceration. Diabetes Med 3:335-337, 1986

[6] Sinacore DR, Mueller MJ, Diamond JE, et al: Diabetic plantar ulcers treated by total contact casting: A clinical report. Phys Ther 67:1543-1549, 1987

[7] Diamond JE, Sinacore DR, Mueller MJ: Molded double-rocker plaster shoe for healing a diabetic plantar ulcer: A case report. Phys Ther 67:1550-1552, 1987

[8] Walker SC, Helm PA, Pullium G: Total contact casting and chronic diabetic neuropathic foot ulcerations: Healing rates by wound location. Arch Phys Med Rehabil 68:217-221, 1987

[9] Mueller MJ, Diamond JE, Sinacore DR, et al: Total contact casting in the treatment of diabetic plantar ulcers: A controlled clinical trial. Diabetes Care, to be published

[10] Birke JA, Sims DS, buford WL: Walking casts: Effect on plantar foot pressures. J Rehabil Res Dev 22:18-22, 1985

[11] Birke JA, Sims DS: Plantar Sensory Threshold in the Hansen's Disease Ulcerative Foot. Read at the Proceedings of the International Conference on Biomechanics and Clinical Kinesiology of the Hand and Foot. Madras, India, December 16-18, 1985

[12] Holewski JJ, Stess RM, Graf PM, et al: Aesthesiometry: Quantification of cutaneous pressure sensation in diabetic peripheral neuropathy. J Rehabil Res Dev 25:1-10, 1988

[13] Boulton AJ, Betts RP, Franks CI, et al: The natural history of foot pressure abnormalities in neuropathic diabetic subjects. Diabetes Res 5:73-77, 1977

[14] Grigic A, Rosenbloom AL, Weber TF, et al: Joint contractures common manifestation of childhood diabetes. J Pediatr 88:584-588, 1976

[15] Rosenbloom AL, Silverstein JH, Lexotte DC, et al: Limited joint mobility in childhood diabetics indicates increased risk for microvascular diseases. N Engl J Med 305:191-194, 1982

[16] Rosenbloom AL, Silverstein JH, Riley WJ, et al: Limited joint mobility in childhood diabetics: Family studies. Diabetes Care 6:370-373, 1983

[17] Shinabarger NA: Limited joint mobility in adults with diabetes mellitus. Phys Ther 67: 215-218, 1987

[18] Brownlee M, Vlassara H, Cerami A: Nonenzymatic glycosylation and the pathogenesis of diabetic complications. Ann Intern Med 101: 527-537, 1984

[19] Starkman HS, Gleason RE, Rand LI, et al: Limited joint mobility of the hand in patients with diabetes mellitus: Relation to chronic complications. Ann Rheum Dis 45:130-135, 1986

[20] Larsen K, Holstein P: Abnormal extension of the big toe as a cause of ulceration in diabetic feet. Prosthet Orthor Int 11:31-32, 1987

[21] Birke JA, Cornwall MW, Jackson M: Relationship between hallux limitus and ulceration of the great toe. Journal of Orthopaedic and Sports Physical Therapy 10:172-176, 1988

[22] Delbridge L, Perry P, Marr S, et al: Limited joint mobility in the diabetic foot: Relationship to neuropathic ulceration. Diabetic Med 5:333-337, 1988

[23] Root ML, Orien WP, Weed JH: Clinical Biomechanics: Normal and Abnormal Function of the Foot. Los Angeles, CA, Clinical Biomechanics Corp, 1977, vol 2, pp 37-41, 168-175

[24] Diamond JE, Mueller MJ, Delitto A, et al: Reliability of a diabetic foot evaluation. Phys Ther, to be published

[25] McPoil TG, Brocato RS: The foot and ankle: Biomechanical evaluation and treatment. In Gould JA, Davies GJ (eds): Orthopaedic and Sports Physical Therapy. St Louis, MO, C V Mosby Co, 1985, vol 2, pp 313-341

[26] BMDP2V (Analysis of Variance and Covariance Including Repeated Measures), BMDP3S (Nonparametric Analysis): Program Version, 1987. Los Angeles, CA, BMDP Statistical Software, Inc, 1987

M Mueller, MHS, PT, is Instructor, Program in Physical Therapy, Washington University Medical School, and Physical Therapist, Department of Physical Therapy, Irene Walter Johnson Rehabilitation Institute, 509 S Euclid Ave, St Louis, MO 63110.

J Diamond, BS, PT, is Physical Therapist, Department of Physical Therapy, Irene Walter Johnson Rehabilitation Institute.

A Delitto, MHS, PT, is Instructor, Program in Physical Therapy, Washington University Medical School, and Consulting Physical Therapist, Department of Physical Therapy, Irene Walter Johnson Rehabilitation Institute.

D Sinacore, MHS, PT, is a physical therapist and a doctoral student, Department of Anatomy, School of Medicine, West Virginia University, Morgantown, WV 26506.

This study was supported by a grant from the Foundation for Physical Therapy.

This article was submitted July 6, 1988; was with the authors for revision for nine weeks; and was accepted February 10, 1989.