Elsevier

Bone

Volume 105, December 2017, Pages 237-244
Bone

Full Length Article
Immobilization-induced osteolysis and recovery in neuropathic foot impairments

https://doi.org/10.1016/j.bone.2017.09.009Get rights and content

Highlights

  • Before immobilization, foot temperature in Charcot neuroarthropathy subjects were higher than plantar ulcer subjects.

  • Before immobilization, calcaneal BMD in NPU feet averaged 486 ± 136 mg/cm2 and CNA feet averaged 456 ± 138 mg/cm2, p > 0.05).

  • After 14-16 weeks of cast immobilization, NPU feet lost 3 mg/cm2; CNA feet lost 48 mg/cm2 of BMD, p < 0.05.

  • After 33-53 weeks of recovery, calcaneal BMD is blunted in CNA feet compared to NPU feet.

  • After recovery, 61% of NPU index feet and 84% of CNA index feet were classified as osteopenic or osteoporotic, p < 0.05.

Abstract

Background

Neuropathic foot impairments treated with immobilization and off-loading result in osteolysis. In order to prescribe and optimize rehabilitation programs after immobilization we need to understand the magnitude of pedal osteolysis after immobilization and the time course for recovery.

Objective

To determine differences in a) foot skin temperature; b) calcaneal bone mineral density (BMD) after immobilization; c) calcaneal BMD after 33–53 weeks of recovery; and d) percent of feet classified as osteopenic or osteoporotic after recovery in participants with neuropathic plantar ulcers (NPU) compared to Charcot neuroarthropathy (CNA).

Methods

Fifty-five participants with peripheral neuropathy were studied. Twenty-eight participants had NPU and 27 participants had CNA. Bilateral foot skin temperature was assessed before immobilization and bilateral calcaneal BMD was assessed before immobilization, after immobilization and after recovery using quantitative ultrasonometry.

Results

Before immobilization, skin temperature differences in CNA between their index and contralateral foot were markedly higher than NPU feet (3.0 degree C versus 0.7 degree C, respectively, p < 0.01); BMD in NPU immobilized feet averaged 486 ± 136 mg/cm2, and CNA immobilized feet averaged 456 ± 138 mg/cm2, p > 0.05). After immobilization, index NPU feet lost 27 mg/cm2; CNA feet lost 47 mg/cm2 of BMD, p < 0.05. After recovery, 61% of NPU index feet and 84% of CNA index feet were classified as osteopenic or osteoporotic.

Conclusions

There was a greater osteolysis after immobilization with an attenuated recovery in CNA feet compared to NPU feet. The attenuated recovery of pedal BMD in CNA feet resulted in a greater percentage of feet classified as osteoporotic and osteopenic.

Introduction

Neuropathic foot disease is an amalgam of impairments characterized by peripheral neuropathy, vascular disease, skin ulceration, infection, and arthropathy including fracture, joint subluxation and dislocation resulting in non-reducible deformities. Neuropathic foot impairments occur most often in individuals with diabetes mellitus (DM). Two of the most common diabetic neuropathic foot impairments seen either in community clinics or diabetic foot specialty clinics are Charcot neuroarthropathy (CNA) and neuropathic plantar ulcers (NPU) [1], [2]. Both NPU and acute CNA occur in the presence of sensory and autonomic peripheral neuropathy [3], [4]. NPUs often occur in areas of high stresses (pressures) on the weight bearing surface of the foot, frequently in the forefoot or mid foot with deformities [5]. CNA can occur in any of the small joints or bones in the foot and believed to result from unperceived (even repetitive minor) trauma. Some authors suggest CNA often start in the bones comprising the medial column of the foot [6] resulting in progressive foot deformities [7]. Some studies have implicated that low pedal bone density may be an underlying contributor to both neuropathic foot impairments since neuropathic osteopenia has been associated with diabetic metatarsal fractures [8] ankle fractures [9], progression of acquired foot and ankle deformities [10] which too often culminate in lower extremity amputation [11]. Pedal osteolysis may be accelerated by local and systemic inflammation which accompanies the acute onset of both diabetic foot impairments [12], [13].

Both CNA and NPU impairments are commonly managed with pressure off-loading and immobilization [14], [15]. Total contact casting (TCC) is considered the gold-standard method for off-loading and immobilization because it combines maximal protection to insensitive feet and optimal pressure off-loading in high stress areas to rapidly heal plantar ulcers and acute arthropathies [14], [15], [16], [17] yet still allow for protected weight bearing and ambulation. Though TCC is highly effective for ulcer healing and reducing the acute inflammatory stages of CNA, there may be several unavoidable consequences to prolonged immobilization and off-loading including a further acceleration of pedal bone osteolysis [13], [18], [19], [20]. After healing with immobilization, a program of rehabilitation may be beneficial to restore foot and ankle mobility, regain muscle strength and allow a gradual return to walking and weight bearing activities in therapeutic footwear in order to prevent recurrence or subsequent sequelae. A program of rehabilitation may also help the recovery of pedal bone density [18], however, in order for orthopaedic and rehabilitation specialists to design and prescribe optimal interventions to remedy the immobilization-induced consequences, it is important to know the magnitude and time course of recovery from these impairments.

There have been few reports of immobilization-induced pedal osteolysis in individuals with diabetic, neuropathic foot impairments [13], [19], [20], [21], [22] and no previous reports comparing the impact of pedal osteolysis or recovery in individuals with NPU to individuals with CNA. Therefore, we aimed to determine the magnitude of pedal osteolysis in both neuropathic impairments after immobilization and the time course of recovery. The purposes of our study were to determine if there were differences in a) foot skin temperature; b) calcaneal bone mineral density (BMD) loss after immobilization; c) calcaneal BMD loss after recovery; and d) percent of feet classified as osteopenic and osteoporotic after recovery in participants with NPU compared to CNA. We tested the hypotheses that foot skin temperature difference, calcaneal BMD and percent of feet classified as osteopenic and osteoporotic would be similar (i.e., no differences) in diabetic neuropathic participants with CNA and NPU before cast immobilization, after immobilization and after recovery.

Section snippets

Materials and methods

Twenty-eight participants with PN and a unilateral NPU were compared to 27 participants with PN and stage 1 or 2 CNA. Both groups of participants were seeking treatment and followed in our weekly diabetic foot clinic or referred to our physical therapy service for TCC immobilization and off-loading. Inclusion criteria for CNA participants included a radiograph-confirmed overt fracture or arthropathy (subluxation or dislocation) consistent with CNA without evidence of deep or local infection,

Results

Groups of participants were not different in physical characteristics before immobilization except for the location of ulcer or arthropathy, χ2 = 13.25, p = 0.001, (Table 1). All participants had evidence of PN, being unable to sense the 10-gram SW monofilament on > 3 plantar surface locations. Three participants (2 with CNA; 1 with NPU) had PN but no diagnosed DM. The participants were included in our analysis since PN is the major complication that was common to both types of foot impairments.

Discussion

This is the first study to compare calcaneal BMD after immobilization and recovery in two commonly encountered diabetic neuropathic foot impairments. Our results confirm earlier observations that CNA results in a marked local inflammation with concomitant bone loss [4], [12], [13], [20], [26], [38]. Skin temperature in CNA index feet was markedly higher than NPU index feet. These higher skin temperature differences may have likely accounted for the greater osteolysis in CNA index feet compared

Conclusion

Immobilization-induced osteolysis is rapid and profound in individuals with diabetic neuropathic foot impairments, though greater in individuals with CNA perhaps due to a greater inflammation that accompanies CNA compared to NPU. Recovery of pedal BMD after immobilization is highly variable, with an attenuated magnitude in all participants with diabetes and neuropathy, regardless of whether impaired by CNA or NPU. Foot and ankle specialists treating neuropathic foot impairments with

Author contributions

David R. Sinacore, PT, PhD, FAPTA, provided concept, data collection, data analysis, writing, funding support, and review for this study.

Kathryn L. Bohnert MS, CBDT, provided patient recruitment, patient consent, data collection, data base & retrieval and review for this study.

Mary K. Hastings, PT, DPT, MSCI, ATC, provided concept, data collection, data analysis, writing and review for this study.

Michael J Strube, PhD provided research design, statistical analysis, writing and review for this

Acknowledgement

Funded by the National Institutes of Health grant numbers R01 DK59224 (PI: Sinacore) from the National Institute of Diabetes and Digestive and Kidney Diseases), and Washington University Diabetes Research Center P30 DK020579 (PI: Schafer), and Washington University Institute of Clinical and Translational Sciences Multidisciplinary Clinical Research Career Development Program UL1-RR 024992 (PI: Evanoff).

Mary K Hastings PT, DPT was supported by Eunice Kennedy Shriver National Institute of Child

Equipment suppliers

  • a.

    Exergen Model DT1001™ Exergen Corp, Watertown MA, USA.

  • b.

    Tempa-Dot™ 3M Health Care, St Paul, MN, USA

  • c.

    Sahara® Clinical Bone Sonometer, Hologic, Bedford MA, USA

  • d.

    SPSS Version 22.0; SPSS Inc, 233 S Wacker Dr, 11th Fl, Chicago, IL, USA.

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      Rather, so-called non-removable devices imply different physical or psychological thresholds that patients can accept to prevent their future self from removing the device [63]. It is also worth noting that of the reviewed studies only three investigated activity-related side-effects (reporting no [40] or few [55,56] falls and moderate satisfaction with performance of daily activities [41]), although other studies have found that prolonged immobilization of the ankle joint with knee-high devices results in muscle atrophy [64], reduced range of motion [65] and loss of calcaneal bone mass [66]. Thus, future studies should include side-effects of restricted weight-bearing activity from a wider perspective, including both specific bodily side-effects (glycemic control, weight gain, loss of muscle mass, joint flexibility, and bone mass) and a wider health perspective, taking emotional and social aspects into account.

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