Remote Temperature Monitoring in Patients With Visual Impairment Due to Diabetes Mellitus: A Proposed Improvement to Current Standard of Care for Prevention of Diabetic Foot Ulcers

Abstract

Background:

Two debilitating sequelae of diabetes are foot ulcerations and vision impairing conditions including retinopathy, open-angle glaucoma, and cataracts. Current standard of care recommends daily visual screening of feet. Despite willingness, many patients are impeded by visual impairment. We investigate whether once-daily remote temperature monitoring can improve self-screening for patients at risk for diabetic foot complications.

Methods:

We followed four male veterans with diabetes mellitus, peripheral neuropathy, impaired visual acuity, and at least one other diabetes-related visual impairment in a high-risk podiatry clinic. Patients received a telemedicine remote temperature monitoring mat and instructed on proper daily use. Each patient developed a “hotspot,” defined as a 1.75°C localized temperature difference between matched pedal locations, which resulted in telephone triage outreach.

Results:

In three cases, outreach resulted in a sooner appointment where patients were found to have a relevant outcome at the hotspot. Patients in cases 1-3 had University of Texas (UT) 1A ulcerations. The patient in case 4 had inflammation from trauma. All patients had refractive errors plus another vision impairing condition that potentially delayed identification of lesions. Patients in cases 1 and 2 have cataracts, patients in cases 2 and 3 have retinopathy, and patient in case 4 has glaucoma.

Conclusions:

As an adjunct to daily preventative diabetic self-care, once-daily remote temperature monitoring technology can augment self-screening to prompt necessary outreach and treatment and potentially prevent costly and debilitating diabetic foot complications. This case series serves as a pilot study for real-world application of thermometry, where further large-scale research is needed.

Keywords

diabetic foot ulcer early detection remote temperature monitoring visual impairment

Foot ulcers are a common and devastating complication of diabetes. The global prevalence of diabetic foot ulcer (DFU) is 6.3%, with North America having the highest prevalence at 13%.^1,2 In 2015, the International Diabetes Federation estimated that diabetic foot ulcers develop in 9.1-26.1 million people worldwide annually.^2,3

The development of DFU is associated with significant increased morbidity and mortality. Patients with a DFU are three times more likely to die at any time compared to patients with diabetes without a foot ulcer.⁴ A retrospective study of Veterans Health Administration (VHA) data found the one-year, two-year, and five-year survival rates for veterans who had suffered a DFU to be 81%, 69% and 29%, respectively.⁵ Another retrospective study in veterans found that diabetes-related lower extremity amputations are common and expensive. These investigators reported that the VHA performed 3403 diabetes-related lower extremity amputations (LEA), 2.7 per 1000 veterans with diabetes, in fiscal year 2010, far surpassing the rate of traumatic LEA in veterans. The average inpatient cost associated with each of these diabetes-related LEA procedures (excluding LEA-attributable costs postdischarge) exceeded $60 000 in 2010.⁶

Under current standard of care recommendations, patients with diabetes are educated and instructed by doctors, nurses, or diabetes educators to perform a daily visual foot exam to look for preulcerative lesions, discoloration, and swelling of their feet.^7-10 Education on self-care is imperative because recent research indicates that half of DFUs can be prevented through effective education and 50-70% of lower limb amputations are the result of a DFU.¹¹

Unfortunately, other vision impairing sequelae of diabetes, such as retinopathy, open-angle glaucoma, and cataracts prevent many patients from adequately completing daily self-exams. Advanced diabetes mellitus has been associated with several morphological and functional changes in optical anatomy. Developing over several years, adults with diabetes experience an increase in lens thickness and distortion in the curvature of the lens surface.¹² Hyperglycemia has been associated with myopic refraction, while hypoglycemia has been suggested to lead to the development of hyperopia, or farsightedness.^12,13

Retinopathy affects about a third of all patients with diabetes,¹⁴ causes loss of visual acuity,^15-19 and is an independent risk factor for diabetic foot ulcers (DFU) and amputation.^20-27 In addition to retinopathy, diabetes can exacerbate open-angle glaucoma,^28,29 cataracts,^30-33 and macular edema.^14,34 Due to these increased risks of visual impairment, current guidelines from the American Diabetes Association (ADA) recommend annual eye examinations. Despite patient education and awareness of these risks, one-third of these patients fail to complete annual vision screening.^35,36

Despite patients’ comprehension and willingness to adhere to daily foot exam, vision impairing comorbidities prevent them from performing one adequately. Therefore, it is necessary to develop alternative screening methods for prevention of DFUs. One such modality is thermometry, the use of skin temperature monitoring to detect the inflammation due to repetitive microtrauma or acute injury preceding to skin breakdown.^37,38 Thermometry is evidence based and supported by three randomized controlled trials.^38-40 A recent multicenter cohort study of 132 patients utilizing thermometric foot mat found that the system identified 97% of observed DFUs with an average lead time of 37 days.³⁷ However, the current literature is lacking on the implementation of this technology with appropriate treatment interventions in a real-world setting.

This case series illustrates the implementation of a remote temperature monitoring (RTM) mat (Podimetrics RTM System; Podimetrics, Inc, Somerville, MA) to identify ulcerative and preulcerative lesions to prompt noninvasive intervention in patients with diabetes-related visual impairment who are unable to perform effective daily visual foot exams.^37,41 This easy-to-use smart floor mat contains more than 2000 thermistor sensors. The patient is instructed to stand stationary on the mat once daily for about 20 seconds, after which the data are then wirelessly transmitted to a secure server and automatically analyzed for signs of inflammation.³⁷

Methods

This case series was conducted at a single center (Southern Arizona Veterans Affairs Health Care System). Four male veteran patients were chosen via retrospective chart analysis from the authors’ high-risk podiatry clinic. Patients had previously been screened and prescribed a thermometric smart mat for daily use as an adjunct to standard preventative diabetic foot care. To qualify for the mat at the high-risk podiatry clinic, the patients must have at least three of the following: peripheral neuropathy (per Semmes-Weinstein monofilament testing), peripheral vascular disease, foot deformity, history of foot ulceration, or history of LEA. Due to the small sample size, this study was not required to obtain IRB approval per VA guidelines.⁴²

Patients were asked to stand barefoot on the RTM mat at home for a once-daily foot “scan” at approximately the same time each day. Mat sensors cover the entire mat surface so patients with poor vision do not need precise foot placement³⁷ (Figure 1A). Deidentified thermometric scans are transmitted securely to a remote server. Clinical staff can access foot temperature maps, called “thermograms,” derived from the scans through a secure online physician portal (Figure 1B). These data are used for triage by health providers and to counsel patients. They are recorded in patient’s medical records via clinician note. All data collected, used, and presented herein have been deidentified in accordance with best practices and federal and local regulations.⁴²

Figure 1A.

Figure 1B.

Secure clinician portal to analyze thermograms.

The data collected by the mat are automatically analyzed for temperature differences, or “asymmetry,” between the left and right feet at six locations: heel; arch; first, third, fifth metatarsal heads; and hallux, using the approach most common in the literature.^38-40 Although a threshold of 2.2 degrees of asymmetry has been most commonly described in the literature, the decision to utilize a 1.75 degree threshold was made in an effort to optimize sensitivity.³⁷ A patient with temperature asymmetry exceeding 1.75°C over two or more consecutive uses at the same location triggers a deidentified action-oriented notification and inflammation report from the device manufacturer to the clinical staff. This alert identifies the laterality, anatomic location, and degrees of asymmetry detected. Each asymmetry triggers a phone call for triage. The outreach is done by a designated clinician who contacts the patient and asks for subjective information relating to erythema, edema, contusions, pain, and skin breakdown. If possible, the clinician will guide a caregiver through a visual exam. A protocol has been developed to reduce walking for the next several days, continue offloading footwear, and, if necessary, schedule a sooner appointment date.

This case series was conducted in accordance with VHA guidance on case series. Thermometry is recognized as a component of standard care^43-45 and the device is cleared by the US Food and Drug Administration (K150557) for this intended use. This case series does not constitute research due to small size, lack of testable hypothesis, and practice in accordance with standard of care. Thus, it does not require approval by an institutional review board.⁴²

Results

Case 1 is a 71-year-old male with type 2 diabetes mellitus (HbA1c = 5.6%), neuropathy, B12 deficiency, neurocognitive disorder, hypertension, Charcot neuroarthropathy of the right foot and ankle, hyperopia with astigmatism and presbyopia, glaucoma with borderline ocular hypertension of both eyes, and mild cataract of both eyes.

The patient received telephone outreach due to three consecutive scans with peak asymmetry of 3.1°C localized to the right hallux (Figure 2). The patient performed a visual exam while on the phone and reported no redness, no swelling, no calluses, and no open wounds to the area of clinical concern. He denied trauma, increased activity, or any other changes and elected to keep his routine appointment in two months rather than be seen sooner.

Figure 2.

Localized inflammation hotspot of 3.1°C detected on the right hallux. A superficial plantar hallux ulcer was found.

The following day, the patient called the podiatry department to report that his wife performed a visual exam of the patient’s feet and found an ulcer to the plantar right hallux. He was seen the same day for debridement of a University of Texas Diabetic Wound Classification⁴⁶ UT1A ulcer measuring 0.7 x 0.7 cm x superficial. With proper education of the patient and his wife, proper dressing changes, and offloading, the ulcer healed without any advanced modality in 19 days.

Case 2 is a 68-year-old male with type 2 diabetes mellitus (HbA1c = 6.5%), neuropathy, lumbar post-laminectomy syndrome with radiculitis, degenerative lumbar stenosis, myopia with astigmatism and presbyopia, nonproliferative retinopathy of the left eye, and cataracts of both eyes.

The patient received telephone outreach for an asymmetry of 2.7°C diffusely to the right forefoot (Figure 3). On the phone, the patient reported no knowledge of trauma, change of footwear, or ulceration to the area. He kept his previously scheduled appointment and was seen nine days later. Upon exam, a UT1A ulcer measuring 0.8 x 0.8 x 0.3 cm was discovered after debriding hyperkeratosis of his right plantar 2nd metatarsal head. The patient was given proper toe offloading in conjunction with his diabetic shoes, and the ulcer healed in 33 days.

Figure 3.

Diffuse forefoot hotspot of 2.7°C detected on the right forefoot. Superficial ulcer found plantar to second metatarsal.

Case 3 is a 68-year-old male with type 2 diabetes mellitus (HbA1c = 7.1%), neuropathy, diabetic nephropathy, hypertension, hyperlipidemia, myopia with astigmatism and presbyopia, and proliferative diabetic retinopathy.

The patient received telephone outreach for an asymmetry of 3.7°C to the left hallux (Figure 4). Upon outreach, the patient denied trauma and reported he “didn’t think there was an ulcer” but had pain in the left hallux. The patient has loss of protective sensation.

Figure 4.

Hotspot of 3.7°C detected on the left hallux. A fissure in the hallux sulcus was found.

The following day the patient was seen in clinic. Upon exam, there was a UT1A fissure measuring 1.0 x 1.0 x 0.1 cm in the sulcus of the left plantar hallux. It was debrided and dressed appropriately. His offloading orthotic in the shoe was found to be appropriate and he was given dressing supplies. The fissure healed in 5 days.

Case 4 is a 65-year-old male with type 2 diabetes mellitus (HbA1c = 7.6%), neuropathy, paresthesias, adrenal tumor, depression, hypertension, and glaucoma of the left eye due to glaucomatocyclitic crisis.

The patient received telephone outreach due to an asymmetry >3°C between both halluces. The right hallux had previously been warmer, then became cold (approximately ambient temperature) in the thermograms (Figure 5). The patient reported no redness, no swelling, no ulcers in the area of clinical concern upon outreach triggered by the mat. The patient reported he may have had a bandage on his toes, though he didn’t remember which while standing on the mat. He then reported a subungual hematoma of the right hallux two weeks prior likely due to trauma that was resolving uneventfully. He went on to heal uneventfully.

Figure 5.

Asymmetry between halluces of 3°C. The right hallux was initially warmer, then cooled to ambient temperature. Inflammation due to trauma.

Discussion

The economic and time cost of a 3- to 5-minute outreach phone call which triggers a 15-minute clinic visit for debridement, is inexpensive compared to a DFU, the aggregate costs of which exceeds $1.5 billion annually and continues to increase.^47-49 For high risk cohorts such as those who have recently healed from a wound, incidence has been consistently shown to be between 30% and 40% in the year following epithelialization.² Given the large treatment effect documented across three RCT in the 2000s, which averaged 70%,^38-40 the number needed to treat may be as low as four during this critical period of remission. Lifetime incidence of foot ulcers among patients with diabetes has been estimated at 25%,⁵⁰ which implies a lifetime number needed to treat of six. Thus, the economics of prevention, especially among high risk cohorts, is compelling: A recent meta-analysis reported that the average cost to a public payor in the year following a foot ulcer exceeds $44 000.⁵¹

Severity of ulcers determines the average per-episode cost, which ranges from $1900 for Wagner grade I⁵² to over $27 000 for Wagner grade IV or V with inpatient care accounting for greater than 70% of dollars spent.^53,54 Early intervention can shorten the DFU course and also decrease major resource utilization in emergency department visits and hospital admissions. Because as many as 50% of patients who heal from a DFU experience recurrence within 2 years, wound healing is impacted by both the timeliness of initial intervention and the severity of the wound.^37,55-58 The remote temperature monitoring mat alerted clinical staff to areas of concern that were triaged appropriately and treated quickly. The ulcers in cases 1-3 were of low severity and uninfected (UT1A) at initial presentation. None of the patients in these cases had a DFU-related hospital admission or emergency room visit in the time following their hotspots—59 weeks for case 1, 87 weeks for case 2, 87 weeks for case 3, and 74 weeks for case 3.

In case 1, the patient performed a visual exam to the best of his ability but failed to see an ulcer. He has hyperopia with presbyopia, glaucoma, and cataracts. Hyperglycemia causes transient refractive changes in patients with diabetes. After episodes of hyperglycemia are resolved, patients’ corneal typography trends toward hyperopia, for which this patient wears corrective lenses.¹² Patients with diabetes can perform adequately on Snellen eye exams, which test for differentiation between shape sizes, but perform poorly in low-contrast testing.⁵⁹ In a self visual exam where examining pedal skin color and appearance are paramount, this impacts the effectiveness the exam being performed. The patient’s systemic hypertension may have caused damage to the microvasculature of the retina likely explaining the etiology of his primary open-angle glaucoma.^28-29,60-61

In case 2, the patient has myopia with astigmatism as well as presbyopia, cataracts of both eyes, and nonproliferative retinopathy of the left eye. For patients who have retinopathy combined with myopia and presbyopia, focusing on objects like the foot can be a challenge. Myopia is an anatomic refractive error which causes incoming light to be focused anterior to the retina, while presbyopia is an age-related refractive error that causes light to be focused posterior to the retina.⁶² This variation in focus could explain why the patient in case 2 could not see the ulceration on his foot. There is evidence that myopic eyes may be less likely to have retinopathy due to morphology, but the addition of presbyopia exacerbates the visual impairment.⁶³

The patient in case 3 has myopia and presbyopia with proliferative retinopathy in both eyes. Worldwide, diabetic retinopathy affects one third of patients with diabetes.¹⁴ Data show that development of cataracts begins with impaired fasting glucose and progresses earlier and occurs 2-5 times more often in patients with diabetes.^30,32

The patient in case 4 has hypertension in conjunction with glaucomatocyclitic crises which are attacks of increased intraocular pressure thought to be due to mononuclear cell infiltration of trabecular interspaces.⁶⁴ The transient nature of this pathology may mean self-visual exams are impaired even when the patient experiences no symptoms.

Previous literature outlined using thermometry to prompt reduced ambulation for patients with asymmetry between contralateral locations on the feet exceeding 2.2°C over two consecutive days.^38-40 At the 2.2°C threshold, the RTM mat was shown to predict 97% of nonacute plantar DFUs with 37 days lead time and a specificity of 43%.³⁷ A previously unpublished analysis on the original dataset suggests that at the 1.75°C threshold, the RTM mat was able to predict 100% of nonacute plantar DFUs with 42 days lead time and specificity of 25%.⁶⁵ During the initial phase of RTM use, the decision was made to lower the facility threshold from 2.2°C to 1.75°C.⁴¹ In a noninterventional setting, this false positive rate may seem quite high, but the specificity in a research setting considered only inflammation with incident DFU as a true positive finding. In reality, pedal inflammation and diabetic foot complications is multifactorial and can stem from preulcerative lesions like callus that increase plantar pressures by up to 30% and result in inflammation that would have been reported as a false positive in the previous research on the mat.⁶⁶ Repetitive microtrauma can cause increased local pedal pressures, which leads to subcutaneous hemorrhage and ultimately tissue breakdown.^67-69 Debridement of these preulcerative lesions is a vital modality in prevention of DFU as it can lower peak plantar pressures more than reduced ambulation, accommodative footwear, and tendo-Achilles lengthening.^70,71 In patients with diabetes-related visual impairment and neuropathy, identification of hyperkeratotic or devitalized tissue is delayed, and as illustrated in the preceding cases, was recognized by the RTM prior to their regularly scheduled diabetic care clinic visits.⁷²

Loss of visual acuity can be a complication of pathologic changes to ocular anatomy secondary to increased systemic inflammation in diabetes. For example, macular edema is the deposition of proteinaceous fluid around the macula from leaky microvasculature, causing disruption to the central field of vision. The mechanism is proposed to be hyperglycemia-independent and instead be due to advanced glycation end products (AGE) that affect both the micro- and macrovascular systems.^73-79 Systemic inflammation could also account for bilateral pedal abnormalities that are not recognized by conventional asymmetry-based remote temperature monitoring approaches.

These cases highlight the promise of early detection in patients with diabetes-related visual impairment for improved outcomes for those at high risk for amputation and ulceration.

Limitations

The authors acknowledge this is a small case series limited by its size and lack of comparator. Although thermometry is recommended by several practice guidelines^68,80,81 and outcomes trials^38-40 the RTM mat is not yet widely available outside the VA system due to lack of insurance reimbursement. More research with a larger cohort is warranted to explore the benefit of once-daily remote temperature monitoring to augment daily self-exam in patients at-risk for DFUs.

Conclusion

Many patients with advanced diabetes mellitus suffer from visual impairment in the form of retinopathy, glaucoma, cataract, and macular edema as a progression of their disease and are therefore not able to adequately perform visual screening exams of their feet, which is a recommended part of preventive practice. When used as an adjunct to daily preventative diabetic self-care, remote temperature monitoring can be a technological solution for improved self-screening to prompt appropriate outreach and treatment, and potentially prevent ulceration for those at high risk of complication.

Footnotes

Acknowledgements

The Southern Arizona VA provided support and facilities.

Authors’ Note

Amanda L. Killeen is a third year resident and Kara M. Brock is a second year resident.

Abbreviations

ADA, American Diabetes Association; AGE, advanced glycation end products; DFU, diabetic foot ulcers; HbA1c, hemoglobin A1c; LEA, lower extremity amputations; RTM, remote temperature monitoring; UT, University of Texas; VHA, Veterans Health Administration.

Declaration of Conflicting Interests

The author(s) declared no potential conflicts of interest with respect to the research, authorship, and/or publication of this article.

Funding

The author(s) received no financial support for the research, authorship, and/or publication of this article.

ORCID iD

Amanda L. Killeen

References

Zhang

Jing

, et al. Global epidemiology of diabetic foot ulceration: a systematic review and meta analysis. Ann Med. 2017;49:196-116.

Armstrong

Boulton

Bus

Diabetic foot ulcers and their recurrence. N Engl J Med. 2017;376:2367-2375.

IDF Diabetes Atlas. 7th ed. Brussels, Belgium: International Diabetes Federation, 2015. Available at: http://www.diabetesatlas.org.

Walsh

Hoffstad

Sullivan

Margolis

DJ.

Association of diabetic foot ulcer and death in a population-based cohort from the United Kingdom. Diabet Med. 2016;33:1493-1498.

Brennan

Hess

Bartle

, et al. Diabetic foot ulcer severity predicts mortality among veterans with type 2 diabetes. J Diabetes Complications. 2017;31:556-561.

Franklin

Rajan

Tseng

, et al. Cost of lower-limb amputation in US veterans with diabetes using health services data in fiscal years 2004-2010. J Rehabil Res Dev. 2014;51:1325-1330.

Chin

Huang

Hsu

BR.

Impact of action cues, self-efficacy and perceived barriers on daily foot exam practice in type 2 diabetes mellitus patients with peripheral neuropathy. J Clin Nurs. 2013;22:61-68.

Schaper

Van Netten

Apelqvist

, et al. Prevention and management of foot problems in diabetes: a Summary Guidance for Daily Practice 2015, based on the IWGDF Guidance Documents. Diabetes Metab Res Rev. 2016;32(suppl 1):7-15.

Miller

Carter

Shih

Giovinco

Boulton

AJM

Armstrong

DG.

How to do a 3 minute diabetic foot exam. J Fam Pract. 2014;63;646-656.

10.

Pernat

Peršič

Usvyat

, et al. Implementation of routine foot check in patients with diabetes on hemodialysis: associations with outcomes. BMJ Open Diabetes Res Care. 2016;4:e000158.

11.

Yazdanpanah

Nasiri

Adarvishi

Literature review on the management of diabetic foot ulcer. World J Diabetes. 2015;6:37-53.

12.

Sonmez

Bozkurt

Atmaca

, et al. Effect of glycemic control on refractive changes in diabetic patients with hyperglycemia. Cornea. 2005;24:531-537.

13.

Klein

Lee

Klein

Refraction in adults with diabetes. Arch Ophthalmol. 2011;129:56-62.

14.

Ding

Wong

TY.

Current epidemiology of diabetic retinopathy and diabetic macular edema. Curr Diab Rep. 2012;12:346-354.

15.

Sinclair

Bayer

Girling

Woodhouse. Older adults, diabetes mellitus and visual acuity: a community-based case-control study. Age Ageing. 2000;29:335-339.

16.

Rand

Prud’homme

Fred

Ederer

, et al. Factors influencing the development of visual loss in advanced diabetic retinopathy. Invest Ophthalmol Vis Sci. 1985;26:983-991.

17.

American Diabetes Association. Microvascular complications and foot care. Sec. 9. In standards of medical care in diabetes 2016. Diabetes Care. 2016;39(suppl 1):S72-S80.

18.

Fong

Aiello

Gardner

, et al. Retinopathy in diabetes. Diabetes Care. 2004;27(suppl 1):S84-87.

19.

Lavery

Armstrong

Vela

, et al. Practical criteria for screening patients at high risk for diabetic foot ulceration. Arch Intern Med. 1998;158:157-162.

20.

Boyko

Ahroni

Forsberg

Davignon

Smith

DG.

A prospective study of risk factors for diabetic foot ulcer. The Seattle Diabetic Foot Study. Diabetes Care. 1999;22:1036-1042.

21.

Moss

Klein

BE.

The 14-year incidence of lower-extremity amputation in a diabetic population. The Wisconsin Epidemiologic Study of Diabetic Retinopathy. Diabetes Care. 1999;22:951-959.

22.

Hwang

Lee

Park

, et al. Association between diabetic foot ulcer and diabetic retinopathy. PLOS ONE. 2017;12.

23.

Crisologo

Lavery

LA.

Remote home monitoring to identify and prevent diabetic foot ulceration. Ann Transl Med. 2017;5:430.

24.

Pemayun

TGD

Naibaho

Novitasari

Amin

Minuljo

TTM

. Risk factors for lower extremity amputation in patients with diabetic foot ulcers: a hospital-based case-control study. Diabet Foot Ankle. 2015;6:29629.

25.

Quilici

MTV

de Sa Del Fiol

Vieire

AEF

Toledo

. Risk factors for foot amputation in patients hospitalized for diabetic foot infection. J Diab Res. 2016;8931508:8.

26.

Parisi

MCR

Neto

Menenzes

, et al. Baseline characteristics and risk factors for ulcer, amputation and severe neuropathy in diabetic foot at risk: the BRAZUPA study. Diabetol Metab Syndr. 2016;8:25.

27.

Sellman

Katzman, Andreasson

Londahl

Presence of chronic diabetic foot ulcers is associated with more advanced retinopathy. Diabet Med. 2018;35:1364-1370.

28.

Zhao

Chen

Diabetes and risk of glaucoma: systemic review and a meta-analysis of prospective cohort studies. Int J Ophthalmol. 2017;10:1430-1435.

29.

Bonovas

Peponis

Filioussi

Diabetes mellitus as a risk factor for primary open-angle glaucoma: a metanalysis. Diabet Med. 2004;21:609-614.

30.

Saxena

Mitchell

Rochtchina

Five-year incidence of cataract in older persons with diabetes and pre-diabetes. Ophthalmic Epidemiol. 2004;11:4, 271-277.

31.

Klein

BEK

Klein

Moss

. Incidence of cataract surgery in the Wisconsin epidemiologic study of diabetic retinopathy. Am J Ophthalmol. 1994;119:295-300.

32.

Javadi

Zarei-Ghanavati

Cataracts in diabetic patients: a review article. J Ophthalmic Vis Res. 2008;3:52-65.

33.

Bernth-Petersen

Bach

Epidemiologic aspects of cataract surgery. III: frequency of diabetes and glaucoma in a cataract population. Acta Ophthalmol (Copenh). 1983;61:406-416.

34.

Lang

GE.

Anti-VEGF treatment in diabetic macular edema. Ophthalmologica. 2012;227(suppl 1):21-29.

35.

Konstantinidis

Carron

de Ancos

, et al. Awareness and practices regarding eye diseases among patients with diabetes: a cross sectional analysis of the CoDiab-VD cohort. BMC Endocr Disord. 2017;17:56.

36.

Department of Veterans Affairs Office of the Inspector General. Healthcare inspection foot care for patients with diabetes and additional risk factors for amputation, 2013. Available at: https://www.va.gov/oig/pubs/VAOIG-11-00711-74.pdf.

37.

Frykberg

Gordon

Reyzelman

, et al. Feasibility and efficacy of a smart mat technology to predict development of diabetic plantar ulcers. Diabetes Care. 2017;40:973-980.

38.

Lavery

Higgins, Lanctot

, et al. Preventing diabetic foot ulcer recurrence in high-risk patients: use of temperature monitoring as a self-assessment tool. Diabetes Care. 2007;30:14-20.

39.

Lavery

Higgins

Lanctot

, et al. Home monitoring of foot skin temperatures to prevent ulceration. Diabetes Care. 2004;27:2642-2647.

40.

Armstrong

Holtz-Neiderer

Wendel

Mohler

Kimbriel

Laver

LA.

Skin temperature monitoring reduces the risk for diabetic foot ulceration in high-risk patients. Am J Med. 2007;120:1042-1046.

41.

Killeen

Walters

JL.

Remote temperature monitoring in diabetic foot ulcer detection. Wounds. 2018;30:E44-E48.

42.

Veterans Health Administration Office of Research and Development. Guidance on Case Reports. 2017. Available at: https://www.research.va.gov/resources/policies/guidance/Case-Report-Guidance.pdf.

43.

Armstrong

Lavery

Liswood

Todd

Tredwell

JA.

Infrared dermal thermometry for the high-risk diabetic foot. Phys Ther. 1997;77:169-175.

44.

Sibbald

Mufti

Armstrong

DG.

Infrared skin thermometry: an underutilized cost-effective tool for routine wound care practice and patient high-risk diabetic foot self-monitoring. Adv Skin Wound Care: J Prev Heal. 2015;28:37-44.

45.

Lavery

Armstrong

DG.

Temperature monitoring to assess, predict, and prevent diabetic foot complications. Curr Diab Rep. 2007;7:416-419.

46.

Lavery

Armstrong

Harkless

LB.

Classification of diabetic foot wounds. J Foot Ankle Surg. 1996;35:528-531.

47.

Hicks

Selvarajah

Mathioudakis

, et al. Trends and determinants of costs associated with the inpatient care of diabetic foot ulcers. J Vasc Surg. 2014;60:1247-1254.

48.

Rice

Desai

Cummings

Birnbaum

Skornicki

Parsons

NB.

Burden of diabetic foot ulcers for Medicare and private insurers. Diabetes Care. 2014;37:651-665.

49.

Armstrong

DG.

The big picture 2015: lower extremity complications of diabetes. Diabetic Foot J. 2015;18:114.

50.

Singh

Preventing foot ulcers in patients with diabetes. JAMA. 2005;293:217.

51.

Chan

Cadarette

Wodchis

Wong

Mittmann

Krahn

Cost-of-illness studies in chronic ulcers: a systematic review. J Wound Care. 2017;26(suppl 4):S4-S14.

52.

Wagner

FW.

The dysvascular foot: a system for diagnosis and treatment. Foot Ankle. 1981;2:64-122.

53.

Stockl

Vanderplas

Tafesse

Chang

Costs of lower-extremity ulcers among patients with diabetes. Diabetes Care. 2004;27:21.

54.

Harrington

Zagari

Corea

Klitenic

A cost analysis of diabetic lower-extremity ulcers. Diabetes Care. 2000;23:1333-1338.

55.

Margolis

Malay

Hoffstad

, et al. Incidence of diabetic foot ulcer and lower extremity amputation among Medicare beneficiaries, 2006 to 2008: Data Points #2. 2011 Feb 17. In: Data Points Publication Series. Rockville, MD: Agency for Healthcare Research and Quality; 2011.

56.

Smith-Strøm

Iversen

Igland

, et al. Severity and duration of diabetic foot ulcer (DFU) before seeking care as predictors of healing time: a retrospective cohort study. PLOS ONE. 2017;12:e0177176.

57.

Ndosi

Wright-Hughes

Brown

, et al. Prognosis of the infected diabetic foot ulcer: a 12-month prospective observational study. Diabet Med. 2018;35:78-88.

58.

Young

Jeffcoate

The National Diabetes Footcare Audit of England and Wales: an overview. Diabet Foot J. 2017;20:235-238.

59.

Regan

Neima

Low-contrast letter charts in early diabetic retinopathy, ocular hypertension, glaucoma, and Parkinson’s disease. Br J Ophthalmol. 1984;68:885-889.

60.

Wong

Mitchell

The eye in hypertension. Lancet. 2007;369:425-435.

61.

Gordon

Beiser

Brandt

JD.

The ocular hypertension treatment study: baseline factors that predict the onset of primary open-angle glaucoma. Arch Ophthalmol. 2002;120:714-720.

62.

National Eye Institute. Refractive Errors. Available at: https://nei.nih.gov/health/errors. Accessed November 29, 2018.

63.

Lim

Lamoureux

MeiSaw

Tay

Mitchell

YinWong

Are myopic eyes less likely to have diabetic retinopathy?

Ophthalmology. 2010;117:524-530.

64.

Harstad

Ringvold

Glaucomatocyclitic crises (Posner-Schlossman syndrome). A case report. Acta Ophthalmol (Copenh). 1986;64:146-151.

65.

Bloom

A remote thermometric system for the early detection of DFU. Poster presented at: Desert Foot Conference; Phoenix, AZ; 2017.

66.

Veves

Murray

Young

Boulton

AJ.

The risk of foot ulceration in diabetic patients with high foot pressure: a prospective study. Diabetologia. 1992;35:660-663.

67.

Bus

van Netten

Lavery

, et al; International Working Group on the Diabetic Foot. IWGDF guidance on the prevention of foot ulcers in at risk patients with diabetes. Diabetes Metab Res Rev. 2016;32(suppl 1):16-24.

68.

Frykberg

Zgonis

Armstrong

, et al; American College of Foot and Ankle Surgeons. Diabetic foot disorders. A clinical practice guideline (2006 revision). J Foot Ankle Surg. 2006;45(5 suppl):S1-S66.

69.

Orsted

Searles

Trowell

Shapera

Miller

Rahman

Best practice recommendations for the prevention, diagnosis, and treatment of diabetic foot ulcers: update 2006. Adv Skin Wound Care. 2007;20:655-669.

70.

Young

Cavanagh

Thomas

Johnson

Murray

Boulton

AJ.

The effect of callus removal on dynamic plantar foot pressures in diabetic patients. Diabet Med. 1992;9:55-57.

71.

Edmonds

ME.

Diabetic foot ulcers. BMJ. 2006;332:407-410

72.

Killeen

Neff

Petersen

, et al. Remote temperature monitoring to prompt timely preventative debridement: a case series of two patients. Poster presented at: American Podiatric Medical Association; Washington, DC; 2018.

73.

Porter

. What causes macular edema? American Academy of Ophthalmology. https://www.aao.org/eye-health/diseases/macular-edema-cause.

74.

Stolar

Glycemic control and complications in type 2 diabetes mellitus. Am J Med. 2010;123(suppl):3-11.

75.

Chilelli

Burlina

Lapolla

AGEs, rather than hyperglycemia, are responsible for microvascular complications in diabetes: a “glycoxidation-centric” point of view. Nutr Metab Cardiovasc Dis. 2013;23:913-919.

76.

Giacco

Brownlee

Schmidt

AM.

Oxidative stress and diabetic complications. Circ Res. 2010;107:1058-1070.

77.

Manigrasso

Juranek

Ramasamy

Schmidt

AM.

Unlocking the biology of RAGE in diabetic Microvascular complications. Trends Endocrinol Metab. 2014;25:15-22.

78.

Singh

Barden

Mori

Beilin

Advanced glycation end-products: A review. Diabetalogia. 2001;44:129-146.

79.

Ciulla

Amador

Zinman

Diabetic retinopathy and diabetic macular edema: pathophysiology, screening, and novel therapies. Diabetes Care. 2003;26:2653-2664.

80.

Bus

Netten

Lavery

, et al. IWGDF guidance on the prevention of foot ulcers in at-risk patients with diabetes. Diabetes Metab Res Rev. 2016;32(suppl 1):16-24.

81.

Lavery

Davis

Berriman

, et al. WHS guidelines update: diabetic foot ulcer treatment guidelines. Wound Repair Regen. 2016;24:112-126.