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Erschienen in: Diabetologia 7/2016

28.04.2016 | Article

Prospective study on microangiopathy in type 2 diabetic foot ulcer

verfasst von: Fabio Fiordaliso, Giacomo Clerici, Serena Maggioni, Maurizio Caminiti, Cinzia Bisighini, Deborah Novelli, Daniela Minnella, Alessandro Corbelli, Riccardo Morisi, Alberto De Iaco, Ezio Faglia

Erschienen in: Diabetologia | Ausgabe 7/2016

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Abstract

Aims/hypothesis

We investigated the significance of microangiopathy in the development of foot ulcer, which is still disputed.

Methods

We assessed microangiopathy by histological analysis of the capillary ultrastructure using transmission electron microscopy and capillary density and arteriolar morphology in paraffin-embedded sections from the skin of type 2 diabetic patients: 30 neuroischaemic patients (Isc) revascularised with peripheral angioplasty and 30 neuropathic patients (Neu) with foot ulcer, compared with ten non-diabetic volunteers.

Results

In the diabetic patients, capillaries in the dermal papillary layer were fewer (−22.2%, 159 ± 43 vs 205 ± 52 mm2 in non-diabetic volunteers, p < 0.01). They also showed detrimental remodelling, with a 2.2-fold increase in capillary basement membrane thickness (3.44 ± 1.19 vs 1.53 ± 0.34 μm in non-diabetic volunteers, p < 0.001) and a 57.7% decrease in lumen area (14.6 ± 11.1 vs 34.7 ± 27.5 μm2, p < 0.001). No differences were observed between the diabetic Isc or Neu patients. Isc were more prone to develop arteriolar occlusion than Neu (16.8 ± 6.9% vs 6.7 ± 3.7%, respectively, p < 0.001). No patient had been amputated at 30 days and healing time was significantly longer in Isc (180 ± 120 vs 64 ± 50 days in Neu, p < 0.001).

Conclusions/interpretation

Capillary microangiopathy is present in equal measure in neuroischaemic and neuropathic diabetic foot skin. The predominance of arteriolar occlusions with neuroischaemia indicated the existence of an additional ‘small vessel disease’ that did not affect an effective revascularisation and did not worsen the prognosis of major amputations but slowed the healing process of the neuroischaemic foot ulcer.

Trial registration:

ClinicalTrials.gov NCT02610036.
Literatur
1.
Zurück zum Zitat UK Prospective Diabetes Study (UKPDS) Group (1998) Intensive blood-glucose control with sulphonylureas or insulin compared with conventional treatment and risk of complications in patients with type 2 diabetes (UKPDS 33). Lancet 352:837–853CrossRef UK Prospective Diabetes Study (UKPDS) Group (1998) Intensive blood-glucose control with sulphonylureas or insulin compared with conventional treatment and risk of complications in patients with type 2 diabetes (UKPDS 33). Lancet 352:837–853CrossRef
2.
Zurück zum Zitat The Diabetes Control and Complications Trial Research Group (1993) The effect of intensive diabetes treatment on the development and progression of long-term complications in insulin dependent diabetes mellitus: the Diabetes Control and Complications Trial. N Engl J Med 329:977–986CrossRef The Diabetes Control and Complications Trial Research Group (1993) The effect of intensive diabetes treatment on the development and progression of long-term complications in insulin dependent diabetes mellitus: the Diabetes Control and Complications Trial. N Engl J Med 329:977–986CrossRef
3.
Zurück zum Zitat Korzon-Burakowska A, Edmonds M (2006) Role of the microcirculation in diabetic foot ulceration. Int J Low Extrem Wounds 5:144–148CrossRefPubMed Korzon-Burakowska A, Edmonds M (2006) Role of the microcirculation in diabetic foot ulceration. Int J Low Extrem Wounds 5:144–148CrossRefPubMed
4.
Zurück zum Zitat Flynn MD, Tooke JE (1992) Aetiology of diabetic foot ulceration: a role for the microcirculation? Diabet Med 8:320–329CrossRef Flynn MD, Tooke JE (1992) Aetiology of diabetic foot ulceration: a role for the microcirculation? Diabet Med 8:320–329CrossRef
5.
Zurück zum Zitat Chao CY, Cheing GL (2009) Microvascular dysfunction in diabetic foot disease and ulceration. Diabetes Metab Res Rev 25:604–614CrossRefPubMed Chao CY, Cheing GL (2009) Microvascular dysfunction in diabetic foot disease and ulceration. Diabetes Metab Res Rev 25:604–614CrossRefPubMed
6.
Zurück zum Zitat Sharma S, Rayman G (2014) Microvascular disease. In: Hinchliffe RJ, Schaper NC, Thompson MM, Tripathi RK, Timaran CH (eds) The diabetic foot, 1st edn. JP Medical Publishers, London, pp 101–110 Sharma S, Rayman G (2014) Microvascular disease. In: Hinchliffe RJ, Schaper NC, Thompson MM, Tripathi RK, Timaran CH (eds) The diabetic foot, 1st edn. JP Medical Publishers, London, pp 101–110
7.
8.
Zurück zum Zitat Shami SK, Chittenden SJ (1991) Microangiopathy in diabetes mellitus: II. Features, complications and investigation. Diabetes Res 17:157–168PubMed Shami SK, Chittenden SJ (1991) Microangiopathy in diabetes mellitus: II. Features, complications and investigation. Diabetes Res 17:157–168PubMed
9.
Zurück zum Zitat Yusof MI, Al-Astani AD, Jaafar H, Rashid FA (2008) Morphometric analysis of skin microvasculature in the diabetic foot. Singap Med 49:100–104 Yusof MI, Al-Astani AD, Jaafar H, Rashid FA (2008) Morphometric analysis of skin microvasculature in the diabetic foot. Singap Med 49:100–104
10.
Zurück zum Zitat (2000) World Medical Association Declaration of Helsinki: ethical principles for medical research involving human subjects. JAMA 284:3043–3045 (2000) World Medical Association Declaration of Helsinki: ethical principles for medical research involving human subjects. JAMA 284:3043–3045
11.
Zurück zum Zitat Norgren L, Hiatt WR, Dormandy JA, Nehler MR, Harris KA, Fowkes FGR on behalf of the TASC II Working Group (2007) Inter-society consensus for the management of peripheral arterial disease (TASC II). Eur J Vasc Endovasc Surg 33(Suppl):S73–S108 Norgren L, Hiatt WR, Dormandy JA, Nehler MR, Harris KA, Fowkes FGR on behalf of the TASC II Working Group (2007) Inter-society consensus for the management of peripheral arterial disease (TASC II). Eur J Vasc Endovasc Surg 33(Suppl):S73–S108
12.
Zurück zum Zitat Faglia E, Clerici G, Caminiti M, Quarantiello A, Curci V, Somalvico F (2010) Evaluation of feasibility of ankle pressure and foot oximetry values for the detection of critical limb ischemia in diabetic patients. Vasc EndovascSurg 44:184–189CrossRef Faglia E, Clerici G, Caminiti M, Quarantiello A, Curci V, Somalvico F (2010) Evaluation of feasibility of ankle pressure and foot oximetry values for the detection of critical limb ischemia in diabetic patients. Vasc EndovascSurg 44:184–189CrossRef
13.
Zurück zum Zitat Lavery LA, Armstrong DG, Murdoch DP, Peters EJ, Lipsky BA (2007) Validation of the Infectious Diseases Society of America’s diabetic foot infection classification system. Clin Infect Dis 44:562–565CrossRefPubMed Lavery LA, Armstrong DG, Murdoch DP, Peters EJ, Lipsky BA (2007) Validation of the Infectious Diseases Society of America’s diabetic foot infection classification system. Clin Infect Dis 44:562–565CrossRefPubMed
14.
Zurück zum Zitat Faglia E, Favales F, Morabito A (2001) New ulceration, new major amputation and patient survival in diabetic subjects hospitalized for foot ulcer: 6.5 years follow-up. Diabetes Care 24:78–83CrossRefPubMed Faglia E, Favales F, Morabito A (2001) New ulceration, new major amputation and patient survival in diabetic subjects hospitalized for foot ulcer: 6.5 years follow-up. Diabetes Care 24:78–83CrossRefPubMed
15.
Zurück zum Zitat Armstrong DG, Cohen K, Courric S, Bharara M, Marston W (2011) Diabetic foot ulcers and vascular insufficiency: our population has changed, but our methods have not. J Diabetes Sci Technol 1:1591–1595CrossRef Armstrong DG, Cohen K, Courric S, Bharara M, Marston W (2011) Diabetic foot ulcers and vascular insufficiency: our population has changed, but our methods have not. J Diabetes Sci Technol 1:1591–1595CrossRef
16.
Zurück zum Zitat Gershater MA, Löndahl M, Nyberg P et al (2009) Complexity of factors related to outcome of neuropathic and neuroischaemic/ischaemic diabetic foot ulcers: a cohort study. Diabetologia 52:398–407CrossRefPubMed Gershater MA, Löndahl M, Nyberg P et al (2009) Complexity of factors related to outcome of neuropathic and neuroischaemic/ischaemic diabetic foot ulcers: a cohort study. Diabetologia 52:398–407CrossRefPubMed
17.
Zurück zum Zitat Ndip A, Jude EB (2009) Emerging evidence for neuroischemic diabetic foot ulcers: model of care and how to adapt practice. Int J Low Extrem Wounds 8:82–94CrossRefPubMed Ndip A, Jude EB (2009) Emerging evidence for neuroischemic diabetic foot ulcers: model of care and how to adapt practice. Int J Low Extrem Wounds 8:82–94CrossRefPubMed
18.
Zurück zum Zitat Flynn MD, Edmonds ME, Tooke JE, Watkins PJ (1988) Direct measurement of capillary blood flow in the diabetic neuropathic foot. Diabetologia 3:652–656CrossRef Flynn MD, Edmonds ME, Tooke JE, Watkins PJ (1988) Direct measurement of capillary blood flow in the diabetic neuropathic foot. Diabetologia 3:652–656CrossRef
19.
Zurück zum Zitat Netten PM, Wollersheim H, Thien T, Lutterman JA (1996) Skin microcirculation of the foot in diabetic neuropathy. Clin Sci (Lond) 91:559–565CrossRef Netten PM, Wollersheim H, Thien T, Lutterman JA (1996) Skin microcirculation of the foot in diabetic neuropathy. Clin Sci (Lond) 91:559–565CrossRef
20.
Zurück zum Zitat Jörneskog G, Brismar K, Fagrell B (1995) Skin capillary circulation is more impaired in the toes of diabetic than non-diabetic patients with peripheral vascular disease. Diabet Med 12:36–41CrossRefPubMed Jörneskog G, Brismar K, Fagrell B (1995) Skin capillary circulation is more impaired in the toes of diabetic than non-diabetic patients with peripheral vascular disease. Diabet Med 12:36–41CrossRefPubMed
21.
Zurück zum Zitat Quigley FG, Faris IB, Duncan HJ (1991) A comparison of Doppler ankle pressures and skin perfusion pressure in subjects with and without diabetes. Clin Physiol 11:21–25CrossRefPubMed Quigley FG, Faris IB, Duncan HJ (1991) A comparison of Doppler ankle pressures and skin perfusion pressure in subjects with and without diabetes. Clin Physiol 11:21–25CrossRefPubMed
22.
Zurück zum Zitat Williams DT, Price P, Harding KG (2006) The influence of diabetes mellitus and lower limb arterial disease on cutaneous foot perfusion. J Vasc Surg 44:770–775CrossRefPubMed Williams DT, Price P, Harding KG (2006) The influence of diabetes mellitus and lower limb arterial disease on cutaneous foot perfusion. J Vasc Surg 44:770–775CrossRefPubMed
23.
Zurück zum Zitat Jörneskog G, Brismar K, Fagrell B (1995) Skin capillary circulation severely impaired in toes of patients with IDDM, with and without late diabetic complications. Diabetologia 38:474–480CrossRefPubMed Jörneskog G, Brismar K, Fagrell B (1995) Skin capillary circulation severely impaired in toes of patients with IDDM, with and without late diabetic complications. Diabetologia 38:474–480CrossRefPubMed
24.
Zurück zum Zitat LoGerfo FW, Coffman JD (1984) Current concepts. Vascular and microvascular disease of the foot in diabetes. Implications for foot care. N Engl J Med 311:1615–1619CrossRefPubMed LoGerfo FW, Coffman JD (1984) Current concepts. Vascular and microvascular disease of the foot in diabetes. Implications for foot care. N Engl J Med 311:1615–1619CrossRefPubMed
25.
Zurück zum Zitat Goldenberg S, Alex M, Joshi RA, Blumenthal HT (1959) Nonatheromatous peripheral vascular disease of the lower extremity in diabetes mellitus. Diabetes 8:261–273CrossRefPubMed Goldenberg S, Alex M, Joshi RA, Blumenthal HT (1959) Nonatheromatous peripheral vascular disease of the lower extremity in diabetes mellitus. Diabetes 8:261–273CrossRefPubMed
26.
Zurück zum Zitat Strandness DE Jr, Priest RE, Gibbons GE (1964) Combined clinical and pathologic study of diabetic and nondiabetic peripheral arterial disease. Diabetes 13:366–372CrossRefPubMed Strandness DE Jr, Priest RE, Gibbons GE (1964) Combined clinical and pathologic study of diabetic and nondiabetic peripheral arterial disease. Diabetes 13:366–372CrossRefPubMed
27.
Zurück zum Zitat Ross R (1981) Atherosclerosis: a problem of the biology of arterial wall cells and their interactions with blood components. Arteriosclerosis 1:293–331CrossRefPubMed Ross R (1981) Atherosclerosis: a problem of the biology of arterial wall cells and their interactions with blood components. Arteriosclerosis 1:293–331CrossRefPubMed
28.
Zurück zum Zitat Faglia E, Clerici G, Clerissi J et al (2007) When is a technically successful peripheral angioplasty effective in preventing above-the-ankle amputation in diabetic patients with critical limb ischaemia? Diabet Med 24:823–829CrossRefPubMed Faglia E, Clerici G, Clerissi J et al (2007) When is a technically successful peripheral angioplasty effective in preventing above-the-ankle amputation in diabetic patients with critical limb ischaemia? Diabet Med 24:823–829CrossRefPubMed
29.
Zurück zum Zitat Bakker K, Apelqvist J, Schaper NC (2012) International Working Group on Diabetic Foot Editorial Board. Practical guidelines on the management and prevention of the diabetic foot 2011. Diabetes Metab Res Rev 28(Suppl 1):225–231CrossRefPubMed Bakker K, Apelqvist J, Schaper NC (2012) International Working Group on Diabetic Foot Editorial Board. Practical guidelines on the management and prevention of the diabetic foot 2011. Diabetes Metab Res Rev 28(Suppl 1):225–231CrossRefPubMed
30.
Zurück zum Zitat Margolis DJ, Kantor J, Berlin JA (1999) Healing of diabetic neuropathic foot ulcers receiving standard treatment. A meta-analysis. Diabetes Care 22:692–695CrossRefPubMed Margolis DJ, Kantor J, Berlin JA (1999) Healing of diabetic neuropathic foot ulcers receiving standard treatment. A meta-analysis. Diabetes Care 22:692–695CrossRefPubMed
31.
Zurück zum Zitat Hartemann-Heurtier A, Van Ha G, Danan JP et al (2002) Outcome of severe diabetic foot ulcers after standardised management in a specialised unit. Diabetes Metab 28:477–484PubMed Hartemann-Heurtier A, Van Ha G, Danan JP et al (2002) Outcome of severe diabetic foot ulcers after standardised management in a specialised unit. Diabetes Metab 28:477–484PubMed
32.
Zurück zum Zitat Zimny S, Schatz H, Pfohl M (2002) Determinants and estimation of healing times in diabetic foot ulcers. J Diabet Complications 16:327–332CrossRef Zimny S, Schatz H, Pfohl M (2002) Determinants and estimation of healing times in diabetic foot ulcers. J Diabet Complications 16:327–332CrossRef
33.
Zurück zum Zitat Arora S, Pomposelli F, LoGerfo FW, Veves A (2002) Cutaneous microcirculation in the neuropathic diabetic foot improves significantly but not completely after successful lower extremity revascularization. J Vasc Surg 35:501–505CrossRefPubMed Arora S, Pomposelli F, LoGerfo FW, Veves A (2002) Cutaneous microcirculation in the neuropathic diabetic foot improves significantly but not completely after successful lower extremity revascularization. J Vasc Surg 35:501–505CrossRefPubMed
34.
Zurück zum Zitat Söderström M, Arvela E, Albäck A, Aho PS, Lepäntalo M (2008) Healing of ischaemic tissue lesions after infrainguinal bypass surgery for critical leg ischaemia. Eur J Vasc Endovasc Surg 36:90–95CrossRefPubMed Söderström M, Arvela E, Albäck A, Aho PS, Lepäntalo M (2008) Healing of ischaemic tissue lesions after infrainguinal bypass surgery for critical leg ischaemia. Eur J Vasc Endovasc Surg 36:90–95CrossRefPubMed
35.
Zurück zum Zitat Hehrlein C, Chuang CH, Tuntelder JR, Tatsis GP, Littmann L, Svenson RH (1991) Effects of vascular runoff on myointimal hyperplasia after mechanical balloon or thermal laser arterial injury in dogs. Circulation 84:884–890CrossRefPubMed Hehrlein C, Chuang CH, Tuntelder JR, Tatsis GP, Littmann L, Svenson RH (1991) Effects of vascular runoff on myointimal hyperplasia after mechanical balloon or thermal laser arterial injury in dogs. Circulation 84:884–890CrossRefPubMed
Metadaten
Titel
Prospective study on microangiopathy in type 2 diabetic foot ulcer
verfasst von
Fabio Fiordaliso
Giacomo Clerici
Serena Maggioni
Maurizio Caminiti
Cinzia Bisighini
Deborah Novelli
Daniela Minnella
Alessandro Corbelli
Riccardo Morisi
Alberto De Iaco
Ezio Faglia
Publikationsdatum
28.04.2016
Verlag
Springer Berlin Heidelberg
Erschienen in
Diabetologia / Ausgabe 7/2016
Print ISSN: 0012-186X
Elektronische ISSN: 1432-0428
DOI
https://doi.org/10.1007/s00125-016-3961-0

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