Original Article
Aldose Reductase Pathway Inhibition Improved Vascular
and C-Fiber Functions, Allowing for Pressure-Induced
Vasodilation Restoration During Severe Diabetic
Neuropathy
Claire Demiot,
1,2
Maylis Tartas,
1,3
Be ´ renge ` re Fromy,
1
Pierre Abraham,
1,3
Jean Louis Saumet,
1,3
and Dominique Sigaudo-Roussel
1
Pressure-induced vasodilation, a neurovascular mechanism
relying on the interaction between mechanosensitive C-
fibers and vessels, allows skin blood flow to increase in
response to locally nonnociceptive applied pressure that in
turn may protect against pressure ulcers. We expected that
severe neuropathy would dramatically affect pressure-in-
duced vasodilation in diabetic mice, and we aimed to
determine whether pressure-induced vasodilation alter-
ation could be reversed in 8-week diabetic mice. Control
and diabetic mice received no treatment or sorbinil, an
aldose reductase inhibitor, or alagebrium, an advanced
glycation end product breaker, the last 2 weeks of diabetes.
Laser Doppler flowmetry was used to evaluate pressure-
induced vasodilation and endothelium-dependent vasodila-
tion after iontophoretic delivery of acetylcholine (ACh).
We assessed the nervous function with measurements of
motor nerve conduction velocity (MNCV) as well as the
C-fiber–mediated nociception threshold. Pressure-induced
vasodilation, endothelial response, C-fiber threshold, and
MNCV were all altered in 8-week diabetic mice. None of the
treatments had a significant effect on MNCV. Although
sorbinil and alagebrium both restored ACh-dependent va-
sodilation, sorbinil was the sole treatment to restore the
C-fiber threshold as well as pressure-induced vasodilation
development. Therefore, the inhibition of aldose reductase
pathway by sorbinil improved vascular and C-fiber func-
tions that allow pressure-induced vasodilation restoration
that could limit neuropathic diabetic cutaneous pressure
ulcers. Diabetes 55:1478 –1483, 2006
D
uring long-term diabetes, progressive microan-
giopathy contributes to progressive loss of pe-
ripheral neurological function, leading to the
development of pressure-induced diabetic foot.
However, the exact pathway leading to ulceration has not
been fully identified, although it is recognized that ulcer-
ation may result from microcirculatory failure (1). Up to
now assessment of the circulation, the nervous control of
sensation, and foot sensitivity to loading are performed to
determine the risk of ulceration in the diabetic foot. In
contrast, local measurement of the microvascular function
is less routinely performed (2).
We reported a novel relationship between nerves and
vessels involving neural mechanosensitivity and cutane-
ous vasodilation, referred to as pressure-induced vasodi-
lation (3). The increase in cutaneous blood flow induced
by local pressure application delays the occurrence of
tissue ischemia, thus protecting the skin against pressure.
The mechanism of pressure-induced vasodilation involves
pressure sensing by specialized capsaicin sensory neurons
that act at the endothelial level to synthesize and release
endothelial factors, such as nitric oxide (NO) (3,4), that
induce smooth muscle relaxation. Therefore, neurovascu-
lar interaction is crucial for pressure-induced vasodilation
development.
More recently, we reported that pressure-induced vaso-
dilation was altered in 1-week diabetic mice with only
vascular dysfunction (5), which was correlated with dia-
betic patients without neuropathy (6). At the point of
clinical diabetes complication detection, significant im-
pairments in nerve function may have already appeared
and handicapped patients. Therefore, we expected that
long-term diabetes in animals with severe neuropathy will
dramatically aggravate pressure-induced vasodilation al-
teration. In this condition, skin blood flow should drop
down directly in response to local applied pressure, lead-
ing to early ischemia, which could favor diabetic foot
occurrence.
Diabetes through hyperglycemia is widely known to be
a major factor that leads to microvascular and nervous
complications (7). Indeed, hyperglycemia-induced end-
organ damage in diabetes is associated with increased flux
of glucose through 1) the polyol metabolic pathway (8 –10)
and 2) accumulation of advanced glycation end products
(AGEs) (11,12), both participating to increase oxidative
From the
1
Laboratory of Physiology, Unite ´ Mixte de Recherche (UMR)6214,
National Center for Scientific Research (CNRS), Institut National de la Sante ´
et de la Recherche Me ´ dicale (INSERM) U771, Medical School, University of
Angers, Angers, France; the
2
Faculty of Pharmaceutical Sciences, University
of Angers, Angers, France; and the
3
Centre Hospitalier Universitaire (CHU),
Laboratoire d’Explorations Vasculaires, Angers, France.
Address correspondence and reprint requests to Dominique Sigaudo-Rous-
sel, Laboratory of Physiology, CNRS, UMR6214, INSERM U771, Medical
School, University of Angers, Angers, F-49045 France. E-mail: domroussel@
yahoo.fr.
Received for publication 3 November 2005 and accepted in revised form 7
February 2006.
ACh, acetylcholine; AGE, advanced glycation end product; ARI, aldose
reductase inhibitor; MNCV, motor nerve conduction velocity; STZ, streptozo-
tocin.
DOI: 10.2337/db05-1433
© 2006 by the American Diabetes Association.
The costs of publication of this article were defrayed in part by the payment of page
charges. This article must therefore be hereby marked “advertisement” in accordance
with 18 U.S.C. Section 1734 solely to indicate this fact.
1478 DIABETES, VOL. 55, MAY 2006