Delivery of the Bioactive Gas Hydrogen Sulfide During
Cold Preservation of Rat Liver: Effects on Hepatic Function
in an Ex vivo Model
Cecilia L. Balaban, Joaquín V. Rodriguez, and Edgardo E. Guibert
Centro Binacional (Argentina-Italia) de Investigaciones en Criobiología Clínica y Aplicada (CAIC), Universidad Nacional
de Rosario, Rosario, Santa Fe,Argentina
Abstract: The insults sustained by transplanted livers
(hepatectomy, hypothermic preservation, and normother-
mic reperfusion) could compromise hepatic function.
Hydrogen sulfide (H2S) is a physiologic gaseous signaling
molecule, like nitric oxide (NO) and carbon monoxide
(CO). We examined the effect of diallyl disulfide as a H2S
donor during hypothermic preservation and reperfusion
on intrahepatic resistance (IVR), lactate dehydrogenase
(LDH) release, bile production, oxygen consumption, bro-
mosulfophthalein (BSP) depuration and histology in an
isolated perfused rat liver model (IPRL), after 48 h of
hypothermic storage (4°C) in University of Wisconsin
solution (UW, Viaspan). Livers were retrieved from male
Wistar rats. Three experimental groups were analyzed:
Control group (CON): IPRL was performed after surgery;
UW: IPRL was performed in livers preserved (48 h—4°C)
in UW; and UWS: IPRL was performed in livers preserved
(48 h—4°C) in UW in the presence of 3.4 mM diallyl dis-
ulfide. Hypothermic preservation injuries were manifested
at reperfusion by a slight increment in IHR and LDH
release compared with the control group. Also, bile pro-
duction for the control group (1.32 mL/min/g of liver)
seemed to be diminished after preservation by 73% in
UW and 69% in UW H2S group at the end of
normothermic reperfusion. Liver samples analyzed by
hematoxylin/eosin clearly showed the deleterious effect
of cold storage process, partially reversed (dilated
sinusoids and vacuolization attenuation) by the addition
of a H2S delivery compound to the preservation
solution. Hepatic clearance (HC) of BSP was affected by
cold storage of livers, but there were no noticeable
differences between livers preserved with or without
diallyl disulfide. Meanwhile, livers preserved in the pres-
ence of H2S donor showed an enhanced capacity for BSP
uptake (kACON = 0.29 min
-1
;kAUW = 0.29 min
-1
;kAUWS
= 0.36 min
-1
). In summary, our animal model suggests that
hepatic hypothermic preservation for transplantation
affects liver function and hepatic depuration of BSP, and
implies that the inclusion of an H2S donor during hypoth-
ermic preservation could improve standard methods
of preparing livers for transplant. Key Words: Liver—
Organ preservation—Liver function tests—Drug kinetics.
Orthotropic liver transplantation is an effective
therapeutic modality for the treatment of end-stage
liver disease. A prerequisite of successful liver trans-
plantation is that the graft must function immedi-
ately, as no satisfactory method for long-term hepatic
support is available at present. This consideration
demands extra attention to preserve maximum
viability during the ischemia period between the
removal of the donor organ and reimplantation. Suc-
cessful liver preservation has been achieved clinically
up to 20 h (1). In experimental procedures, this time
has been extended up to 48 h (2). The insults sus-
tained by the transplanted livers (hepatectomy,
hypothermic preservation, and normothermic reper-
fusion) could compromise hepatic function. Simple
tests of active metabolism such as oxygen consump-
tion and bile production, among others, could be used
to assess liver function.
As hydrogen sulfide (H2S) was included in the
gasotransmitter classification as a powerful gaseous
signaling molecule along with carbon monoxide and
doi:10.1111/j.1525-1594.2011.01256.x
Received March 2011.
Address correspondence and reprint requests to Dr. Edgardo E.
Guibert, Centro Binacional de Criobiología—Universidad Nacio-
nal de Rosario,Avda.Arijón 28 bis, S2011BXN Rosario,Argentina.
E-mail: eguibert@fbioyf.unr.edu.ar
Presented in part at the 6th Latin American Congress of Artifi-
cial Organs and Biomaterials, held August 17–20, 2010 in
Gramado, Rio Grande do Sul, Brazil.
Artificial Organs
35(5):508–515, Wiley Periodicals, Inc.
© 2011, Copyright the Authors
Artificial Organs © 2011, International Center for Artificial Organs and Transplantation and Wiley Periodicals, Inc.
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