Jvasc-02-1-b

J Vasc Br 2002, Vol. 1, Nº1 39
Iliac artery lesions as experimental models of
vascular trauma inducing intraperitoneal
and retroperitonial hemorrhage
Luiz Francisco Poli de Figueiredo,1 Ruy Jorge Cruz Jr.,2 Victor Bruscagin,3
Samir Rasslan,3 Maurício Rocha e Silva2
SummaryObjective: The initial treatment of uncontrolled hemorrhage is controversial. Therefore, the
objective of this study was to develop an experimental model of retroperitoneal hemorrhage, induced by aniliac artery puncture through the femoral artery, to evaluate its hemodynamic and metabolic consequences andto correlate them with the blood loss volume, measured by radioisotopes.
Method: We designed two experimental models of uncontrolled hemorrhage induced by an intraperitoneal
and a retroperitoneal iliac artery lesions in dogs (17.1±0.56 kg). In the first set of experiments, a suture wasplaced through the common iliac artery to produce a 3 mm tear, when the external suture lines were pulledafter incision closure, to induce an intraperitoneal hemorrhage. After 20 minutes, the animals were randomizedto controls (CT, n=6, no fluids) or to lactated Ringer’s (LR, 32 mL/kg in 15 min, n=6). Intraabdominal bloodloss volume was directly measured 40 minutes after the iliac artery tear. In another set of experiments, dogswere randomized to unilateral (UL, n=11) or bilateral (BL, n=11) iliac artery puncture, using a metallic deviceintroduced through the femoral arteries and followed for 120 minutes. Initial and final blood volumes weredetermined using radioactive tracers, 99mTC and 51Cr, respectively.
Results: In the first set of experiments, all animals presented acute fall in arterial pressure and cardiac
output. CT animals remained with severe hypotension and low flows, while LR showed transient improvementsin arterial pressure and cardiac output, without promoting significant increases in blood loss volume (CT47.8±5.9 vs. RL 49.4±0.7, in mL/kg). In the second set of experiments, UL was associated with a stable arterialpressure and a moderate decrease in cardiac output and oxygen delivery. BL induced an abrupt and sustaineddecrease in mean arterial pressure and a much greater reduction in cardiac output, oxygen delivery andconsumption. Retroperitoneal blood loss after BL was 36.8±3.2 ml/kg, while after UL was 25.1±3.4 ml/kg(P=0.0262).
Conclusion: Bilateral iliac artery puncture produces hypotension and low flow state, while a unilateral iliac
artery lesion causes a compensated shock state. Both the anterior iliac tear or posterior iliac puncture showed tobe clinically relevant models of vascular trauma, inducing uncontrolled intraperitoneal and retroperitonealhemorrhages, respectively.
Key words: resuscitation; iliac artery; hemorrhage; shock. / Palavras-chave: ressuscitação, artéria ilíaca,
Clinically relevant models of vascular trauma are Supported by Fundação de Amparo à Pesquisa do Estado de São Paulo,São Paulo, Brazil (bolsa FAPESP – 98/15658-0).
needed for studies addressing controversies on trauma 1. Applied Physiology Service, Instituto do Coração/Faculdade de Medici- research and new surgical strategies. Currently, one of na da USP (InCor/FMUSP). Dept. of Surgery, Universidade Federal deSão Paulo/Escola Paulista de Medicina (UNIFESP/EPM).
the greatest controversies is the prehospital and 2. Applied Physiology Service, InCor/FMUSP.
emergency room approach of hypotensive trauma 3. Emergency Service, Dept. of Surgery, Faculdade de Ciências Médicas victims sustaining injuries which could result inuncontrolled hemorrhage. Volume resuscitation has been the mainstay treatment of these patients.1 However, Copyright 2002 by Sociedade Brasileira de Angiologia e Cirurgia Vascular.
40 J Vasc Br 2002, Vol. 1, Nº1
Experimental models of vascular trauma – Poli de Figueiredo et alii this approach has been challenged by several authors, Animal preparation
based on experimental studies2-4 that suggest that fluid These studies were performed using 48 male mongrel infusion, prior to bleeding control, may result in dogs, weighing 17±1.5 kg. Dogs were fasted for 12 increased blood loss. Additionally, a controversial clinical hours before the study, with free access to water.
study suggested that delayed fluid resuscitation is Anesthesia was induced with an intravenous injection associated with better outcome for hypotensive victims of sodium pentobarbital, 25 mg/kg. After endotracheal with penetrating torso.5 These studies hypothesized intubation, the animals were allowed to breathe that fluid infusion, before hemorrhage control, would spontaneously, with no supplemental oxygen, enhance bleeding through several mechanisms, such as throughout the experiment. Additional doses of increased blood pressure, which would dislodge blood pentobarbital, 2 mg/kg, were used whenever required.
clots, and the dilution of clotting factors. The highest The right common femoral artery was dissected bleeding risk was considered for patients sustaining and cannulated with a polyethylene cannula to measure penetrating abdominal vascular trauma. To address the mean arterial pressure at the abdominal aorta and to controversy on whether fluid infusion increases bleeding, collect arterial blood samples for blood gas, pH, we directly measured intra-abdominal blood loss in bicarbonate, base excess, hemoglobin and plasma sodium animals with uncontrolled hemorrhage after an iliac analysis. The right common femoral vein was cannulated in a similar fashion for fluid infusion. A 7Fr flow- Uncontrolled retroperitoneal hemorrhage, as directed pulmonary artery catheter (93A-131H-7F, induced by pelvic fractures, may result in hypovolemic Edwards Swan-Ganz, Baxter Edwards Critical Care, shock and fluid resuscitation is the cornerstone Irvine, CA) was introduced through the right external therapeutic approach, associated with external fixation, jugular vein and its tip placed in the pulmonary artery, in selected cases.7-10 Whether fluid resuscitation guided by pressure and wave tracings. This catheter was increases retroperitoneal uncontrolled hemorrhage is used to sample mixed venous blood for blood gas not known. Clinically relevant models of retroperitoneal analysis and to measure pulmonary arterial pressure and hematoma are not sufficiently available. The only cardiac output (Edwards COM-2 Cardiac Output experimental model of retroperitoneal hemorrhage that Computer, Baxter Edwards Critical Care, Irvine, CA).
we are aware of was described by Baylis in 1962, Cardiac output was measured intermittently by the produced by an injection of venous blood, collected thermodilution technique in triplicate, with 3-mL bolus through the femoral vein, into the retroperitoneal injections of isotonic saline at 20o C every 10 minutes.
space.11 We developed an experimental model of All pressure measuring catheters were connected to retroperitoneal hemorrhage, induced by an iliac artery pressure transducers and then to a Biopac Data puncture through the femoral artery, to evaluate its Acquisition System (Model MP100, Biopac Systems, hemodynamic and metabolic consequences and to Goleta, CA) or to a galvanometric recorder (model correlate them with the blood loss volume, measured by 7700 Hewlett-Packard, San Diego, CA) for continuous recording of heart rate, systemic arterial and pulmonary We present both experimental models of iliac artery artery pressures and waveforms. Arterial and venous trauma which could be suitable for several studies blood samples were analyzed by a Stat Profile Ultra including fluid resuscitation, coagulation, shock and Analyzer (Nova Biomedical, Waltham, MA).
new surgical approaches such as endovascular andvideolaparoscopic surgeries.
Iliac artery tear for intraabdominal hemorrhage (n =
20)
Material and methods
A six-centimeter, pararectal longitudinal incision The experimental protocols were approved by the was then performed at the left lower quadrant. After Institutional Review Board of the Heart Institute celiotomy, bowel loops were displaced medially. The (InCor), University of São Paulo, in compliance with left common iliac artery was identified and dissected for the Principles of Laboratory Animal Care formulated about 1 centimeter. A 3-0 polypropylene suture was by the National Society for Medical Research and the passed through the anterior portion of the artery, exit Guide for the Care and Use of Animals by the National points 3 mm apart, in order to produce a 3 mm arterial tear at the appropriate experimental moment. The Experimental models of vascular trauma – Poli de Figueiredo et alii J Vasc Br 2002, Vol. 1, Nº1 41
extremities of the suture lines were exteriorized through hemorrhage, which was associated, in pilot studies, the incision, which was closed by planes for airtightness with massive blood loss and rapid death in four dogs.
Thirty minutes after completion of surgical After the surgical preparation, animals were placed preparation, baseline measurements were obtained (0 on their left side and allowed to stabilize. Baseline min). With both femoral arteries catheterized with our measurements were obtained and an uncontrolled, device, the animals were then randomized for unilateral intraabdominal hemorrhage was induced by pulling lesion (UL, n=11) at the right iliac artery or bilateral out both extremities of the external suture lines. The lesions (BL, n=11) at the right and left iliac arteries.
animals were allowed to bleed for 20 minutes, after After 120 minutes from induction of hemorrhage, the which survivors were randomly assigned to the following animals were euthanized by an anesthesia overdose and experimental groups: control group (CT, n=6) received saturated KCl infusion. A celiotomy was then performed no fluid; or lactated Ringer’s group (LR, n=6), 32 to observe the presence and the extension of the mL/kg injected over a 15-minute period. Forty minutes retroperitoneal hematoma, and the presence or absence after the induction of uncontrolled hemorrhage, the of blood within the peritoneal cavity.
animals were euthanized by an anesthetic overdose Heart rate and both mean systemic and pulmonary followed by a saturated KCl injection. A xiphopubic arterial pressures were monitored continuously median laparotomy was rapidly performed, the left iliac throughout the experiment. Cardiac output was artery was clamped, and all intraabdominal blood loss measured at 10-minute intervals. Arterial and venous was directly measured by weighing all clots and free hematocrit, hemoglobin, base deficit, oxygen saturation blood. The iliac artery was then resected, opened and oxygen tension were measured at 0, 10, 60 and 120 longitudinally, and the size of the iliac artery tear was minutes. Oxygen delivery, oxygen consumption and cardiac index were calculated using standard formulae.
Heart rate, mean systemic and pulmonary arterial Red blood cell and blood volumes were determined pressures were continuously recorded. Intermittent by isotope dilution technique of two radioactive tracers, cardiac output (CO) was measured at 5-minute intervals technetium (99mTC) and chromium (51Cr), according and expressed as cardiac index [CO / body surface area to the Kowalsky and Perry guidelines.13 A volume of 3 (BSA= 0.112*weight2/3)]. Hemodynamic data were mL of blood was collected through the left jugular vein analyzed at baseline, and every five-minute interval and labeled with technetium (99mTc - TCK-11, CIS thereafter. Mixed venous oxygen saturation (SvO2) and Bio International, France), which has a half-life of 6 arterial base excess, oxygen tension, oxygen saturation, hours. The concentration of radioactive red blood cells bicarbonate and hemoglobin levels were measured at 0, (TLi = injected total load, in counts/min/mL) was 20, 30 and 40 minutes. Oxygen delivery was calculated determined using a well-type scintillation counter (Phillips Medical System Division XL1100, Eindhoven,Nederlands). These marked red cells were returnedthrough the left jugular vein and a 15-minute interval Iliac artery puncture for retroperitoneal hemorrhage
was observed to allow a homogeneous distribution of (n=22)
the radiotracer. Another 7 mL blood sample was collected Both common femoral arteries were dissected and through the pulmonary artery catheter and the prepared to be cannulated to induce the uncontrolled concentration of the radiotracer (TLc = collected total retroperitoneal hemorrhage at the appropriate moment.
load, in counts/min/mL) was determined. Baseline red To produce reproducible unilateral or bilateral iliac cell blood volume (RCVb, in mL/kg) was estimated by arterial lesions, we adapted a standard radio antenna, the dilution technique of marked red cells, through the which is a stainless steel hollow tube and a solid, blunt- following formula: [RCVb = TLi / TLc]. Fifteen minutes ended stainless steel shaft, and introduced it through before the end of the experiment, the final red blood cell both common femoral arteries. Uncontrolled volume (RCVf) was determined, using a similar retroperitoneal hemorrhage was produced by driving technique as described above; however, chromium (51Cr, the shaft forward and immediately retracting it back, Instituto de Pesquisas de Energia Nuclear-IPEN/ inducing a 2 mm lesion in the posterior aspect of the CNEN, São Paulo, Brazil) was used to label the red iliac artery, thereby avoiding an intraperitoneal cells. Baseline and final blood volumes (BVb and BVf, 42 J Vasc Br 2002, Vol. 1, Nº1
Experimental models of vascular trauma – Poli de Figueiredo et alii respectively) were estimated through the respective redcell volume and the corrected hematocrit: [BVb,f =RCVb,f / 0.96 x Ht]. The volume of red cells in thehematoma (RCVh) was estimated as the differencebetween baseline and final red cell volume (RCVh =RCVb –RCVf), while the blood volume (BVh) in thehematoma was calculated from RCVh and the initialhematocrit: [BVh = RCVh / 0.96 x Ht].
Results
Iliac artery tear for intraabdominal hemorrhage (n =
20)
At baseline all animals were stable (Figure 1, Table 1). The size of the arterial tear was very similar betweengroups (in mm, CT 2.4±0.4; LR 2.3±0.2). Totalintraabdominal blood loss, measured at the end of theexperiments, was not significantly different betweenCT (47.8±5.9 mL/kg) and LR (49.4±0.7 mL/kg).
metabolic profile of severe hemorrhagic shock.
Significant and abrupt drops in mean arterial pressure,cardiac output, O2 delivery, SvO2, base excess and bicarbonate levels were observed (Figure 1, Table 1).
Eight dogs died before randomization, and were thereby Figure 1 - Mean arterial pressure (in mmHg) and cardiac
excluded. Animals from the CT group remained in index (in L/min/m2, mean ± SEM) during 40 severe shock throughout the experiment. The LR group min of uncontrolled intraabdominal hemor- showed a gradual elevation in mean arterial pressure rhage from an iliac artery tear for groups CT (no which, at 40 minutes, was not different from baseline fluids, n=6), and LR (32 mL/kg in 15 min, n=6) Oxygen delivery, mixed venous oxygen saturation, hemoglobin and arterial pH, bicarbonate and baseexcess levels (mean ± SEM) during 40 min of uncontrolled intraabdominal hemorrhage from an iliacartery tear for groups CT (no fluids, n=6) and LR (32 mL/kg in 15 min, n=6) 20-minute
30-minute
40-minute
O2 delivery (mLO2/min)
SVO2 %
Hemoglobin (g/dL)
Base excess (mMol/L)
Bicarbonate (mEq/L)
Experimental models of vascular trauma – Poli de Figueiredo et alii J Vasc Br 2002, Vol. 1, Nº1 43
values. However, in this group, two deaths occurredduring the experimental period, at 34 and 38 min.
Therefore, values presented for 35 and 40 minutes inthe LR group represent sample sizes of five and fouranimals, respectively. LR infusion restored cardiacoutput to baseline values (Figure 1) and was associatedwith partial restoration in O2 delivery, SvO2. There were no significant improvements in pH, base excessand bicarbonate levels after LR. Hemorrhage did notcause significant variations in hemoglobin levels in theCT group during the experiment. In contrast, therewere significant decreases following LR treatment.
Iliac artery puncture for retroperitoneal hemorrhage
(n=22)
Baseline measurements showed no significant differences between groups regarding measuredhemodynamic and metabolic parameters. Mean arterialpressure remained stable following unilateral iliac arterylesion throughout the experiment. In contrast, bilateral Figure 2 -
Mean arterial pressures (in mmHg) and cardiac lesions induced an abrupt and sustained decrease in index (in L/min/m2, mean ± SEM), during 120 mean arterial pressure, from 131.9±5.9 mmHg to min of uncontrolled retroperitoneal hemorrhagefrom an iliac artery tear for UL (unilateral iliac 88.6±10.8 mmHg. Mean arterial pressure remained artery lesion, n=11) and BL (bilateral iliac artery significantly lower than that in the unilateral iliac lesion group throughout the experiment (Figure 2). Cardiacoutput and oxygen delivery presented rapid, sustainedand significant decreases after both unilateral or bilateraliliac artery lesion. However, the bilateral iliac arterylesion was associated with a much greater reduction inboth cardiac output and oxygen delivery than the Discussion
unilateral lesion throughout the experiment (Figure 2, We presented two distinct models of iliac artery Table 2). Oxygen consumption was preserved following lesions inducing predictable hemodynamic responses the unilateral lesion until the last experimental moment, and blood loss volumes, which may be useful to develop 120 minutes, when it became lower than baseline values studies in several areas of physiology and treatment of and similar to the bilateral lesion group. The bilateral vascular trauma and uncontrolled hemorrhage. A major iliac lesion induced an abrupt and sustained decrease in controversy regarding prehospital treatment of oxygen consumption throughout the experiment, which posttraumatic hypotension in victims concerns fluid was significantly lower than in the unilateral lesion resuscitation.2-5 Both models adequately simulated the group, except for the last experimental moment (Table clinical behavior of a penetrating abdominal injury 2). Arterial base excess levels showed a progressive with an intraabdominal hemorrhage and an exclusive decrease in both groups. Hemoglobin levels remained retroperitoneal hemorrhage, such as observed in complex stable after unilateral iliac lesion while bilateral lesions pelvic fractures. In our model of uncontrolled caused a significant decrease in hemoglobin levels intraabdominal hemorrhage, induced by an iliac arterial throughout the study (Table 2). Total blood loss into tear, we provide experimental evidence supporting an the retroperitoneal space was greater after bilateral iliac opposite hypothesis, namely, that 20 minutes after lesion, 36.8±3.2 ml/kg, than following unilateral lesion, trauma, fluid resuscitation does promote hemodynamic benefits while no fluid resuscitation is associated with 44 J Vasc Br 2002, Vol. 1, Nº1
Experimental models of vascular trauma – Poli de Figueiredo et alii Oxygen delivery, oxygen consumption, hemoglobin and base deficit levels (mean ± SEM) during 120minutes of uncontrolled retroperitoneal hemorrhage for UL (unilateral iliac artery lesion, n=11) and BL(bilateral iliac arteries lesions, n=11) groups Baseline
O2 delivery (mLO2/min)
O2 consumption (mLO2 /min/m)
Hemoglobin (g/dl)
Base excess (mMol/L)
low cardiac output and metabolic derangement.
required to further clarify the key issue of fluid Moreover, no increase in intraabdominal bleeding resuscitation in trauma. On the positive side, a 2-3 mm followed either of the fluid resuscitation regimens. It iliac artery tear in a spontaneously breathing dog caused could be argued that treated animals were not restored a major hemorrhage, which closely mimics a penetrating to baseline arterial pressure, thereby decreasing the abdominal injury affecting a large vessel. Eight dogs possibility of clot disruption and consequent rebleeding, died before treatment, and were excluded from the which is the basis for the hypotensive resuscitation analysis. These animals presented rapid hypotension, concept.5 Two deaths occurred before the end of the below the 20 mmHg mark, followed by cardiac arrest.
experiment after large volume resuscitation only in LR The majority of survivors also presented a rapid drop in group. These animals rank among the four highest mean arterial pressure to the 25 - 45 mmHg range, five blood losses in the entire protocol, but the arteriotomy minutes after the lesion, suggesting that most bleeding size was not different from all other animals.
occurs immediately. These findings show that our There are limitations in our iliac artery tear model, model is adequate, since it is very similar to civilian as is also true for all controlled and uncontrolled series, in which several victims sustaining iliac artery hemorrhage models. Clinical presentations of trauma lesions die on their way to the hospital, and most of the victims are complex, transport conditions vary, and ones who reach the surgical theater present acute prehospital and emergency room protocols differ.
hemorrhagic shock caused by intraabdominal Resuscitation tends to be an ongoing process, while in our protocol animals where only observed for a short Transfemoral bilateral iliac artery puncture showed period and received no surgical correction. Therefore, to be a clinically relevant model of uncontrolled great caution should be exercised when extrapolating retroperitoneal hemorrhage, which induces a blood loss our findings to the clinical scenario. Our follow-up equivalent to 43% of the initial blood volume, moderate after treatment was deliberately very short: we chose to hypotension and a marked decrease in cardiac output.
finish our experimental protocol 40 minutes after the This condition is frequently observed in patients iliac artery tear, in order to precisely measure blood loss sustaining blunt trauma and pelvic fractures, in whom within the abdominal cavity. Our objective was to mortality is high, largely due to associated lesions and specifically address the ongoing controversy on whether retroperitoneal bleeding contributing to shock.8,19,20 fluid resuscitation, during prehospital setting, increases It is not known whether fluid resuscitation increases bleeding after a penetrating injury.2-5,14,15 A longer retroperitoneal hemorrhage and clinically relevant follow-up period, to include a survival evaluation, models of retroperitoneal hematoma are lacking. In our would have jeopardized this objective, but is obviously model, major hemodynamic and metabolic changes Experimental models of vascular trauma – Poli de Figueiredo et alii J Vasc Br 2002, Vol. 1, Nº1 45
were observed immediately after arterial punctures, conclude that bilateral iliac artery puncture through the without further derangement throughout the femoral arteries produce a clinically relevant model of experimental protocol. These data suggest that most of uncontrolled retroperitoneal hemorrhage, with the bleeding occurred within the first five minutes and hypotension and low flow state, while a unilateral iliac hemorrhage was severe enough to result in artery lesion causes a compensated shock state.
decompensation, since sustained hypotension, lowcardiac output and metabolic acidosis were observed.
No intraabdominal bleeding was observed, whichindicates that clot formation, increase in retroperitonealspace pressure and moderate hypotension effectivelyavoided continuous blood loss. Therefore, our model is References
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Fax: (11) 3068.9955 – Phone: (11) 3069.5297 Mortality in retroperitoneal hematoma. J Trauma DESTAQUE no próximo número do Jornal Vascular Brasileiro:
GUIDELINES
Prevention of venous thromboembolism
Guidelines compiled in accordance with the scientific evidence Chairman of Editorial Committee: A.N. Nicolaides
Co-editors: H.K. Breddin, J. Fareed, S. Goldhaber, S. Haas, R. Hull, E. Kalodiki, K. Myers, M. Samama, A. Sasahara.
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e Fernandes (Portugal), C. Fisher (Australia), J. Fletcher (Australia), M. Freeman (UK), S.Z Goldhaber (USA), L.J. Greenfield
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H. Roberts (USA), P. Roderick (UK), M Samama (France), A. Sasahara (USA), J.H. Scurr (UK), R. Simkin (Argentina), S.
Simonian (USA), A. Strano (Italy), M. Tsapogas (USA), A.G. Turpie (Canada), O.N. Ulutin (Turkey), M. Vandendriessche
(Belgium), M. Veller (South Africa), L. Villavincencio (USA), J. Walenga (USA), Z-G. Wang (China), D. Warwick (UK).
Int Angiol 2001;20:1-37.
Nosso agradecimento especial ao Professor A.N. Nicolaides e ao International Angiology
pela cessão dos direitos de reimpressão no J Vasc Br 2002;1(2).

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