Annals of Vascular Surgery
Volume 24, Issue 3 , Pages 321-327, April 2010

Retroperitoneal Approach to Abdominal Aortic Aneurysm Repair Preserves Splanchnic Perfusion as Measured by Gastric Tonometry

  • Nityanand Arya

      Affiliations

    • Vascular and Endovascular Unit, Belfast City Hospital, Belfast, UK
    • Corresponding Author InformationCorrespondence to: Mr Nityanand Arya, Specialist Registrar, Level 5, Vascular Unit, Belfast City Hospital, Belfast BT9 7AB, UK
  • ,
  • Muhammad Anees Sharif

      Affiliations

    • Vascular and Endovascular Unit, Belfast City Hospital, Belfast, UK
  • ,
  • Luk Louis Lau

      Affiliations

    • Vascular and Endovascular Unit, Belfast City Hospital, Belfast, UK
  • ,
  • Bernard Lee

      Affiliations

    • Vascular and Endovascular Unit, Belfast City Hospital, Belfast, UK
  • ,
  • Raymond J. Hannon

      Affiliations

    • Vascular and Endovascular Unit, Belfast City Hospital, Belfast, UK
  • ,
  • Ian S. Young

      Affiliations

    • Department of Medicine, Queen's University, Mulhouse Building, Grosvenor Road, Belfast, UK
  • ,
  • Chee Voon Soong

      Affiliations

    • Vascular and Endovascular Unit, Belfast City Hospital, Belfast, UK

published online 11 September 2009.

Article Outline

Background

We investigated if minimizing bowel manipulation and mesenteric traction using the retroperitoneal approach in open abdominal aortic aneurysm (AAA) repair preserves splanchnic perfusion, as measured by gastric tonometry, and reduces the systemic inflammatory response and dysfunction of the various organs.

Methods

Patients undergoing elective AAA repair were randomized into three groups. Group I had repair via the retroperitoneal approach, while groups II and III were repaired via the transperitoneal approach with the bowel packed within the peritoneal cavity or exteriorized in a bowel bag, respectively. A tonometer was used to measure gastric intramucosal pH (pHi), as an indicator of splanchnic perfusion, just prior to aortic clamping, during clamping, and at 0.5, 1, 2, 4, 6, and 12hr after clamp release. Multiorgan dysfunction syndrome (MODS) and systemic inflammatory response syndrome (SIRS) scores were calculated and systemic interleukins (IL-6 and IL-10) measured at predetermined intervals.

Results

Thirty-four patients were successfully randomized. The gastric pHi was significantly lower in group II (n=12) and group III (n=11) compared to group I (n=11) during aortic clamping and immediately after clamp release (p<0.05). The aortic clamp time, blood loss, MODS and SIRS scores, and systemic cytokine response were similar in all three groups. When the three groups were combined, there were significant positive correlations between the operation time, aortic clamp time, and amount of blood lost and transfused with plasma IL-6 levels and MODS score on the first postoperative day.

Conclusion

The retroperitoneal approach for open AAA repair is associated with gastric tonometric evidence of better splanchnic perfusion compared to the transperitoneal approach.

 

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Introduction 

Between 20% and 50% of patients undergoing elective open repair of abdominal aortic aneurysm (AAA) may develop single- or multiorgan dysfunction in the postoperative period.1, 2 Although the exact etiology of multiorgan dysfunction syndrome (MODS) following AAA repair remains unclear and most likely multifactorial, intestinal ischemia has been suggested to play an important role.3, 4

During transperitoneal AAA repair, intestinal manipulation and mesenteric traction may contribute to impairment of intestinal mucosal barrier function and allow permeation of luminal contents and bacterial products, such as endotoxin, across the intestinal wall.5 This is followed by activation of the inflammatory cascade and release of cytokines such as interleukin-6 (IL-6) and IL-10, modulators of the systemic inflammatory response syndrome (SIRS) and MODS.3, 6, 7, 8, 9, 10

In support of this, previous studies have demonstrated that the retroperitoneal approach for AAA repair, which avoids peritoneal exposure and bowel manipulation, can reduce portal concentrations of IL-6, the systemic inflammatory response, and dysfunction of the various organs.11, 12 It is speculated that mesenteric traction and bowel manipulation associated with the transperitoneal approach of repairing AAA may cause vasoconstriction of the splanchnic vessels and intestinal ischemia.

Although severe intestinal ischemia leading to transmural bowel infarction is rare following elective AAA repair, subclinical intestinal ischemia affecting only the mucosa is not uncommon.3, 13, 14 Unfortunately, the detection of mild intestinal ischemia is difficult. Amid all the different techniques of detecting intestinal ischemia, one that has been demonstrated to be reliable, whether it is transmural infarction or just mucosal ischemia, is silicone tonometry, which indirectly measures the intestinal intramucosal pH (pHi). This has been shown to correlate well with intestinal oxygen consumption as oxygen delivery falls below a critical level.15 A reduction in sigmoid pHi following transperitoneal AAA repair has been shown to predict the development of colon ischemia and endotoxemia.3, 14 In addition, a decrease in gastric pHi level has been shown to prognosticate morbidity and mortality in critically ill patients.8, 16, 17, 18, 19

The aim of this study was to investigate if minimizing bowel manipulation and mesenteric traction using the retroperitoneal approach in open AAA repair preserves splanchnic perfusion, as measured by gastric tonometry, and reduces the systemic inflammatory response and dysfunction of the various organs.

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Methods 

Over a period of 22 months from January 2003, all patients undergoing elective open repair of infrarenal AAA were prospectively recruited into the study after written informed consent. Patients with aortoiliac aneurysms, chronic renal impairment (serum creatinine >100 umol/L), ongoing inflammatory process (e.g., inflammatory bowel disease, active rheumatoid arthritis), or previous laparotomy were excluded from the study. The study was approved by the local research ethics committee.

Patient Recruitment and Surgical Techniques 

Recruited patients were randomized into three groups using an envelope system. Group I patients had repair through the retroperitoneal approach, using a left flank incision. Group II and group III patients had their aneurysms repaired through a midline transperitoneal approach. In group II the bowel handling was kept to a minimum and the small bowel was packed within the peritoneal cavity, while in group III the small intestine was exteriorized into a plastic bowel bag and retracted to the right side of the abdominal wound to expose the infrarenal aorta. During the operation, a self-retaining retractor (OmniTract; Omni-Tract Surgical, St. Paul, MN) was routinely used in all three groups for wound retraction and exposure.

All patients had standardized general anesthesia with endotracheal intubation. Epidural analgesia was provided with an epidural catheter inserted at the T10 level. Antibiotic prophylaxis with cefuroxime 1.5g was administered at induction, and heparin (70IU/kg) was given intravenously prior to aortic clamping. All patients had their cardiac rhythm and rate, central venous pressure, and arterial blood pressure monitored. The mean arterial blood pressure was maintained within 10% of the preinduction value, and the intravascular volume was supplemented if required with 0.9% sodium chloride solution and 4% modified gelatin solution (Gelofusine; B. Braun, Melsungen, Germany) as guided by the central venous pressure. Pantoprazole 40mg was started preoperatively and continued for 3 days after the operation, to reduce the back-diffusion of hydrogen ions during acid secretion to improve the accuracy of gastric tonometric measurements.20, 21

All aneurysms were repaired using the inlay graft technique with a knitted polyester tube graft (InterGard; Intervascular, La Ciotat, France). Postoperative pain relief was provided by a continuous epidural infusion of bupivacaine and managed by the acute pain team per routine protocol. All patients were managed initially in the high dependency unit (HDU) or the intensive care unit (ICU) and later transferred to the vascular surgery ward when deemed appropriate.

The operative time, clamp time, and amounts of blood lost and transfused were recorded prospectively. In addition, the MODS and SIRS scores were calculated preoperatively and daily for 3 days after the operation.22, 23

Gastric Tonometry 

Gastric mucosal perfusion was assessed using air tonometry with the TRIP® silicone nasogastric tube (Datex-Engstrom, Charlottenlund, Finland) attached to the automated Tonocap TC-200 machine (Datex-Engstrom). After induction of anesthesia, the TRIP nasogastric tube was passed and its position in the stomach was confirmed by the operating surgeon. In the retroperitoneal group, the position was confirmed by auscultation over the stomach as air was injected through the tonometer and/or aspiration of gastric juice. The position of the tube was confirmed subsequently by X-ray in the immediate postoperative period.

The TRIP tonometer tube is a modified nasogastric tube with a semipermeable silicone balloon incorporated at the tip and a sampling line along its length. After allowing at least 10minutes for the concentration of carbon dioxide within the balloon to equilibrate with that of the gastric mucosa, the air in the balloon was withdrawn via the sampling line by the Tonocap machine, and the partial pressure of carbon dioxide (PCO2) measured. At the same time, an arterial sample of blood was taken for measurement of arterial pH (pHa) and arterial PCO2 (PaCO2), to allow the pHi to be calculated using the Henderson-Hasselbalch equation (pHi=pHa + log10 [PaCO2/PCO2]). pHi measurements were taken prior to aortic clamping (preclamp), 30 and 60min after clamping of the aorta (AC), and at 0.5, 1, 2, 4, 6, and 12hr after aortic clamp release (CR). Based on the results of previous studies in the literature, a pHi <7.30 was considered to indicate gastric ischemia.19

IL-6 and IL-10 Measurements 

Venous blood (10mL) was also collected in endotoxin-free tubes for measurements of IL-6 and IL-10 prior to surgery, just prior to aortic clamping, 2 and 6hr after aortic CR, and daily until the third postoperative day. The plasma of these samples was isolated within 10min of collection by centrifugation at 4°C and 460g, aliquoted into sterile cryotubes, and stored at −70°C until analysis. IL-6 and IL-10 concentrations were measured by enzyme-linked immunosorbent assay using the commercially available ELI-pair kits (Diaclone, Besancon, France). The detection ranges of IL-6 and IL-10 were 6.26-200 and 12.5-400pg/mL, respectively.

Statistical analysis was done on SPSS (version 12.0.1; SPSS, Inc., Chicago, IL), with all the results expressed as median (interquartile range). The results from the three groups were compared using the Kruskal-Wallis test, and if significant, intergroup comparisons were performed using the Mann-Whitney U-test. Contingency tables were tested by Fisher's exact test. p<0.05 was considered significant.

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Results 

The demographic details, premorbid medical conditions, and aneurysm size of the three groups of patients are detailed in Table I. Even though patients were randomly allocated to the three groups, group II patients were significantly older than those in group I or group III (p=0.04). The duration of operation, aortic clamp time, intraoperative blood loss, length of stay in the ICU or HDU, length of postoperative stay in hospital, and incidence of postoperative complications were similar in all three groups (Table II, Table III). Similarly, there was no significant difference in the intraoperative fluid requirement between the three groups.

Table I. Preoperative demographics
Group I (n=11)Group II (n=12)Group III (n=11)
Age (years)68 (63-72)75 (71-81)67 (59-74)
M:F10:111:110:1
AAA size (cm)6.4 (5.8-7.8)6.4 (5.7-7.6)6.6 (5.6-7.8)
HT799
IHD (MI/angina)433
Stroke300
Smoking81110
Hyperlipidemia659

HT, hypertension; IHD, ischemic heart disease; MI, myocardial infarction.

p =0.04, Kruskas-Wallis test.

Table II. Operative details and length of stay
Group IGroup IIGroup IIIp
Operative time (min)170 (160-225)168 (125-190)160 (130-195)0.24
Clamp time (min)65 (55-90)68 (50-83)60 (55-75)0.74
Blood lost (L)2 (1.4-3.9)2.8 (1.1-4.3)1.8 (1.3-2.8)0.54
Blood transfused (L)0.8 (0.4-1.2)1.1 (0.3-1.6)0.6 (0.2-1)0.45
Intraoperative fluid (L)5 (4.5-6.5)5 (4-7.1)5 (4.5-5.5)0.9
ICU/HDU stay (hr)23 (22-47)54 (27-88)48 (23-71)0.16
Postoperative stay (days)9 (7-10)9.5 (8-12)10 (8-13)0.28
Table III. Postoperative complications
Group IGroup IIGroup III
Chest infection/atelectasis353
Myocardial infarction100
Atrial fibrillation103
Wound infection122
Jaundice110
Ileus012

A transient drop in pHi during AC and after CR was observed in all the groups (Fig. 1). This reduction in pHi was significantly greater in groups II and III compared to group I at 0.5 and 1hr after AC and 0.5hr following CR. In fact, this difference in pHi between groups I and III was observed prior to AC (p=0.034), 0.5hr (p=0.004) and 1hr (p=0.001) during AC, and 0.5hr (p=0.005) and 1hr (p=0.013) after CR. The number of patients with significant gastric ischemic episodes, defined as pHi <7.30 on at least 50% of the time points measured, was greater in group III compared to group I; but this failed to reach statistical significance (p=0.09) (Fig. 2).

All patients showed a rise in plasma IL-6 and IL-10 concentrations and MODS and SIRS scores in the postoperative period (Table IV). However, there was no statistically significant difference between the three groups. When the data from all three groups were combined, there were significant positive correlations between operation time, AC time, and blood loss with plasma IL-6 and IL-10 levels and MODS score on the first postoperative day (Table V).

Table IV. Comparison of sequential changes in IL-6 and IL-10 concentrations and MODS and SIRS scores
GroupsPreoperative2hr after CR6hr after CRPOD 1POD 2
IL-6 (pg/mL)I<12172 (38-426)193 (24-263)127 (67-261)196 (83-346)
II<1297 (63-223)95 (39-212)123 (17-208)180 (73-302)
III<1282 (52-192)26 (16-190)92 (12-184)173 (59-245)

IL-10 (pg/mL)I<1263 (33-317)42 (13-132)12 (12-54)12 (12-55)
II<1275 (52-194)43 (12-149)12 (12-50)12 (12-22)
III<12151 (56-261)14 (12-37)12 (12-38)12 (12-12)

SIRS scoreI0 (0-0)--1 (0-2)1 (1-2)
II0 (0-0)--1 (1-2)2 (2-3)
III0 (0-0)--2 (1-2)2 (0-3)
MODS scoreI0 (0-0)--2 (1-3)2 (1-2)
II0 (0-1)--3 (2-3.75)2.5 (2-3.75)
III0 (0-0.75)--2 (2-3)2 (2-3)

POD, postoperative day.

Table V. Correlation between IL-6 and IL-10 levels and operative parameters (with the data of all three groups combined, n=34)
Spearman's correlation coefficient (p)
IL-6 (6hr after CR) (pg/mL)IL-10 (6hr after CR) (pg/mL)MODS score (POD 1)
Aortic clamp time0.523 (p=0.001)0.367 (p=0.039)0.410 (p=0.016)
Operation time0.529 (p=0.001)0.433 (p=0.011)0.243 (p=0.166)
Blood loss0.371 (p=0.03)0.282 (p=0.10)0.498 (p=0.003)
Blood transfused0.477 (p=0.004)0.358 (p=0.038)0.589 (p=0.000)

POD, postoperative day.

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Discussion 

Intestinal ischemia during AAA repair may occur as a consequence of multiple contributing factors. Clamping of the aorta and iliac arteries, reduced intraoperative arterial pressure, and splanchnic vasoconstriction as a result of local autonomic response are some of the factors that may reduce intestinal blood flow. Intestinal manipulation and traction on the mesentery during aortic exposure may add to the vasoconstriction of the mesenteric vessels and reduction in mean arterial pressure, both of which can exacerbate the resulting splanchnic ischemia.24, 25, 26 Although overt transmural intestinal ischemia is rare following elective AAA repair, milder forms of ischemia affecting only the mucosa are not uncommon.3, 13, 14, 27, 28 Unfortunately, the detection of intestinal ischemia, in particular that which is subclinical, is challenging.

One technique that has been well validated for clinical monitoring of intestinal perfusion is silicone tonometry, which measures pHi as an indicator of intestinal perfusion.15 This method of assessing intestinal perfusion has been popularized by Fiddian-Green et al.,28, 29 and pHi has been found to correlate well with other indicators of splanchnic perfusion. The development of low pHi or intramucosal acidosis has been shown to be indicative of intestinal ischemia and an accurate prognosticator of dysfunction of the various organs after AAA surgery.30, 31 Furthermore, it has been demonstrated that the development of intramucosal acidosis following AAA repair is not just confined to the sigmoid colon but can also be observed in the stomach.27, 32, 33 This suggests that the reduction in blood flow is not limited to the large bowel but may affect the entire intestinal tract.

In this study, the lower gastric pHi in group III compared to group I at the start of the operation, even before the aorta was cross-clamped, suggests that the mere acts of intestinal exposure and manipulation can affect splanchnic perfusion. However, as the gastric pHi consequently fell in all three groups when the aorta was cross-clamped and immediately following CR, other factors, which may be of greater significance, may amplify the splanchnic ischemia. However, the drop in pHi being significantly less in the retroperitoneal group with respect to both the transperitoneal groups implies that the absence of intestinal exposure and manipulation may minimize the degree of ischemia incurred by the intestine.

There was no difference in operative time, clamp time, and intraoperative fluid requirements between the three groups, suggesting the higher pHi in group I was unrelated to these factors. Similarly, there was no significant difference in pHa in the three groups at any of the time points measured. In addition, Nakatsuka27 demonstrated that the decrease in gastric mucosal pHi was not significantly correlated with cardiac output, implying that the decrease in pHi occurred in spite of adequate cardiac output and that local factors play a major role in influencing splanchnic perfusion in these patients.

There are, however, some drawbacks in the study. The number of patients with significant gastric ischemic episodes, defined as pHi <7.30 on at least 50% of the time points measured, was greater in group III compared to group I; but this failed to reach statistical significance (p=0.09). This may be due to a type II error because of the small number of patients in each group.

Previous work has also demonstrated that patients developing significant gastric intramucosal acidosis following AAA repair and cardiac surgery suffer from more major postoperative complications, especially those with persistently low pHi of more than 10hr duration.17, 18 In addition, low gastric pHi has been found to be predictive of perioperative mortality in patients presenting with ruptured AAA.4 As already pointed out, the number of patients in the present study was small, and this made it difficult to assess differences in mortality among the groups. Furthermore, none of the patients had persistently significant intramucosal acidosis. Although there was no significant difference in the MODS score between the three groups, a shorter hospital stay was observed in the retroperitoneal group.

A consequence of bowel ischemia is the disruption in mucosal barrier function resulting in endotoxemia and the generation of cytokines. Cytokines are pleiotropic polypeptides that play a central role in the development of SIRS and MODS and have been shown to predict perioperative morbidity following AAA repair.9, 10 The cytokine responses in the present study concur with those of other published reports.7, 9, 34 Both serum IL-10 and IL-6 rose within hours of the surgical insult and fell rapidly toward normal by the second or third day without any significant difference in the cytokine responses between the three groups. This is similar to the findings of Shindo et al.,12 who showed no significant difference in IL-6 and IL-8 concentrations in patients having transperitoneal and retroperitoneal repair of AAA, although the cytokine concentrations were higher during transperitoneal repair. They also found no significant difference between the groups in C-reactive protein concentration or SIRS score.12

Soong et al.3, 35 demonstrated that intramucosal acidosis of the sigmoid colon was associated with increased concentrations of plasma endotoxin and IL-6 during elective AAA repair. However, similar to Syk et al.,31 we failed to show such a correlation between pHi measurements and concentrations of IL-6 and IL-10. On the other hand, a positive correlation was found between operative clamp time, amounts of blood lost and transfused, and length of surgery with the concentrations of cytokines and MODS score. This suggests that the severity of operative stress is probably a more important influence on the host inflammatory response in the majority of patients undergoing AAA repair, with mesenteric traction and bowel manipulation playing only a cursory role at the start of the operation.

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Conclusion 

The results demonstrate that gastric mucosal perfusion is better maintained if bowel manipulation and mesenteric traction can be minimized using the retroperitoneal approach of repairing AAA. However, the lack of difference in the cytokine response between the groups suggests that direct bowel injury and the resulting ischemia may be too mild to contribute significantly to the development of SIRS and MODS. The correlation between the concentration of cytokines and MOD score and the amount of blood transfused implies that there are other more critical factors which may have greater influence on patient outcome following AAA repair.

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PII: S0890-5096(09)00128-9

doi:10.1016/j.avsg.2009.06.003

Annals of Vascular Surgery
Volume 24, Issue 3 , Pages 321-327, April 2010