Renal arterial resistive index response to intraabdominal hypertension in a porcine model*

Laboratory Investigations

Renal arterial resistive index response to intraabdominal hypertension in a porcine model* Andrew W. Kirkpatrick, MD, FACS; Robert Colistro, MD; Kevin B. Laupland, MD; Daniel L. Fox, MB, ChB; David E. Konkin, MD; Volker Kock, PA; John R. Mayo, MD; Savvas Nicolaou, MD

Objective: The abdominal compartment syndrome is a potentially life-threatening condition with frequent renal involvement. There are few if any means of inferring subclinical effects before organ dysfunction. Because intrarenal pressure correlates with renal sonographic indices in other renal diseases, the purpose of this study was to determine the relationship between increasing intraabdominal hypertension and renal vascular flow velocities in a porcine model using renal Doppler ultrasound. Design: Animal study. Setting: University research laboratory. Subjects: Eight anesthetized, mechanically ventilated, wellhydrated, 30-kg female Yorkshire pigs. Interventions: Intraabdominal hypertension was induced by instillation of warmed intraperitoneal saline through a midline laparoscopic port. Intraabdominal pressure (IAP) was continuously monitored directly from the peritoneum and indirectly from the bladder. IAP was varied from 0 to 50 mm Hg in increments of 5 mm Hg. At each IAP level, gray-scale, color, and spectral Doppler renal arcuate artery ultrasound was obtained and resistive index (RI) and peak airway pressure calculated.

I

ntraabdominal hypertension (IAH) effects almost every human organ system, but is typically clinically recognized as cardiac, respiratory, and renal dysfunction (1– 6). In its most advanced degree, when associated with new organ failure, it is known as the abdominal compartment syndrome (ACS) (7). These

*See also p. 320. From the Departments of Surgery (AWK), Critical Care Medicine (AWK, KBL), and Medicine (KBL), Foothills Medical Centre, Calgary, Alberta, Canada; the Departments of Radiology (RC, DLF, JRM, SN) and Surgery (DEK), Vancouver Hospital and Health Sciences Centre, Vancouver, British Columbia, Canada; and the Department of National Defense, Ottawa, Ontario, Canada (VK). The authors have not disclosed any potential conflicts of interest. Presented, in part, in poster format (by Dr. Colistro) at the First World Congress on Emergency and Intensive Care Ultrasound, June 11, 2005, Milan, Italy, where it was awarded the first prize in intensive care research. Copyright © 2006 by the Society of Critical Care Medicine and Lippincott Williams & Wilkins DOI: 10.1097/01.CCM.0000249824.48222.B7

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Measurements and Main Results: Excellent agreement between direct and indirect IAP was found (bias, 0.032 mm Hg; 95% limits, ⴚ5.5 to 5.6 mm Hg). A linear relationship between RI and indirect IAP was observed and was defined by the regression equation: RI ⴝ 0.553 ⴙ 0.0104 ⴛ bladder pressure. There was a trend toward different RIs between left and right kidneys (p ⴝ .052) at the same IAP. RI varied in a linear fashion at low peak airway pressure and demonstrated an inflection point with steeper subsequent slope after peak airway pressure of 30 cm H2O. RI values rapidly returned to near baseline after abdominal decompression. Conclusions: In this model, the renal artery RI correlated strongly and linearly with the severity of intraabdominal hypertension, making renal Doppler ultrasound a potential noninvasive screening tool for the renal effects of intraabdominal hypertension. Further studies are warranted. (Crit Care Med 2007; 35:207–213) KEY WORDS: intraabdominal hypertension; postoperative renal failure; critical care; sonography; Doppler sonography

syndromes have been increasingly recognized in the last decade (5, 8, 9), even among populations who have not had abdominal surgery or even a primary intraabdominal problem, a condition referred to as secondary IAH/ACS (6, 10 –12). As untreated, ACS invariably leads to death (13, 14); it is assumed that either prophylaxis or earlier intervention to reduce IAH might improve the previously dismal outcomes of established ACS (12, 15). This increased attention, presumably facilitated by the acceptance of routine and often continuous monitoring (6, 16), has led to the frequent detection of severe IAH not apparently associated with obvious organ failure. In this situation, surgeons have been reluctant to perform decompressive laparotomies, recognizing the many associated complications of an open abdomen (17, 18). Given the sensitivity of the gut mucosa to hypoperfusion, gastric tonometry has been suggested as one technology that might offer modalities that provide insight into which patients may go on to develop end-organ

dysfunction and who thus benefit from earlier interventions designed to reduce IAH (15, 19, 20). The kidneys are particularly susceptible to IAH (21), presumably due to the serial nature of the renal vasculature (22). Thus, increased intraabdominal pressure (IAP) may begin to affect renal function at only 10 mm Hg and markedly impairs renal function at pressures as low as 20 mm Hg (23, 24). This low pressure threshold suggests that the kidney might be a potential marker to indicate adverse physiologic effects, thus prompting intervention at an earlier spectrum of disease. During the last two decades, a great deal of clinical and laboratory experience with alterations in the Doppler waveform analysis of the kidneys, semiquantified as the resistive index (RI), has accumulated for both acute and chronic renal diseases (25–27). This index has been thought to indirectly reflect the degree of resistance in the intrarenal vasculature (28). There has been varied clinical and laboratory experiences suggesting 207

that this index is either very useful (29 –31) or quite unreliable (32, 33). It has emerged from further analysis of these seemingly paradoxic results that it is the intrarenal pressure per se that most affects the conductance and arterial distensibility of the renal vascular bed, resulting in elevated RIs, rather than the overall mean renal vascular resistance (34, 35). Given the primacy of intrarenal pressure in determining RI values (36), we thus undertook initial studies to discern whether sonographic measures would noninvasively indicate physiologic and pathophysiologic changes in a porcine model of IAH.

METHODS Ethical approval for the study was granted by the University of British Columbia Animal Care Committee (protocol A03-0290). Eight female Yorkshire pigs were fasted overnight before the study to reduce bowel gas and to allow safe anesthesia. Anesthesia was induced with intramuscular ketamine (10 mg/kg), and each animal underwent endotracheal intubation. Positioned supine on warming pads, each pig was ventilated with a Drager artificial ventilation system (Drager North America, Telford, PA). General anesthesia was maintained with inhalational 1% halothane. Peripheral intravenous access was obtained and maintenance fluids were provided using lactated Ringer solution at a standardized rate (total for a 24-hr period: first 10 kg, 100 mL/kg; next 10 kg, 50 mL/kg; 10 mL/kg thereafter). The electrocardiogram was monitored continuously. An indwelling urinary catheter was inserted to measure bladder pressure. Baseline Doppler ultrasound examinations (Acuson Sequoia, Siemens Medical Solutions, Mountain View, CA) and calculation of RIs were performed on each kidney. RIs were calculated automatically by the ultrasound machine using standard methodology (RI ⫽ [peak systolic velocity ⫺ peak diastolic velocity]/peak systolic velocity). Each study animal was similarly instrumented. A standard 12/5-mm laparoscopic port was inserted through the midline anterior abdominal wall. Thereafter the peritoneal cavity was infused with warmed normal saline to obtain the chosen pressure level, followed by an equilibrium phase for ⱖ60 secs. IAP was monitored with both continuous direct intraperitoneal and intermittent intravesical pressure transducers, without instilling any fluid into the bladder but ensuring a continuous fluid column in the catheter. All pressure measurements were recorded at end-expiration after being zeroed at the midaxillary line as per World Society on Abdominal Compartment Syndrome Guidelines (7, 37). Direct IAP was varied from between 0 and 50 mm Hg in increments of 5 mm Hg based on direct IAP. Direct IAPs were compared with transduced pressures from the urinary bladder.

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Figure 1. Agreement between direct and bladder intraabdominal pressure (IABP) determinations. Bland-Altman plot of agreement between directly measured IABP and indirectly measured IABP (Foley catheter measurements). The solid line represents the bias and dashed lines the limits of agreement.

Figure 2. Linear relationship between resistive index (RI) and bladder pressure. Scatterplot of left renal RI at varying levels of bladder pressure in eight pigs. The linear regression line defined by the equation RI ⫽ 0.553 ⫹ 0.0104 ⫻ bladder pressure is shown with 95% confidence limits.

Doppler ultrasound interrogation of segmental and arcuate renal arteries was performed on both kidneys in succession, first right then left. RIs were calculated from the measured peak systolic and end-diastolic velocities of arcuate vessels. Peak airway pressure was recorded and qualitative two-dimensional ultrasound assessments of renal morphology were made at each abdominal pressure. After recordings at IAP of 50 mm Hg, a midline decompressive laparotomy was performed and saline evacuated from the abdomen. After a minimum 120-sec equilibrium phase, segmental and arcuate renal arteries were again interrogated with Doppler ultrasound and RIs calculated. All statistical analyses were performed using Stata 9.0 (StataCorp, College Station, TX). Agreement between two different measurement techniques were assessed using Bland-Altman plots with reporting of the bias and the 95% limits of agreement (38). For comparison between left- and right-sided measurements using

the RI, a paired t-test was used. Given that the right kidney was assessed first and therefore the left kidney had longer time of exposure to the increased IAP, left-sided measurements alone were used to predict the linear relationship between RI and bladder and other pressures using least-squares linear regression. In all comparisons, a p value of ⬍.05 was deemed to represent statistical significance.

RESULTS There was excellent average agreement between bladder pressure measurements and direct IAP determinations across a range of pressures, as shown in Figure 1. The bias was 0.03 mm Hg (SD 2.76) and the 95% limits of agreement were ⫺5.49 to 5.55 mm Hg. For the determination of RI at a given IAP, a trend was observed for paired measurements to be slightly higher among the left kidney as compared with the right Crit Care Med 2007 Vol. 35, No. 1

Table 1. Resistive index (RI) values calculated from linear regression model Intraabdominal Pressure, mm Hg

Calculated RI Value

12 15 20 25 40

0.68 0.71 0.76 0.81 0.97

RI ⫽ 0.55 ⫹ 0.01 ⫻ bladder pressure (in millimeters of mercury).

(mean difference RI, 0.016 ⫾ 0.069; 95% confidence interval, ⫺0.000, 0.0313; p ⫽ .052). A positive linear relationship was observed between increasing intravesical pressures and left renal RI, as shown in Figure 2. The least-squares linear regression line for this relationship was defined by the equation: RI ⫽ 0.553 ⫹ 0.0104 ⫻ bladder pressure (in millimeters of mercury). In this model, IAP of 25 mm Hg predicted an RI of 0.81 (Table 1). The peak systolic velocity linearly increased and the peak diastolic velocity linearly decreased with increasing IAP, as expected based on the RI relationship (Figs. 3 and 4). A nonlinear relationship existed between peak airway pressure and IAP. Although the RI varied in a relatively positive linear relationship at low airway pressures, there seemed to be a point of inflection between 30 and 40 mm Hg, with a steeper slope at higher pressures (Fig. 5). Representative sonographic images are given in Figures 6 – 8. Qualitative observations included a trend toward increasing renal echogenicity with increasing IAPs. Increased renal echogenicity is a nonspecific finding, and when identified, the term “medical renal disease” is given. Also, a reduction in renal size and renal excursion with respiration was observed at IAPs of ⬎15 mm Hg. Assessment of renal venous physiology demonstrated patency at all recorded IAPs; however, phasic venous flow was dampened at the extreme end of iatrogenic IAH. After decompressive laparotomy, renal RI returned to within normal range values near baseline for each animal within 120 secs. Renal size and excursion with respiration also quickly returned to baseline. One animal (pig 4) was noted to have hydronephrosis at baseline gray-scale sonography, with a baseline IAP of 3 mm Hg. The consequent RIs were 0.73 for the right kidney and 0.78 for the left kidney. Despite these abnormal baseline values, the RIs consisCrit Care Med 2007 Vol. 35, No. 1

Figure 3. Relationship between peak diastolic velocity and intraabdominal pressure. Scatterplot of peak diastolic velocity at varying levels of bladder pressure in eight pigs. The linear regression line defined by the equation peak diastolic velocity ⫽ 0.16 ⫺ 0.004 ⫻ bladder pressure is shown with 95% confidence limits.

Figure 4. Relationship between peak systolic velocity and intraabdominal pressure. Scatterplot of peak systolic velocity at varying levels of bladder pressure in eight pigs. The linear regression line defined by the equation peak systolic velocity ⫽ 0.21 ⫹ 0.005 ⫻ bladder pressure is shown with 95% confidence limits.

Figure 5. Relationship between peak airway pressure and resistive index (RI). Scatterplot of RI at varying levels of peak airway pressure (in millimeters of mercury) in eight pigs.

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Figure 6. Porcine kidney submitted to 10 mm Hg of intraabdominal pressure.

Figure 7. Porcine kidney submitted to 25 mm Hg of intraabdominal pressure.

tently increased with increased IAP to become 1.0 bilaterally at 20 mm Hg, reflecting no diastolic flow velocity.

DISCUSSION The principle finding of this study was that the RI was linearly related to the IAP. Although this might be expected from renal studies with other disease processes, this finding has not been described in the setting of IAH to our knowledge. Our data suggest that a noninvasive bedside sonographic examination might provide early evidence of a kidney being subjected to fully reversible vascular stresses due to IAH, before other irreversible changes being manifested. 210

Acute renal failure complicating injury, illness, surgical, and interventional procedures is a serious complication, resulting in morbidity and death (39). The mortality of postinjury or surgical acute renal failure continues to exceed 50%, despite the institution of continuous renal replacement therapies (39 – 41). The kidneys are physiologically at risk of IAH, with a functional anatomy that depends on ultrafiltration, resorption, and secretion, having two capillary beds in series (22), and are bound by a tightly restraining renal capsule (42). Mathematical substitution and a consideration of renal physiology emphasizes this sensitivity. The filtration gradient, the mechanical force across the glomerulus, is the differ-

ence in pressure head between the glomerular filtration pressure and proximal tubular pressure. Under sustained increases in IAP, the proximal tubular pressure can be considered, essentially, the IAP (43– 45). The filtration gradient equals the glomerular filtration pressure minus proximal tubular pressure. Because the glomerular filtration pressure itself is the difference between mean arterial pressure minus IAP, substituting mathematically reveals that the filtration gradient can be considered as the difference between mean arterial pressure and twice the IAP. Harman et al. (23) evaluated renal function in kidneys subjected to 20 mm Hg of extrinsic pressure, noting that the glomerular filtration rate and renal blood flow decreased to 21% and 23% of normal, despite maintenance of a cardiac output of 83% of normal, noting a 555% increase in renal vascular resistance compared with only a 30% increase in systemic vascular resistance. Although not well appreciated, IAH is not only very common in the critically ill (8, 46) but also is an independent cause of renal dysfunction (44). In 1995, Sugrue et al. (21) reported the results of routine bladder pressure monitoring after laparotomy in 88 patients, noting measurements of ⬎20 mm Hg in 33% of the group. This level of increased IAP carried a 12- and 11-fold increased association of renal dysfunction and death, respectively, although increased IAP preceded renal dysfunction in only 35% of patients (21). Further prospective studies of 263 postoperative intensive care unit patients noted that IAP of ⬎18 mm Hg occurred in 40% of patients, with renal impairment occurring in 32%, being independently associated with increased IAP, hypotension, sepsis, and older age. Further, the rate of renal impairment seemed to be dose related, with the rate of renal impairment doubling at 25 mm Hg compared with 18 mm Hg (44). Biancofiore et al. (47) reported that 31% of post–liver transplant patients had IAPs persistently ⬎25 mm Hg and that 41% were consistently ⬎18 mm Hg. Those developing renal failure had significantly higher mean IAP than those who did not (28 mm Hg vs. 19 mm Hg). Although it has been suggested that earlier intervention in cases of increased IAP might ameliorate the pathologic consequences of the ACS (5, 12, 44, 48 –52), intervening after overt organ dysfunction does not seem to ameliorate the course of renal dysfunction. Sugrue et al. (48) Crit Care Med 2007 Vol. 35, No. 1

Figure 8. Porcine kidney submitted to 35 mm Hg of intraabdominal pressure.

found that although decompressing the abdomen improved the mean IAP (from 24 to 14 mm Hg) and lung compliance (24 to 28 mL/cm H2O), there was no overall improvement in urine output and serum creatinine, leading to the conclusion that abdominal decompression alone will not reverse the renal sequelae of excessive IAP once established. Measurement of RI may be a means by which the early onset of ACS might be detected so as to allow intervention before its overt development and potentially irreversible consequences. Treatment of these syndromes, once diagnosed, typically involves abdominal decompression through laparotomy and temporary closure. Thresholds for diagnosis and treatment are controversial and likely vary from patient to patient. Body mass index greatly influences the baseline IAP (9). This further complicates common numerical thresholds for defining IAH. Increased IAP itself is not synonymous with ACS. The greatest uncertainty and practice variation applies to IAH and no established organ dysfunction. Patients with IAPs of ⬍25 mm Hg have generally been observed (and frequently subjected to further futile crystalloid preloading), whereas those with higher pressures have been recommended to undergo decompression (11, 13, 53). Most challenging are those with IAPs between 16 and 25 mm Hg but no obvious syndrome. They are at great risk of deterioration and must be monitored closely— but how? An ideal noninvasive measuring device would be one that is safe, noninvasive, cheap, and that could Crit Care Med 2007 Vol. 35, No. 1

discriminate between those who will deteriorate and would thus benefit from decompressive laparotomy and those who would likely improve and who could thus be spared an open abdomen. Doppler sonography is a modality that might take advantage of the kidneys’ particular susceptibility to IAH. Despite the almost ubiquitous use of sonography in the critically ill patient, there has been remarkably little reported use in the care of the critically ill patient with IAH/ACS. This is in distinction to less acute renal pathology, for which there has been a large amount of work examining the potential of Doppler sonography to improve the sonographic assessment of renal dysfunction (35). RIs are vascular indices that are commonly calculated after renal transplantation, and although they do not discriminate the actual pathology, the finding of diminished, absent, or reversed diastolic flow in renal allografts almost always indicates pathologically increased renovascular impedance, except when severe hypotension is present (26, 33). RIs have also been used to study a number of renal processes such as obstructive uropathy (29, 54), acute renal failure (55), hypertension (31), and hemolytic-uremic syndrome (56). RIs are independent of both the diameter of the vessel and the angle of insonation (57). RIs in the range of 0.6 – 0.8 are considered normal, 0.8 – 0.9 are equivocal, and ⬎0.9 suggest increased vascular resistance (25), although some would consider any RI of ⬎0.7 abnormal (29).

We are unaware of any previous report regarding the potential utility of sonography for the early diagnosis of renal dysfunction secondary to IAH. However, Takano et al. (58) performed powerDoppler sonography of normal kidneys during increased IAP ranging from 0 to 100 mm Hg, in increments of 20 mm Hg, as induced by Valsalva maneuver, and noted decreased signals. In one case of ascites, renal power-Doppler studies demonstrated increased mean flow intensities after IAP had been decreased from 22 to 16 mm Hg by removing 1650 mL of fluid at paracentesis (58). This pilot model was intended to validate the relationship between the RI and variations of IAP. As such, it was not intended to quantify other indices of renal perfusion, such as the urine output, renal blood flow, glomerular filtration rate, abdominal perfusion pressure, or the filtration gradient (44, 45, 51), or to measure the renal responses to ischemia, shock, resuscitation, and reperfusion. Our regression equations used the indirectly measured bladder pressures rather than the directly measured intraperitoneal pressures, as the bias approached zero and bladder pressure measurements are more clinically relevant. We used no priming volume for our bladder pressure measurements, consistent with recent work that cautions against overdistending the bladder (59, 60). The study produced IAH through the direct instillation of intraperitoneal fluid, rather than elucidating a generalized shock/ischemia/ massive resuscitation/reperfusion sequence that would be expected to result in generalized edema of the both the abdominal cavity and abdominal wall, and in gastrointestinal ileus. The infused saline in this model likely provided a good sonographic window to evaluate the porcine kidneys. It is likely that the interrogation of the kidneys would not be as easy in clinical practice as in this study. The human kidneys are retroperitoneal organs, however, and thus may be interrogated through a simpler window than other intraperitoneal organs, even with gross abdominal distension and ileus. Although evaluation of the course of the main renal arteries in their entirety is usually not feasible, the intrarenal vasculature can be detected in virtually all patients (25). Other developments in sonographic techniques may also have future utility, including power-Doppler sonography (61), three- and four-dimensional 211

sonographic techniques (62), and improved sono-contrast agents (63). In this porcine model, renal arcuate artery RI correlated strongly with the severity of IAH, even at supraphysiologic extremes. IAP of 25 mm Hg marked the threshold of abnormal renal RI of 0.81, suggesting that renal Doppler ultrasound may be a potential noninvasive, bedside screening tool for early ACS and early detection of adverse end-organ physiologic effects on renal perfusion. Renal Doppler ultrasound may be the “canary” that will provide surgeons and intensivists with the needed early objective evidence of impending renal failure. The examination could be performed early in a resuscitation, thus providing baseline RI data that could be individualized, thus correcting for baseline factors such as chronic renal disease and obesity. This might potentially allow for timely decompressive therapy and temporary closure to alleviate renal and other end-organ dysfunction before the onset of potentially irreversible sequelae. Prospective studies in a human population are warranted.

REFERENCES 1. Schein M, Wittman DH, Aprahamian CC, et al: The abdominal compartment syndrome: The physiological and clinical consequences of elevated intra-abdominal pressure. J Am Coll Surg 1995; 180:745–752 2. Nathens AB, Brenneman FD, Boulanger BR: The abdominal compartment syndrome. Can J Surg 1997; 40:254 –258 3. Kirkpatrick AW, Brenneman FD, McLean RF, et al: Is clinical examination an accurate indicator of raised intra-abdominal pressure in critically injured patients. Can J Surg 2000; 43:207–211 4. Malbrain ML: Intra-abdominal pressure in the intensive care unit: Clinical tool or toy? In: Yearbook of Intensive Care and Emergency Medicine. Vincent JL (Ed). Berlin, Springer-Verlag, 2002, pp 792– 814 5. Malbrain ML: Is it wise not to think about intraabdominal hypertension in the ICU? Curr Opin Crit Care 2004; 10:132–145 6. Kirkpatrick AW, Balogh Z, Ball CG, et al: The secondary abdominal compartment syndrome: Iatrogenic or unavoidable? J Am Coll Surg 2006; 202:668 – 679 7. World Society on the Abdominal Compartment Syndrome, Executive Committee. Consensus Definitions, 2005. Available at: http:// www.wsacs.org/. Accessed March 29, 2006 8. Malbrain ML, Deeren D, De Potter TJR: Intra-abdominal hypertension in the critically ill: It is time to pay attention. Curr Opin Crit Care 2005; 11:156 –171 9. Malbrain ML, Chiumello D, Pelosi P, et al:

212

10.

11.

12.

13.

14.

15.

16.

17.

18.

19.

20.

21.

22.

23.

Prevalence of intra-abdominal hypertension in critically ill patients: A multicentre epidemiological study. Intensive Care Med 2004; 30:822– 829 Balogh Z, McKinley BA, Cocanour CS, et al: Secondary abdominal compartment syndrome is an elusive early complication of traumatic shock resuscitation. Am J Surg 2002; 184:538 –544 Balogh Z, McKinley BA, Cocanour CS, et al: Supranormal trauma resuscitation causes more cases of abdominal compartment syndrome. Arch Surg 2003; 138:637– 643 Maxwell RA, Fabian T, Croce M, et al: Secondary abdominal compartment syndrome: An underappreciated manifestation of severe hemorrhagic shock. J Trauma 1999; 47: 995–999 Burch JM, Moore EE, Moore FA, et al: The abdominal compartment syndrome. Surg Clin North Am 1996; 76:833– 842 Ivy ME, Atweh NA, Palmer J, et al: Intraabdominal hypertension and abdominal compartment syndrome in burn patients. J Trauma 2000; 49:387–391 Ivatury RR, Porter JM, Simon RJ, et al: Intraabdominal hypertension after life-threatening penetrating abdominal trauma: Prophylaxis, incidence, and clinical relevance to gastric mucosal pH and abdominal compartment syndrome. J Trauma 1998; 44: 1016 –1023 Balogh Z, Jones F, D’Amours S, et al: Continuous intra-abdominal pressure measurement technique. Am J Surg 2004; 188: 679 – 684 Mayberry JC, Goldman RK, Mullins RJ, et al: Surveyed opinion of American trauma surgeons on the prevention of the abdominal compartment syndrome. J Trauma 1999; 47: 509 –514 Kirkpatrick AW, Laupland KB, Karmali S, et al: Spill your guts! Perceptions of Trauma Association of Canada member surgeons regarding the open abdomen and the abdominal compartment syndrome. J Trauma 2006; 60:279 –286 Sugrue M, Jones F, Lee A, et al: Intraabdominal pressure and gastric intramucosal pH: Is there an association? World J Surg 1996; 20:988 –991 Balogh Z, McKinley BA, Holcomb JB, et al: Both primary and secondary abdominal compartment syndrome can be predicted early and are harbingers of multiple organ failure. J Trauma 2003; 54:848 – 861 Sugrue M, Buist MD, Hourihan F, et al: Prospective study of intra-abdominal hypertension and renal function after laparotomy. Br J Surg 1995; 82:235–238 Formation of urine by the kidney: I. Renal blood flow, glomerular filtration, and their control. In: Textbook of Medical Physiology. Eighth Edition. Guyton AC (Ed). Philadelphia, WB Saunders, 1991, pp 286 –307 Harman PK, Kron IL, McLachlan HD, et al: Elevated intra-abdominal pressure and renal function. Ann Surg 1982; 196:594 –597

24. Herman FG, Winton RF: The interaction of intrarenal and extrarenal pressures. J Physiol 1936; 87:77P–78P 25. Thurston W, Wilson SR: The urinary tract. In: Diagnostic Ultrasound. Second Edition. Rumack CM, Wilson SR, Charboneau JW (Eds). St. Louis, Mosby, 1998, pp 329 –397 26. Taylor KJ, Marks WH: Use of Doppler imaging for evaluation of dysfunction in renal allografts. AJR Am J Roentgenol 1990; 155: 536 –537 27. Drudi FM, Pretagostini R, Padula S, et al: Color Doppler ultrasound in renal transplant: Role of resistive index versus renal cortical ratio in the evaluation of renal transplant disease. Nephron Clin Pract 2004; 98: c67– c72 28. Rawashdeh YF, Horlyck A, Mortensen J, et al: Short- and long-term repeatability of intrarenal resistive index in the pig. Invest Radiol 2001; 36:341–346 29. Platt JF, Rubin JM, Ellis JH: Distinction between obstructive and nonobstructive pyelocaliectasis with duplex Doppler sonography. AJR Am J Roentgenol 1989; 153:997–1000 30. Shokeir AA, Nijman RJ, el Azab M, et al: Partial ureteral obstruction: Role of resistive index in stages of obstruction and release. Urology 1997; 49:528 –535 31. Ohta Y, Fujii K, Arima H, et al: Increased renal resistive index in atherosclerosis and diabetic nephropathy assessed by Doppler sonography. J Hypertens 2005; 23:1905–1911 32. Tublin ME, Dodd GD, Verdile VP: Acute renal colic: Diagnosis with duplex Doppler US. Radiology 1994; 193:697–701 33. Kelcz F, Pozniak MA, Pirsch JD, et al: Pyramidal appearance and resistive index: Insensitive and nonspecific sonographic indicators of renal transplant rejection. AJR Am J Roentgenol 1990; 155:531–535 34. Murphy ME, Tublin ME: Understanding the Doppler RI: Impact of renal arterial distensibility on the RI in a hydronephrotic ex vivo rabbit kidney model. J Ultrasound Med 2000; 19:303–314 35. Tublin ME, Bude RO, Platt JF: The resistive index in renal Doppler sonography: Where do we stand? AJR Am J Roentgenol 2003; 180: 885– 892 36. Rawashdeh YF, Horlyck A, Mortensen J, et al: Resistive index: An experimental study of acute complete unilateral ureteral obstruction. Invest Radiol 2003; 38:153–158 37. Sugrue M: Abdominal compartment syndrome. Curr Opin Crit Care 2005; 11: 333–338 38. Bland JM, Altman DG: Statistical methods for assessing agreement between two methods of clinical measurement. Lancet 1986; 327:307–310 39. Reddy VG: Prevention of postoperative renal failure. J Postgrad Med 2002; 48:64 –70 40. Tang IY, Murray PT: Prevention of perioperative acute renal failure: What works? Best Pract Res Clin Anesthesiol 2004; 18:91–111 41. Jarnberg PO: Renal protection strategies in

Crit Care Med 2007 Vol. 35, No. 1

42.

43.

44.

45. 46.

47.

48.

49.

the perioperative period. Best Pract Res Clin Anesthesiol 2004; 18:645– 660 Stone HH, Fuldenwider JT: Renal decapsulation in the prevention of post-ischemic oliguria. Ann Surg 1977; 186:343–355 Caldwell CB, Ricotta JJ: Evaluation of intraabdominal pressure and renal hemodynamics. Curr Surg 1986; 43:495– 498 Sugrue M, Jones F, Deane SA, et al: Intraabdominal hypertension is an independent cause of postoperative renal impairment. Arch Surg 1999; 134:1082–1085 Ulyatt DB: Elevated intra-abdominal pressure. Australasian Anaesth 1992; 108 –114 Malbrain ML, Chiumello D, Pelosi P, et al: Incidence and prognosis of intraabdominal hypertension in a mixed population of critically ill patients: A multiple-center epidemiological study. Crit Care Med 2005; 33: 315–322 Biancofiore G, Bindi ML, Romanelli AM, et al: Postoperative intra-abdominal pressure and renal function after liver transplantation. Arch Surg 2003; 138:703–706 Sugrue M, Jones F, Janjua KJ, et al: Temporary abdominal closure: A prospective evaluation of its effects on renal and respiratory physiology. J Trauma 1998; 45:914 –921 Bloomfield G, Saggi B, Blocher C, et al: Physiologic effects of externally applied continuous negative abdominal pressure for intra-

Crit Care Med 2007 Vol. 35, No. 1

50.

51.

52.

53.

54.

55.

56.

57.

abdominal hypertension. J Trauma 1999; 46: 1009 –1016 Ivatury RR: Abdominal compartment syndrome: A century later, isn’t it time to pay attention? Crit Care Med 2000; 28:2137–2138 Cheatham ML, White MW, Sagraves SG, et al: Abdominal perfusion pressure: A superior parameter in the assessment of intra-abdominal hypertension. J Trauma 2000; 49:621– 627 Malhotra SK, Nakra D: Detection of impending abdominal compartment syndrome. Anaesthesia 2004; 59:1138 –1148 Meldrum DR, Moore FA, Moore EE, et al: Prospective characterization and selective management of the abdominal compartment syndrome. Am J Surg 1997; 174:667– 673 Platt JF, Rubin JM, Ellis JH: Acute renal obstruction: Evaluation with intrarenal duple Doppler and conventional US. Radiology 1993; 186:685– 688 Platt JF, Rubin JM, Ellis JH: Acute renal failure: Possible role of duplex Doppler US in distinction between acute prerenal and acute tubular necrosis. Radiology 1991; 179: 419 – 423 Patriquin HB, O’Regan S, Robitaille P, et al: Hemolytic-uremic syndrome: Intrarenal arterial Doppler patterns as a useful guide to therapy. Radiology 1989; 172:603– 604 Sacerdoti D, Gaiani S, Buonamico P, et al: Interobserver and interequipment variabil-

58.

59.

60.

61.

62.

63.

ity of hepatic, splenic, and renal arterial resistance indices in normal subjects and patients with cirrhosis. J Hepatol 1997; 27:986 –992 Takano R, Ando Y, Taniguchi N, et al: Power Doppler sonography of the kidney: Effect of Valsalva’s maneuver. J Clin Ultrasound 2001; 29:384 –388 De Waele J, Pletinckx P, Blot S, et al: Saline volume in transvesical intra-abdominal pressure measurement: enough is enough. Intensive Care Med 2006; 32:455– 459 Malbrain ML: Different techniques to measure intra-abdominal pressure (IAP): Time for a critical re-appraisal. Intensive Care Med 2004; 30:357–371 Kuwa T, Cancio LC, Sondeen JL, et al: Evaluation of renal cortical perfusion by noninvasive power Doppler ultrasound during vascular occlusion and reperfusion. J Trauma 2004; 56:618 – 624 Chang CH, Yu CH, Ko HC, et al: Quantitative three-dimensional power doppler sonography for assessment of the fetal renal blood flow in normal gestation. Ultrasound Med Biol 2003; 29:929 –933 Wei K, Le E, Bin JP, et al: Quantification of renal blood flow with contrast-enhanced ultrasound. J Am Coll Cardiol 2001; 37: 1135–1140

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