Abdominal entry can be the most challenging step of a laparoscopic procedure. More than half of all laparoscopic complications occur during abdominal entry.1 Serious injury to bowel2 or blood vessels2,3 occur during insertion of the Veress needle or trocar, and unrecognized injuries can have catastrophic morbidity and mortality.4,5 Among patients who have had previous abdominal surgery, 25–50% experience development of adhesions between the abdominal wall and viscera.6–8 Adhesions to the abdominal wall bring bowel and blood vessels in close proximity to sites of laparoscopic entry.
Strategies to prevent injury during initial trocar insertion include alternative sites of entry such as Palmer's point, open laparoscopy, entry under direct visualization, and direct entry with mini-instruments. However, no one entry technique or instrumentation has reduced injuries according to a recent Cochran review.9 Consequently, development of a noninvasive, reliable test to detect adhesions may help surgeons anticipate difficult abdominal entries.
Ultrasonography has been used for many diagnostic and therapeutic indications in medicine. Previous investigators have described a useful ultrasound finding called the visceral slide, which is the presence of intra-abdominal viscera sliding in relation to the abdominal wall.10,11 The absence of this finding is associated with adhesions of viscera to the abdominal wall.12 We conducted a study to determine the accuracy of an office-based ultrasound test to detect obliterating periumbilical adhesions compared with two previously validated tests13 performed in the operating room. We believe that earlier detection of adhesions can enhance preoperative surgical planning, better-assess surgical risks, and improve patient safety.
MATERIALS AND METHODS
Female patients attending the Atlanta Center for Minimally Invasive Surgery and Reproductive Medicine between July 2012 and August 2013 were considered for enrollment in the study. Inclusion criteria were age older than 21 years, planned laparoscopic gynecologic surgery for benign disease, and the ability to understand the study and consent. Exclusion criteria were age younger than 21 years, uterine size more than 20 weeks of gestation (fundus of the uterus higher than the umbilicus), and no history of abdominal or pelvic surgery. Participants were prospectively enrolled during their preoperative visits during the times the investigators or study associates were available. The study was approved by the Institutional Review Board at Northside Hospital (Atlanta, Georgia).
We obtained basic demographic information such as age, race, body mass index (calculated as weight (kg)/[height (m)]2), gravidity, parity, medical history, and surgical history through interview and from medical records of the participants. Participants agreed to undergo three screening tests before laparoscopic surgery: (1) office visceral slide test; (2) preoperative examination with visceral slide test13; and (3) periumbilical ultrasound-guided saline infusion test13 to predict the presence of obliterating periumbilical adhesions. Two surgeons (E.C.D. and C.H.N.) performed each of the three ultrasound tests together, independently formulated a result, discussed their results, and ultimately agreed on one result. If there was a discrepancy, the response of the senior surgeon (C.H.N.) was recorded. Results were concurrent in 79 of 82 cases (96%). The same two surgeons then performed the laparoscopic surgery. The primary outcome was the presence of obliterating periumbilical adhesions. We defined obliterating periumbilical adhesions in accordance with the operative laparoscopy group as cohesive, apron-like, thick tissue including intra-abdominal organs such as small bowel that would prevent safe laparoscopic entry at the umbilicus.14 Secondary outcomes included the presence of any adhesions in the abdomen and pelvis, adverse events during laparoscopic entry, and perioperative complications.
The office visceral slide test was performed at the time of the patient's preoperative visit and examination in the office (Fig. 1). This test is explained and demonstrated in a narrated video supplement titled “The Office Visceral Slide Test,” which is available online at http://links.lww.com/AOG/A489. The office visceral slide test was conducted using a SonoSite ultrasonography with a 5.2-MHz abdominal transducer placed in a sagittal plane at the umbilicus and the ultrasound scan focused on the infraumbilical region between the anterior abdominal wall and the aorto-caval complex. A stable echogenic focus corresponding to omentum or intestine was identified (Fig. 2A) and the distance this focus traveled was recorded as the participant performed an exaggerated inspiration and exhalation (Fig. 2B). The visceral slide, the longitudinal distance the viscera traveled as visualized on ultrasonography from point A to point B, was noted. A normal visceral slide (positive test) is movement of the viscera more than 1 cm. An abnormal visceral slide (negative test) is defined as movement of the viscera less than 1 cm, as established by Tu et al.12
The preoperative examination with visceral slide test was conducted at the time of surgery in the operating room. After the patient was sterilely prepared and draped, the same type of ultrasonography with sterilely draped abdominal transducer was placed at the umbilicus in a sagittal plane. The visceral slide was observed using mechanically assisted exaggerated inspiration and exhalation. Mechanically assisted exaggerated inspiration and exhalation was defined as an elevated tidal volume of 1.5-times to twice the patient's baseline tidal volume and was achieved by controlled mechanical ventilation of the intubated patient in the supine position by an anesthesiologist or nurse anesthetist. The visceral slide was defined in accordance with the original definition10 as the longitudinal distance the intestines or omentum travels as visualized by ultrasonography during an exaggerated inspiration and expiration cycle. A normal visceral slide (positive test) was defined as movement of the viscera more than 1 cm. An abnormal visceral slide (negative test) was defined as movement of the viscera less than 1 cm.
After the preoperative examination with visceral slide, the third screening test, the periumbilical ultrasound-guided saline infusion test,13 was conducted. The sterilely draped transducer was placed in the sagittal plane at the umbilicus. The abdominal wall was elevated with towel clamps, and a sterile 19-gauge spinal needle on a syringe was advanced through the skin and subcutaneous layers under ultrasound guidance at a 90-degree angle. Once beyond the peritoneum, 10 mL sterile normal saline was injected under real-time ultrasound visualization (Fig. 3A). A normal test for periumbilical ultrasound-guided saline infusion was defined as dispersion of the infused saline without fluid loculation (Fig. 3B). The formation of a fluid pocket and nondispersion indicated an abnormal test result and suggested the presence of obliterating periumbilical adhesions. An inconclusive test was defined as one in which the physician was unable to definitively determine the normality or abnormality of the test.
Each of the three screening tests took approximately 2 minutes or less to perform. The surgical procedure was then continued at the discretion of the primary surgeon per standard protocol. With knowledge of the patient's clinical history and preoperative ultrasound testing, the surgeons used their clinical judgment to choose the method and site of entry. After successful entry into the abdominal cavity, assessment of adhesions around the umbilicus was performed. Adhesions under the umbilicus were categorized as obliterating or nonobliterating. Presence of any adhesions in the abdomen and pelvis were noted. Adverse events during laparoscopic entry and perioperative complications were also recorded.
Sample size determination was based on the primary outcome of obliterating periumbilical adhesions and calculated based on the 27% to 67% incidence of adhesions after laparotomy (previous study by Brill and Nezhat6). Based on the lower incidence of adhesions (27%), we calculated that 70 participants would be needed to achieve a power of 80% at α of 0.05% to detect a difference between accuracy of the screening tests. Descriptive statistics were used to explain the data. Results were reported as mean, standard deviation, and range of values, median (range of values), or number and percent. Analyses were performed using SPSS 20.0. Calculations of sensitivity, specificity, positive predictive value (PPV), negative predictive value (NPV), and diagnostic accuracy with 95% confidence intervals for diagnostic and screening test evaluation were performed with OpenEpi 2.3.1. Comparison of the sensitivities and specificities between the tests was performed with the extended McNemar test.15 In reporting the results of the study, we used the Standards for Reporting of Diagnostic Accuracy guidelines intended to increase the quality and validity of studies of diagnostic accuracy.16
Between July 2012 and August 2013, 87 women were asked to participate. Of these, three women declined to participate in the study, two participants were excluded because of the large size of their uterus, and 12 participants were excluded because they had no history of abdominal or pelvic surgery. Of the remaining participants, 70 women with a history of abdominal or pelvic surgery successfully enrolled and completed the study. The demographics and preoperative characteristics of the participants are described in Table 1.
The participants underwent surgery for a variety of benign indications. The study group (n=70) had a median of two (range, 1–6) previous abdominal surgeries. The median number of previous laparotomies was zero (range, 0–5). The median number of previous laparoscopies was one (range, 0–6). Entry location was the umbilicus in 69 of 70 laparoscopic entry procedures. The Palmer's point entry was performed in one case and open laparoscopy at the umbilicus was performed in one case in which umbilical adhesions were suspected based on abnormal preoperative test results and clinical history. In the other cases with abnormal test results, the patients had incisions in the left upper quadrant or pathology such that the umbilicus was considered as the safest site of entry. The incidence of obliterating periumbilical adhesions was 8.6% (6/70 cases). In all of these cases, the participants had a history of one or more laparotomies. Midline infraumbilical, midline supraumbilical incisions, and paramedian incisions had the highest incidences of periumbilical adhesions (Table 2). The incidence of any adhesions in the abdomen or pelvis was 25.7% (18/70 cases).
Tables 3, 4, and 5 describe the statistical measures of performance for the three screening tests compared with the gold standard of diagnostic laparoscopy to detect obliterating periumbilical adhesions. For the study group, the office visceral slide test had a sensitivity of 83.3%, specificity of 100%, PPV of 100%, NPV of 98.5%, and diagnostic accuracy of 98.6%. The preoperative examination with visceral slide test had a sensitivity of 83.3%, specificity of 96.8%, PPV of 71.4%, NPV of 98.4%, and diagnostic accuracy of 95.7%. The periumbilical ultrasound-guided saline infusion test had a sensitivity of 66.7%, specificity of 98.4%, PPV of 80%, NPV of 96.9%, and diagnostic accuracy of 95.7%. Although the sensitivities for the three tests are high, the 95% confidence intervals are wide because of the low incidence of obliterating periumbilical adhesions and small study population.
The extended McNemar test was performed to compare the sensitivities and specificities of the three screening tests to determine whether there is a statistically superior test for preoperatively diagnosing obliterating periumbilical adhesions. After comparing the office visceral slide test with the preoperative examination with visceral slide, the office visceral slide test with the periumbilical ultrasound-guided saline infusion test, and the preoperative examination with visceral slide with the periumbilical ultrasound-guided saline infusion test, with χ2=2 for each of these comparisons, 1 degree of freedom, and significance levels of P<.05, P>.20, and P<.10, there was no significant difference among the sensitivities and specificities of the three screening tests and no significantly superior screening test. However, the study was underpowered because of the unexpectedly low incidence of obliterating periumbilical adhesions.
Preoperative suspicion of intra-abdominal adhesions can improve surgical planning. Surgeons could minimize risks of complications resulting from adhesions by guiding port selection or opting instead to perform laparotomy if significant adhesions are predicted. Patients whose pretest probabilities suggest a high risk of significant adhesions may be considered better candidates for laparotomy. If a preoperative screening test can correctly predict a low risk of significant intra-abdominal adhesions, a minimally invasive approach could be used.
The advantages of a sensitive test performed during the preoperative office evaluation compared with the current adhesion screening performed after induction of anesthesia are as follows: provision of more accurate information to the patient about her planned procedure; efficient preoperative planning so that the patient preparation and positioning in the operating room is initially correct; and minimization of operating room and anesthesia time. This study shows that the sensitivity of the office visceral slide test is similar to the postanesthesia preoperative examination with visceral slide test and periumbilical ultrasound-guided saline infusion.
Several groups have made important advances in developing the ultrasound visceral slide technique for detecting intra-abdominal adhesions. Kodama et al10 first described the visceral slide as the longitudinal sliding of mobile abdominal contents between the deepest layer of the abdominal wall and the aorto-caval junction because of forces applied by respiratory excursions. They noted that restricted visceral slide less than 1 cm was noted beneath the surgical scar in 13 of 14 patients, and all patients with restricted visceral slide had adhesions present.10 Tu et al12 refined the parameters of the visceral slide and found that the sensitivity was maximized at a threshold above 1.5 cm, whereas specificity was highest under 0.8 cm. However, a lower limit of 1 cm for normal visceral slide optimized clinical utility by maximizing NPV without compromising PPV.12 Larciprete et al11 established that the intraobserver reproducibility and interobserver reproducibility of the visceral slide are excellent and have a low coefficient of variation.
In this study, the office visceral slide test was compared with the preoperative examination with visceral slide test and the periumbilical ultrasound-guided saline infusion test to establish its accuracy as a screening test. Previous studies of the visceral slide have had variable results. Our study shows that the sensitivity of the office visceral slide test is 83.7% for predicting dense infraumbilical adhesions, with NPV of 98.5%. All three tests showed similar NPV and sensitivity. This suggests that in similar patients, the office visceral slide test may reasonably replace the postanesthesia tests. The strengths of the office visceral slide test to predict intra-abdominal adhesions are many. The technique of visceral slide is easy to understand and learn. Simplifying the test to a single site, the infraumbilical site, and focusing on the risk of obliterating adhesions maximize the value of the test to determine the adhesions that pose the highest risk for trocar-related bowel and vascular injuries. The test is cost-effective, quick to perform in the office, nonpainful, and has good patient acceptability.
The strength of this study is its prospective study design comparing the three different screening tests in the same participant with two investigators rating each test, which increases scoring consistency and reduces differences in technique as a cause of error.
Our study also has limitations. The small number of participants and low prevalence of obliterating periumbilical adhesions resulted in the study being underpowered. Second, the population included primarily white middle-aged women. Third, the study included potential information bias because of the investigators' knowledge of the participants' medical and surgical histories while performing the three screening tests. Previous knowledge could bias the surgeon's interpretation of these tests because of a high or low pretest probability for adhesions. However, in this study the office visceral slide test had no false-positive results (n=0), but at the same time there was a low number of false-negative results (n=1). Although it would have been ideal to blind the investigators to the participants' medical and surgical histories, the unblinded protocol may simulate the actual clinical setting in which the surgeon or radiologist knows the patient's history when ultrasonography is performed and the pretest probability for the risk of obliterating periumbilical adhesions is developed. Thus, at the risk of introducing information bias, the office visceral slide test performed without blinding may be more valid because it better-simulates its use in clinical practice. Finally, the three screening tests similarly predicted the absence of obliterating periumbilical adhesions in this population. However, the unexpectedly low prevalence of adhesions in the study group prevented robust conclusions. Thus, the office visceral slide test for preoperative planning has the potential for predicting deleterious infraumbilical adhesions as well as postanesthesia testing strategies currently in use.
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