Ultrasound in Med. & Biol., Vol. 41, No. 5, pp. 1241–1246, 2015 Copyright Ó 2015 World Federation for Ultrasound in Medicine & Biology Printed in the USA. All rights reserved 0301-5629/$ - see front matter
http://dx.doi.org/10.1016/j.ultrasmedbio.2015.01.009
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Original Contribution ULTRASONOGRAPHIC ASSESSMENT OF OPTIC NERVE SHEATH DIAMETER DURING PEDIATRIC LAPAROSCOPY JI YOUNG MIN,* JEONG-RIM LEE,* JUNG-TAK OH,y MIN-SOO KIM,* EUN-KYUNG JUN,* and JIWON AN* * Department of Anesthesiology and Pain Medicine, Anesthesia and Pain Research Institute, Yonsei University College of Medicine, Seoul, Republic of Korea; and y Department of Pediatric Surgery, Severance Children’s Hospital, Yonsei University College of Medicine, Seoul, Republic of Korea (Received 16 September 2014; revised 7 January 2015; in final form 16 January 2015)
Abstract—This study investigated the extent of the raised intracranial pressure resulting from carbon dioxide (CO2) pneumoperitoneum by ultrasonographically measuring optic nerve sheath diameter (ONSD) in children undergoing laparoscopic surgery. Twenty-five children aged less than 9 y (53.1 ± 23.3 mo, mean ± standard deviation) and scheduled for an elective laparoscopic surgery participated. ONSD was assessed using ocular ultrasonography 10 min after induction of anesthesia (T0), 10 min after induction of CO2 pneumoperitoneum at 10 mm Hg intra-abdominal pressure (T1) and in an anesthetized state without CO2 pneumoperitoneum at the conclusion of the surgery (T2). During CO2 pneumoperitoneum, ONSD increased significantly compared with ONSD after anesthesia induction (T0: 4.3 ± 0.3 mm, T1: 4.6 ± 0.3 mm, p , 0.05). In all enrolled patients, any neurologic complications were not observed during the intra-operative or post-operative period. In children undergoing laparoscopic surgery, an increase in ONSD was ascertained during CO2 pneumoperitoneum, and thus the corresponding increase in intracranial pressure could be predicted. (E-mail: [email protected]) Ó 2015 World Federation for Ultrasound in Medicine & Biology. Key Words: Ultrasound, Optic nerve sheath, Pediatric laparoscopy.
Although the insertion of an intracranial device is the most accurate method to measure ICP, performing this invasive method during laparoscopic surgery is virtually impossible because of neurosurgical unavailability and concerns about severe complications such as infection, hemorrhage and equipment malfunction (Geeraerts et al. 2008). Thus, the severity and tolerability of increased ICP caused by CO2 pneumoperitoneum are still unknown, especially in pediatric laparoscopy. Measurement of optic nerve sheath diameter (ONSD) using ocular ultrasonography is a simple, non-invasive and reproducible technique for assessing ICP. Previous studies have reported the reliability of ONSD for diagnosing and assessing an increased ICP in various clinical situations including traumatic brain injury, stroke, post-dural puncture headache and pre-eclampsia (Dubost et al. 2011, 2012; Dubourg et al. 2011; Geeraerts et al. 2008). Hence, it could be hypothesized that the extent of the increased ICP during pediatric laparoscopy could be confirmed without serious complications by monitoring ONSD using ocular ultrasonography instead of direct and invasive ICP measurement. To date, there have been no studies on the evaluation of ONSD during pediatric laparoscopy.
INTRODUCTION Laparoscopic surgery is a rapidly growing alternative technique to conventional open surgery. Its advantages include minimal invasiveness, reduced hemorrhage, reduced postoperative pain, earlier discharge and an improved cosmetic effect. Presently, a fair number of diagnostic and surgical procedures are performed using laparoscopy not only in adults, but also in pediatric patients (Hill et al. 2013; Kim et al. 2011; Ostlie and Ponsky 2014). However, to secure a clear surgical view, laparoscopy requires carbon dioxide (CO2) insufflation and pneumoperitoneum, which can cause adverse alterations in hemodynamic respiratory and cerebrovascular physiology (Bannister et al. 2003; Gainsburg 2012). Increased intracranial pressure (ICP) is regarded primarily as a cerebrovascular effect induced by CO2 pneumoperitoneum (Gainsburg 2012; Halverson et al. 1998).
Address correspondence to: Jiwon An, Department of Anesthesiology and Pain Medicine, Anesthesia and Pain Research Institute, Yonsei University College of Medicine, 50 Yonsei-ro, Seodaemun-gu, Seoul 120-752, Republic of Korea. E-mail: [email protected] 1241
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The present observational, single-center study investigated the extent of CO2 pneumoperitoneum-induced ICP elevation using ultrasonographic assessment of ONSD in children undergoing laparoscopic surgery. METHODS This study was approved by the institutional review board of Severance Hospital, Yonsei University Health System (4-2013-0090), and was registered with ClinicalTrials.gov (Ref. No. NCT01840267). Twentyfive children (boys and girls) aged less than 9 y and scheduled for an elective laparoscopic surgery by a single experienced surgeon at Severance Hospital, Yonsei University Health System, Seoul, Republic of Korea, were enrolled in this study. Written informed consent was obtained from the parents of all participants before enrollment. Children with a pre-existing neurologic or ophthalmic disease or a history of neurosurgery or ophthalmic surgery were excluded from this study. The participants were not pre-medicated. On arrival in the surgical suite, standard monitoring devices were employed immediately, including pulse oximetry, electrocardiography and non-invasive arterial blood pressure. General anesthesia was induced with intravenous propofol 2 mg/kg and fentanyl 1 mg/kg. To facilitate endotracheal intubation, rocuronium bromide 0.5 mg/kg was administered intravenously. After endotracheal intubation, positive pressure ventilation was initiated at a fixed tidal volume of 10 mL/kg and a controlled respiratory rate maintaining a 35–40 mm Hg end-tidal carbon dioxide (EtCO2) during the procedure. Anesthesia was maintained using 1–1.5 minimum alveolar concentration (MAC) of sevoflurane in a 50% oxygen/air mixture while monitoring the end-tidal sevoflurane concentration (EtSevo). A forced-air warming system (Bair-Hugger, Augustine-Medical, Eden Prairie, MN, USA) was used during the intra-operative period to preserve body temperature at 36.0–37.0 C. CO2 pneumoperitoneum was established using an intra-abdominal pressure (IAP) of 10 mm Hg. Two investigators (M.S.K. and J.Y.M.) with experience in more than 30 ocular ultrasounds measured the ONSD ultrasonographically, as described previously (Moretti and Pizzi 2011; Tayal et al. 2007). After a thick layer of sterile gel was applied over the closed upper eyelid, a linear 13- to 6-MHz probe (SonoSite MTurebo, SonoSite, Bothell, WA, USA) was placed lightly on the upper eyelid without exerting pressure on the eye. As illustrated in Figure 1, ONSD was assessed 3 mm behind the globe using an electronic digital caliper on the 2-D image. In total, four measurements were obtained in both the transverse and sagittal planes of the left and right optic nerves. The average of the four values
Fig. 1. Ultrasonographic assessment of optic nerve sheath diameter.
measured in both optic nerves was used as the final ONSD for statistical analysis. ONSD, heart rate, blood pressure, respiratory rate, peak inspiratory pressure, plateau pressure, static compliance, EtCO2 and EtSevo were measured at three discrete time points: 10 min after induction of general anesthesia (T0), 10 min after CO2 pneumoperitoneum at a 10 mm Hg intra-abdominal pressure (T1) and in the anesthetized state without CO2 pneumoperitoneum at the conclusion of the surgery (T2). In addition, we recorded the CO2 pneumoperitoneum time, surgical time and anesthetic time, as well as the volume of intravenous fluid administered. Previous clinical studies have proposed that the upper normal limit of ONSD is 5 mm in patients older than 4 y, 4.5 mm in patients aged 1 and 4 y and 4 mm in children aged less than 1 y (Moretti and Pizzi 2011). We counted the number of patients with ONSD above these upper normal limits based on patient age during CO2 pneumoperitoneum. The ONSD range and mean in normal children were previously reported as 2.1–4.3 and 3.08 6 0.36 mm, respectively (Ballantyne et al. 1999). Based on the known observer variation (60.2 mm) in ONSD (Ballantyne et al. 2002), 15 patients were needed to detect a 0.3-mm change in ONSD before and after induction of CO2 pneumoperitoneum at a two-tailed significance level of 5% and power of 90%. A total of 25 patients were included to improve the study power and compensate for patient dropouts. Statistical analyses were conducted using the Statistical Package for the Social Sciences Version 18.0 for Windows (SPSS, Chicago, IL, USA). All data are presented as the mean 6 standard deviation, median (range) or number (percent). A linear mixed model using an
Optic nerve sheath diameter during pediatric laparoscopy d J. Y. MIN et al.
Table 1. Patient demographics and intra-operative data (n 5 25) Age (mo) Age distribution #1 y 1–4 y .4 y Sex (M/F) Height (cm) Weight (kg) Body mass index (kg/m2) Pneumoperitoneum time (min) Operation time (min) Anesthesia time (min)
53.1 6 23.3* 2 (8) 8 (32) 15 (60) 12 (48)/13 (52) 104.0 6 17.8 17.6 6 5.6 15.9 6 1.7 31.7 6 10.5 50.8 6 11.3 75.2 6 13.8
* Results expressed as the mean 6 standard deviation or number (%).
unstructured type as covariance structure was applied for comparing ONSD values and other continuous data, which were investigated at each time point. Post hoc multiple comparisons using the Bonferroni correction were conducted if overall differences were identified between values at each time point. A p-value ,0.05 was deemed to indicate statistical significance. RESULTS Twenty-nine patients were initially screened from April to August 2013; two patients refused to participate and two patients did not meet the inclusion criteria because their histories revealed ocular surgery and ventri-
Fig. 2. Distribution of optic nerve sheath diameter (ONSD) values assessed at each time point. The box of the plot represents the middle 50% of the data, and the line inside the box represents the median value of the data set. The top and bottom of the box represent the third and first quartiles of the data set, and thus, the length of the box represents the interquartile range. The ends of the whiskers represent the minimum and maximum values of all the data, if values do not exist outside the whiskers, which extend to a maximum of 1.5 times the interquartile range. Any values that are not present between the whiskers should be plotted as outliers using a circle (n 5 25).
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Table 2. Measurements of hemodynamic and respiratory variables (n 5 25) T0
T1
T2
Heart rate 128.7 6 17.1* 133.9 6 18.5 126.2 6 18.6 (beats/min) Mean blood pressure 62.1 6 11.0 72.0 6 14.2y 66.2 6 10.9 (mm Hg) Respiratory rate 21.2 6 2.8 21.0 6 3.2 21.2 6 3.0 (breaths/min) y 14.5 6 3.8 20.3 6 5.0 15.5 6 4.3yz Peak inspiratory pressure (cm H2O) 12.8 6 3.4 17.8 6 4.4y Plateau pressure 13.6 6 3.6yz (cm H2O) 16.5 6 5.9 11.7 6 4.4y Static compliance 15.8 6 5.6y (mL/cm H2O) EtCO2 (mm Hg) 35.1 6 1.9 35.5 6 1.9 35.4 6 2.5 2.5 6 0.4y EtSevo (%) 2.4 6 0.3 2.8 6 0.3y EtCO2 5 end-tidal carbon dioxide; EtSevo 5 end-tidal sevoflurane concentration. * Results given as mean 6 standard deviation. y p , 0.05 compared with the value at T0. z p , 0.05 compared with the value at T1.
culoperitoneal shunting, respectively. Finally, 25 patients were included and completed the study protocol. Patient demographics and intra-operative findings are summarized in Table 1. Optic nerve sheath diameters were as follows: 4.3 6 0.3 (mean 6 standard deviation) mm at T0, 4.6 6 0.3 mm at T1 and 4.3 6 0.3 mm at T2. During CO2 pneumoperitoneum with an IAP of 10 mm Hg (T1), ONSD significantly increased compared with its value before the initiation of CO2 pneumoperitoneum (T0) (p , 0.05). Figure 2 illustrates the distribution of ONSD values assessed at each time point. During CO2 pneumoperitoneum, ONSD was higher than the upper normal limit in 7 patients, including 1 of 2 patients less than 1 y old, 5 of 8 patients between 1 and 4 y of age and 1 of 15 patients older than 4 y. Hemodynamic and respiratory parameters are summarized in Table 2. After establishment of CO2 pneumoperitoneum (T1), the mean blood pressure, peak inspiratory pressure and plateau pressure and EtSevo were significantly higher compared with before CO2 pneumoperitoneum (T0). EtCO2 was maintained without a significant difference compared with T1 with T0 under controlled ventilation. No neurologic complications were observed in the patients during the intra-operative or post-operative period. DISCUSSION This study focused on ICP changes during pediatric laparoscopy and revealed an increase of 7% in ONSD during CO2 pneumoperitoneum. Therefore, a corresponding ICP increase could also be assumed during
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pediatric laparoscopy; however, the impact of the elevated ICP is likely insignificant in children with normal intracranial compliance. Among the potential causes of elevated ICP during laparoscopic surgery, a PaCO2 increase during CO2 pneumoperitoneum can be considered preferentially (Gainsburg 2012; Halverson et al. 1998). The increase in PaCO2 is caused by absorption of CO2 from the peritoneal space and impaired gas exchange resulting from cephalad displacement of the diaphragm (Kim et al. 2010; Nguyen et al. 2004). There is a 1.8 mL/ 100 g/min change in cerebral blood flow for each 1-mm Hg change in the PaCO2, and therefore, the ICP increases with elevated cerebral blood flow during CO2 pneumoperitoneum (Gainsburg 2012; Grubb et al. 1974). EtCO2 monitoring has been routinely used to predict PaCO2 during general anesthesia. Our results indicate that the EtCO2 remained within the normocapnic range in all enrolled patients, and there were no significant differences between EtCO2 values measured before and after pneumoperitoneum. Hence, in this study, the impact of PaCO2 on the ICP elevation was presumably minimal at each time point. Several studies have found that the mechanical effects of CO2 pneumoperitoneum could directly induce an ICP elevation, independent of other etiologies such as PaCO2, PaO2, arterial pH and mean arterial pressure changes. The increased IAP during CO2 pneumoperitoneum physically interferes with cerebrospinal fluid drainage from the lumbar venous plexus, which can elevate ICP (Halverson et al. 1998; Josephs et al. 1994). Thus, the direct physical effect of pneumoperitoneum during pediatric laparoscopy can be primarily responsible for elevating ICP under the normal level of PaCO2. Volatile anesthetics are a well-known cause of cerebral vasodilation and the resultant increase in cerebral blood flow. This vasodilatory effect is caused by reduced vascular smooth muscle tension and predominates when anesthesia is maintained above 1.0 MAC (Drummond et al. 1986; Matta et al. 1999). The important consequence of this vasodilatory activity is an increased brain volume and the consequent increase in ICP (Fitch and McDowall 1971). In this study, the use of volatile anesthetics could be considered as a contributing factor in the rise of ICP because sevoflurane concentration during the surgical procedure under CO2 pneumoperitoneum was significantly higher than that before CO2 pneumoperitoneum. Despite this numerical statistical difference, sevoflurane was administered in the limited range of 1– 1.5 MAC to maintain general anesthesia in all enrolled patients, and thus, sevoflurane was not a meaningful confounding factor that could affect the difference in ICP values before and after pneumoperitoneum.
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The most reliable method for assessment of ICP is use of an intraventricular catheter; however, the risk of severe complications such as hemorrhage, as well as the absence of available neurosurgeons, limits the utility of this invasive method (Dubourg et al. 2011; Geeraerts et al. 2008). In particular, given its serious complications including cerebral hemorrhage, the use of such an invasive modality to measure ICP may place undue burden on patients undergoing other nonneurologic surgeries with the risk of increased ICP during the intra-operative period. Thus, an easy and non-invasive technique for assessing intra-operative ICP in these patients is required during these surgeries. Ultrasonographic assessment of ONSD has been known as a simple and non-invasive technique for monitoring and detecting increased ICP (Girisgin et al. 2007; Moretti and Pizzi 2011). A distensible subarachnoid space encircles the retrobulbar optic nerve, and accordingly, the optic nerve sheath has adequate elasticity permitting a detectable dilation in response to ICP elevations (Geeraerts et al. 2008; Hansen and Helmke 1997). Numerous clinical studies have ascertained the accuracy of ONSD assessment in detecting an elevated ICP in various clinical conditions including pediatric hydrocephalus, traumatic brain injury, pre-eclampsia and liver transplantation (Dubost et al. 2012; Helmke et al. 2000; McAuley et al. 2009; Moretti et al. 2009). To use this non-invasive tool as an indicator of increased ICP and guide for therapy, adequate cutoff or reference values of ONSD should be provided. In general, the upper normal limit of ONSD is 5 mm for patients aged .4 y, 4.5 mm between 1 and 4 y and 4 mm in children ,1 y (Ballantyne et al. 1999, 2002; Moretti and Pizzi 2011). However, cutoff values of ONSD corresponding specific values of ICP have been inconsistent in previous studies. In a study comparing ICP measured invasively with ONSD in adult patients receiving neurocritical care, an ONSD value of 5.8 mm indicated an ICP increase .20 mm Hg (Geeraerts et al. 2008). Moretti and Pizzi (2009) suggested that the ONSD threshold for detection of an ICP elevated .20 mm Hg was 5.2 mm in adult patients diagnosed with intracranial hemorrhage. In addition, there is a lack of information on cutoff values of ONSD predicting an elevated ICP in children (Helmke et al. 2000). In particular, a comparative study between ONSD values and ICP measured with an invasive tool has not been performed in pediatric patients (Moretti and Pizzi 2011). Given the available data, ONSD has limited predictive in predicting the exact ICP, and the assessment of ONSD may instead indicate the overall trend in ICP change. In this study, although ONSD values greater than the upper normal limits were observed in some cases, no neurologic complications occurred during the peri-operative period. Thus, the effect of this modest
Optic nerve sheath diameter during pediatric laparoscopy d J. Y. MIN et al.
increase in ICP may be limited in children with normal intracranial compliance. However, in pediatric patients with brain lesions such as tumors or hemorrhage, ICP may increase abruptly after the initiation of pneumoperitoneum. Josephs et al. (1994) reported that there was a significant elevation in ICP from 22.6 to 27.4 mm Hg when inducing pneumoperitoneum in an animal model having intracranial injuries. Therefore, special management regarding elevated ICP should be considered in pediatric patients with abnormal intracranial compliance undergoing laparoscopy. There are some limitations when interpreting our results. First, insufficient experience with ocular ultrasonography might be a possible limitation of this technique. However, Tayal et al. (2007) reported that 25 scans might be required before an inexperienced physician is capable of obtaining an adequate ONSD image, which is a quite steep learning curve. On the basis of these results, the investigator in the present study measured ONSD after sufficient practice with more than 25 scans. Second, variability in ONSD values assessed by ultrasonography should be taken into consideration. As described by Ballantyne et al. (2002), ultrasonographic ONSD assessment is easily learned and reproducible and the average inter-observer variation is 60.2 mm, which is similar to variability intrinsic to the ultrasound machine. We observed an approximately 0.3-mm difference in mean ONSD after inducing CO2 pneumoperitoneum, which is slightly larger than the reported inter-observer variation. Therefore, our results detailing the severity of ICP elevation should be validated with additional studies, although the laparoscopic ICP elevation can be fully predicted based on previous studies (Halverson et al. 1998; Gainsburg 2012). CONCLUSIONS We ascertained an increase in ONSD during CO2 pneumoperitoneum using ultrasonography in children undergoing laparoscopy. In addition, approximately 30% of the enrolled patients had ONSD values greater than the upper normal limit, and these children did not experience any neurologic complications in the perioperative period. Thus, ICP during CO2 pneumoperitoneum is not likely to adversely affect pediatric patients undergoing laparoscopy. The clinical implication of the elevated ICP during pediatric laparoscopy still needs to be confirmed through further research. REFERENCES Ballantyne J, Hollman AS, Hamilton R, Bradnam MS, Carachi R, Young DG, Dutton GN. Transorbital optic nerve sheath ultrasonography in normal children. Clin Radiol 1999;54:740–742.
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Ballantyne SA, O’Neill G, Hamilton R, Hollman AS. Observer variation in the sonographic measurement of optic nerve sheath diameter in normal adults. Eur J Ultrasound 2002;15:145–149. Bannister CF, Brosius KK, Wulkan M. The effect of insufflation pressure on pulmonary mechanics in infants during laparoscopic surgical procedures. Paediatr Anaesth 2003;13:785–789. Drummond JC, Todd MM, Scheller MS, Shapiro HM. A comparison of the direct cerebral vasodilating potencies of halothane and isoflurane in the New Zealand white rabbit. Anesthesiology 1986;65:462–467. Dubost C, Le Gouez A, Jouffroy V, Roger-Christoph S, Benhamou D, Mercier FJ, Geeraerts T. Optic nerve sheath diameter used as ultrasonographic assessment of the incidence of raised intracranial pressure in preeclampsia: A pilot study. Anesthesiology 2012;116: 1066–1071. Dubost C, Le Gouez A, Zetlaoui PJ, Benhamou D, Mercier FJ, Geeraerts T. Increase in optic nerve sheath diameter induced by epidural blood patch: A preliminary report. Br J Anaesth 2011; 107:627–630. Dubourg J, Javouhey E, Geeraerts T, Messerer M, Kassai B. Ultrasonography of optic nerve sheath diameter for detection of raised intracranial pressure: A systematic review and meta-analysis. Intensive Care Med 2011;37:1059–1068. Fitch W, McDowall DG. Effect of halothane on intracranial pressure gradients in the presence of intracranial space-occupying lesions. Br J Anaesth 1971;43:904–912. Gainsburg DM. Anesthetic concerns for robotic-assisted laparoscopic radical prostatectomy. Minerva Anestesiol 2012;78:596–604. Geeraerts T, Merceron S, Benhamou D, Vigue B, Duranteau J. Non-invasive assessment of intracranial pressure using ocular sonography in neurocritical care patients. Intensive Care Med 2008;34:2062–2067. Girisgin AS, Kalkan E, Kocak S, Cander B, Gul M, Semiz M. The role of optic nerve ultrasonography in the diagnosis of elevated intracranial pressure. Emerg Med J 2007;24:251–254. Grubb RL Jr, Raichle ME, Eichling JO, Ter-Pogossian MM. The effects of changes in PaCO2 on cerebral blood volume, blood flow, and vascular mean transit time. Stroke 1974;5:630–639. Halverson A, Buchanan R, Jacobs L, Shayani V, Hunt T, Riedel C, Sackier J. Evaluation of mechanism of increased intracranial pressure with insufflation. Surg Endosc 1998;12:266–269. Hansen HC, Helmke K. Validation of the optic nerve sheath response to changing cerebrospinal fluid pressure: Ultrasound findings during intrathecal infusion tests. J Neurosurg 1997;87:34–40. Helmke K, Burdelski M, Hansen HC. Detection and monitoring of intracranial pressure dysregulation in liver failure by ultrasound. Transplantation 2000;70:392–395. Hill SJ, Koontz CS, Langness SM, Wulkan ML. Laparoscopic versus open reduction of intussusception in children: Experience over a decade. J Laparoendosc Adv Surg Tech A 2013;23:166–169. Josephs LG, Este-McDonald JR, Birkett DH, Hirsch EF. Diagnostic laparoscopy increases intracranial pressure. J Trauma 1994;36:815–819. Kim JY, Shin CS, Kim HS, Jung WS, Kwak HJ. Positive end-expiratory pressure in pressure-controlled ventilation improves ventilatory and oxygenation parameters during laparoscopic cholecystectomy. Surg Endosc 2010;24:1099–1103. Kim JY, Shin CS, Lee KC, Chang YJ, Kwak HJ. Effect of pressureversus volume-controlled ventilation on the ventilatory and hemodynamic parameters during laparoscopic appendectomy in children: A prospective, randomized study. J Laparoendosc Adv Surg Tech A 2011;21:655–658. Matta BF, Heath KJ, Tipping K, Summors AC. Direct cerebral vasodilatory effects of sevoflurane and isoflurane. Anesthesiology 1999; 91:677–680. McAuley D, Paterson A, Sweeney L. Optic nerve sheath ultrasound in the assessment of paediatric hydrocephalus. Child’s Nerv Syst 2009;25:87–90. Moretti R, Pizzi B. Optic nerve ultrasound for detection of intracranial hypertension in intracranial hemorrhage patients: Confirmation of previous findings in a different patient population. J Neurosurg Anesthesiol 2009;21:16–20. Moretti R, Pizzi B. Ultrasonography of the optic nerve in neurocritically ill patients. Acta Anaesthesiol Scand 2011;55:644–652.
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Moretti R, Pizzi B, Cassini F, Vivaldi N. Reliability of optic nerve ultrasound for the evaluation of patients with spontaneous intracranial hemorrhage. Neurocrit Care 2009;11:406–410. Nguyen NT, Anderson JT, Budd M, Fleming NW, Ho HS, Jahr J, Stevens CM, Wolfe BM. Effects of pneumoperitoneum on intraoperative pulmonary mechanics and gas exchange during laparoscopic gastric bypass. Surg Endosc 2004;18:64–71.
Volume 41, Number 5, 2015 Ostlie DJ, Ponsky TA. Technical options of the laparoscopic pediatric inguinal hernia repair. J Laparoendosc Adv Surg Tech A 2014;24: 194–198. Tayal VS, Neulander M, Norton HJ, Foster T, Saunders T, Blaivas M. Emergency department sonographic measurement of optic nerve sheath diameter to detect findings of increased intracranial pressure in adult head injury patients. Ann Emerg Med 2007;49:508–514.
http://dx.doi.org/10.1016/j.ultrasmedbio.2015.01.009
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Original Contribution ULTRASONOGRAPHIC ASSESSMENT OF OPTIC NERVE SHEATH DIAMETER DURING PEDIATRIC LAPAROSCOPY JI YOUNG MIN,* JEONG-RIM LEE,* JUNG-TAK OH,y MIN-SOO KIM,* EUN-KYUNG JUN,* and JIWON AN* * Department of Anesthesiology and Pain Medicine, Anesthesia and Pain Research Institute, Yonsei University College of Medicine, Seoul, Republic of Korea; and y Department of Pediatric Surgery, Severance Children’s Hospital, Yonsei University College of Medicine, Seoul, Republic of Korea (Received 16 September 2014; revised 7 January 2015; in final form 16 January 2015)
Abstract—This study investigated the extent of the raised intracranial pressure resulting from carbon dioxide (CO2) pneumoperitoneum by ultrasonographically measuring optic nerve sheath diameter (ONSD) in children undergoing laparoscopic surgery. Twenty-five children aged less than 9 y (53.1 ± 23.3 mo, mean ± standard deviation) and scheduled for an elective laparoscopic surgery participated. ONSD was assessed using ocular ultrasonography 10 min after induction of anesthesia (T0), 10 min after induction of CO2 pneumoperitoneum at 10 mm Hg intra-abdominal pressure (T1) and in an anesthetized state without CO2 pneumoperitoneum at the conclusion of the surgery (T2). During CO2 pneumoperitoneum, ONSD increased significantly compared with ONSD after anesthesia induction (T0: 4.3 ± 0.3 mm, T1: 4.6 ± 0.3 mm, p , 0.05). In all enrolled patients, any neurologic complications were not observed during the intra-operative or post-operative period. In children undergoing laparoscopic surgery, an increase in ONSD was ascertained during CO2 pneumoperitoneum, and thus the corresponding increase in intracranial pressure could be predicted. (E-mail: [email protected]) Ó 2015 World Federation for Ultrasound in Medicine & Biology. Key Words: Ultrasound, Optic nerve sheath, Pediatric laparoscopy.
Although the insertion of an intracranial device is the most accurate method to measure ICP, performing this invasive method during laparoscopic surgery is virtually impossible because of neurosurgical unavailability and concerns about severe complications such as infection, hemorrhage and equipment malfunction (Geeraerts et al. 2008). Thus, the severity and tolerability of increased ICP caused by CO2 pneumoperitoneum are still unknown, especially in pediatric laparoscopy. Measurement of optic nerve sheath diameter (ONSD) using ocular ultrasonography is a simple, non-invasive and reproducible technique for assessing ICP. Previous studies have reported the reliability of ONSD for diagnosing and assessing an increased ICP in various clinical situations including traumatic brain injury, stroke, post-dural puncture headache and pre-eclampsia (Dubost et al. 2011, 2012; Dubourg et al. 2011; Geeraerts et al. 2008). Hence, it could be hypothesized that the extent of the increased ICP during pediatric laparoscopy could be confirmed without serious complications by monitoring ONSD using ocular ultrasonography instead of direct and invasive ICP measurement. To date, there have been no studies on the evaluation of ONSD during pediatric laparoscopy.
INTRODUCTION Laparoscopic surgery is a rapidly growing alternative technique to conventional open surgery. Its advantages include minimal invasiveness, reduced hemorrhage, reduced postoperative pain, earlier discharge and an improved cosmetic effect. Presently, a fair number of diagnostic and surgical procedures are performed using laparoscopy not only in adults, but also in pediatric patients (Hill et al. 2013; Kim et al. 2011; Ostlie and Ponsky 2014). However, to secure a clear surgical view, laparoscopy requires carbon dioxide (CO2) insufflation and pneumoperitoneum, which can cause adverse alterations in hemodynamic respiratory and cerebrovascular physiology (Bannister et al. 2003; Gainsburg 2012). Increased intracranial pressure (ICP) is regarded primarily as a cerebrovascular effect induced by CO2 pneumoperitoneum (Gainsburg 2012; Halverson et al. 1998).
Address correspondence to: Jiwon An, Department of Anesthesiology and Pain Medicine, Anesthesia and Pain Research Institute, Yonsei University College of Medicine, 50 Yonsei-ro, Seodaemun-gu, Seoul 120-752, Republic of Korea. E-mail: [email protected] 1241
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The present observational, single-center study investigated the extent of CO2 pneumoperitoneum-induced ICP elevation using ultrasonographic assessment of ONSD in children undergoing laparoscopic surgery. METHODS This study was approved by the institutional review board of Severance Hospital, Yonsei University Health System (4-2013-0090), and was registered with ClinicalTrials.gov (Ref. No. NCT01840267). Twentyfive children (boys and girls) aged less than 9 y and scheduled for an elective laparoscopic surgery by a single experienced surgeon at Severance Hospital, Yonsei University Health System, Seoul, Republic of Korea, were enrolled in this study. Written informed consent was obtained from the parents of all participants before enrollment. Children with a pre-existing neurologic or ophthalmic disease or a history of neurosurgery or ophthalmic surgery were excluded from this study. The participants were not pre-medicated. On arrival in the surgical suite, standard monitoring devices were employed immediately, including pulse oximetry, electrocardiography and non-invasive arterial blood pressure. General anesthesia was induced with intravenous propofol 2 mg/kg and fentanyl 1 mg/kg. To facilitate endotracheal intubation, rocuronium bromide 0.5 mg/kg was administered intravenously. After endotracheal intubation, positive pressure ventilation was initiated at a fixed tidal volume of 10 mL/kg and a controlled respiratory rate maintaining a 35–40 mm Hg end-tidal carbon dioxide (EtCO2) during the procedure. Anesthesia was maintained using 1–1.5 minimum alveolar concentration (MAC) of sevoflurane in a 50% oxygen/air mixture while monitoring the end-tidal sevoflurane concentration (EtSevo). A forced-air warming system (Bair-Hugger, Augustine-Medical, Eden Prairie, MN, USA) was used during the intra-operative period to preserve body temperature at 36.0–37.0 C. CO2 pneumoperitoneum was established using an intra-abdominal pressure (IAP) of 10 mm Hg. Two investigators (M.S.K. and J.Y.M.) with experience in more than 30 ocular ultrasounds measured the ONSD ultrasonographically, as described previously (Moretti and Pizzi 2011; Tayal et al. 2007). After a thick layer of sterile gel was applied over the closed upper eyelid, a linear 13- to 6-MHz probe (SonoSite MTurebo, SonoSite, Bothell, WA, USA) was placed lightly on the upper eyelid without exerting pressure on the eye. As illustrated in Figure 1, ONSD was assessed 3 mm behind the globe using an electronic digital caliper on the 2-D image. In total, four measurements were obtained in both the transverse and sagittal planes of the left and right optic nerves. The average of the four values
Fig. 1. Ultrasonographic assessment of optic nerve sheath diameter.
measured in both optic nerves was used as the final ONSD for statistical analysis. ONSD, heart rate, blood pressure, respiratory rate, peak inspiratory pressure, plateau pressure, static compliance, EtCO2 and EtSevo were measured at three discrete time points: 10 min after induction of general anesthesia (T0), 10 min after CO2 pneumoperitoneum at a 10 mm Hg intra-abdominal pressure (T1) and in the anesthetized state without CO2 pneumoperitoneum at the conclusion of the surgery (T2). In addition, we recorded the CO2 pneumoperitoneum time, surgical time and anesthetic time, as well as the volume of intravenous fluid administered. Previous clinical studies have proposed that the upper normal limit of ONSD is 5 mm in patients older than 4 y, 4.5 mm in patients aged 1 and 4 y and 4 mm in children aged less than 1 y (Moretti and Pizzi 2011). We counted the number of patients with ONSD above these upper normal limits based on patient age during CO2 pneumoperitoneum. The ONSD range and mean in normal children were previously reported as 2.1–4.3 and 3.08 6 0.36 mm, respectively (Ballantyne et al. 1999). Based on the known observer variation (60.2 mm) in ONSD (Ballantyne et al. 2002), 15 patients were needed to detect a 0.3-mm change in ONSD before and after induction of CO2 pneumoperitoneum at a two-tailed significance level of 5% and power of 90%. A total of 25 patients were included to improve the study power and compensate for patient dropouts. Statistical analyses were conducted using the Statistical Package for the Social Sciences Version 18.0 for Windows (SPSS, Chicago, IL, USA). All data are presented as the mean 6 standard deviation, median (range) or number (percent). A linear mixed model using an
Optic nerve sheath diameter during pediatric laparoscopy d J. Y. MIN et al.
Table 1. Patient demographics and intra-operative data (n 5 25) Age (mo) Age distribution #1 y 1–4 y .4 y Sex (M/F) Height (cm) Weight (kg) Body mass index (kg/m2) Pneumoperitoneum time (min) Operation time (min) Anesthesia time (min)
53.1 6 23.3* 2 (8) 8 (32) 15 (60) 12 (48)/13 (52) 104.0 6 17.8 17.6 6 5.6 15.9 6 1.7 31.7 6 10.5 50.8 6 11.3 75.2 6 13.8
* Results expressed as the mean 6 standard deviation or number (%).
unstructured type as covariance structure was applied for comparing ONSD values and other continuous data, which were investigated at each time point. Post hoc multiple comparisons using the Bonferroni correction were conducted if overall differences were identified between values at each time point. A p-value ,0.05 was deemed to indicate statistical significance. RESULTS Twenty-nine patients were initially screened from April to August 2013; two patients refused to participate and two patients did not meet the inclusion criteria because their histories revealed ocular surgery and ventri-
Fig. 2. Distribution of optic nerve sheath diameter (ONSD) values assessed at each time point. The box of the plot represents the middle 50% of the data, and the line inside the box represents the median value of the data set. The top and bottom of the box represent the third and first quartiles of the data set, and thus, the length of the box represents the interquartile range. The ends of the whiskers represent the minimum and maximum values of all the data, if values do not exist outside the whiskers, which extend to a maximum of 1.5 times the interquartile range. Any values that are not present between the whiskers should be plotted as outliers using a circle (n 5 25).
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Table 2. Measurements of hemodynamic and respiratory variables (n 5 25) T0
T1
T2
Heart rate 128.7 6 17.1* 133.9 6 18.5 126.2 6 18.6 (beats/min) Mean blood pressure 62.1 6 11.0 72.0 6 14.2y 66.2 6 10.9 (mm Hg) Respiratory rate 21.2 6 2.8 21.0 6 3.2 21.2 6 3.0 (breaths/min) y 14.5 6 3.8 20.3 6 5.0 15.5 6 4.3yz Peak inspiratory pressure (cm H2O) 12.8 6 3.4 17.8 6 4.4y Plateau pressure 13.6 6 3.6yz (cm H2O) 16.5 6 5.9 11.7 6 4.4y Static compliance 15.8 6 5.6y (mL/cm H2O) EtCO2 (mm Hg) 35.1 6 1.9 35.5 6 1.9 35.4 6 2.5 2.5 6 0.4y EtSevo (%) 2.4 6 0.3 2.8 6 0.3y EtCO2 5 end-tidal carbon dioxide; EtSevo 5 end-tidal sevoflurane concentration. * Results given as mean 6 standard deviation. y p , 0.05 compared with the value at T0. z p , 0.05 compared with the value at T1.
culoperitoneal shunting, respectively. Finally, 25 patients were included and completed the study protocol. Patient demographics and intra-operative findings are summarized in Table 1. Optic nerve sheath diameters were as follows: 4.3 6 0.3 (mean 6 standard deviation) mm at T0, 4.6 6 0.3 mm at T1 and 4.3 6 0.3 mm at T2. During CO2 pneumoperitoneum with an IAP of 10 mm Hg (T1), ONSD significantly increased compared with its value before the initiation of CO2 pneumoperitoneum (T0) (p , 0.05). Figure 2 illustrates the distribution of ONSD values assessed at each time point. During CO2 pneumoperitoneum, ONSD was higher than the upper normal limit in 7 patients, including 1 of 2 patients less than 1 y old, 5 of 8 patients between 1 and 4 y of age and 1 of 15 patients older than 4 y. Hemodynamic and respiratory parameters are summarized in Table 2. After establishment of CO2 pneumoperitoneum (T1), the mean blood pressure, peak inspiratory pressure and plateau pressure and EtSevo were significantly higher compared with before CO2 pneumoperitoneum (T0). EtCO2 was maintained without a significant difference compared with T1 with T0 under controlled ventilation. No neurologic complications were observed in the patients during the intra-operative or post-operative period. DISCUSSION This study focused on ICP changes during pediatric laparoscopy and revealed an increase of 7% in ONSD during CO2 pneumoperitoneum. Therefore, a corresponding ICP increase could also be assumed during
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pediatric laparoscopy; however, the impact of the elevated ICP is likely insignificant in children with normal intracranial compliance. Among the potential causes of elevated ICP during laparoscopic surgery, a PaCO2 increase during CO2 pneumoperitoneum can be considered preferentially (Gainsburg 2012; Halverson et al. 1998). The increase in PaCO2 is caused by absorption of CO2 from the peritoneal space and impaired gas exchange resulting from cephalad displacement of the diaphragm (Kim et al. 2010; Nguyen et al. 2004). There is a 1.8 mL/ 100 g/min change in cerebral blood flow for each 1-mm Hg change in the PaCO2, and therefore, the ICP increases with elevated cerebral blood flow during CO2 pneumoperitoneum (Gainsburg 2012; Grubb et al. 1974). EtCO2 monitoring has been routinely used to predict PaCO2 during general anesthesia. Our results indicate that the EtCO2 remained within the normocapnic range in all enrolled patients, and there were no significant differences between EtCO2 values measured before and after pneumoperitoneum. Hence, in this study, the impact of PaCO2 on the ICP elevation was presumably minimal at each time point. Several studies have found that the mechanical effects of CO2 pneumoperitoneum could directly induce an ICP elevation, independent of other etiologies such as PaCO2, PaO2, arterial pH and mean arterial pressure changes. The increased IAP during CO2 pneumoperitoneum physically interferes with cerebrospinal fluid drainage from the lumbar venous plexus, which can elevate ICP (Halverson et al. 1998; Josephs et al. 1994). Thus, the direct physical effect of pneumoperitoneum during pediatric laparoscopy can be primarily responsible for elevating ICP under the normal level of PaCO2. Volatile anesthetics are a well-known cause of cerebral vasodilation and the resultant increase in cerebral blood flow. This vasodilatory effect is caused by reduced vascular smooth muscle tension and predominates when anesthesia is maintained above 1.0 MAC (Drummond et al. 1986; Matta et al. 1999). The important consequence of this vasodilatory activity is an increased brain volume and the consequent increase in ICP (Fitch and McDowall 1971). In this study, the use of volatile anesthetics could be considered as a contributing factor in the rise of ICP because sevoflurane concentration during the surgical procedure under CO2 pneumoperitoneum was significantly higher than that before CO2 pneumoperitoneum. Despite this numerical statistical difference, sevoflurane was administered in the limited range of 1– 1.5 MAC to maintain general anesthesia in all enrolled patients, and thus, sevoflurane was not a meaningful confounding factor that could affect the difference in ICP values before and after pneumoperitoneum.
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The most reliable method for assessment of ICP is use of an intraventricular catheter; however, the risk of severe complications such as hemorrhage, as well as the absence of available neurosurgeons, limits the utility of this invasive method (Dubourg et al. 2011; Geeraerts et al. 2008). In particular, given its serious complications including cerebral hemorrhage, the use of such an invasive modality to measure ICP may place undue burden on patients undergoing other nonneurologic surgeries with the risk of increased ICP during the intra-operative period. Thus, an easy and non-invasive technique for assessing intra-operative ICP in these patients is required during these surgeries. Ultrasonographic assessment of ONSD has been known as a simple and non-invasive technique for monitoring and detecting increased ICP (Girisgin et al. 2007; Moretti and Pizzi 2011). A distensible subarachnoid space encircles the retrobulbar optic nerve, and accordingly, the optic nerve sheath has adequate elasticity permitting a detectable dilation in response to ICP elevations (Geeraerts et al. 2008; Hansen and Helmke 1997). Numerous clinical studies have ascertained the accuracy of ONSD assessment in detecting an elevated ICP in various clinical conditions including pediatric hydrocephalus, traumatic brain injury, pre-eclampsia and liver transplantation (Dubost et al. 2012; Helmke et al. 2000; McAuley et al. 2009; Moretti et al. 2009). To use this non-invasive tool as an indicator of increased ICP and guide for therapy, adequate cutoff or reference values of ONSD should be provided. In general, the upper normal limit of ONSD is 5 mm for patients aged .4 y, 4.5 mm between 1 and 4 y and 4 mm in children ,1 y (Ballantyne et al. 1999, 2002; Moretti and Pizzi 2011). However, cutoff values of ONSD corresponding specific values of ICP have been inconsistent in previous studies. In a study comparing ICP measured invasively with ONSD in adult patients receiving neurocritical care, an ONSD value of 5.8 mm indicated an ICP increase .20 mm Hg (Geeraerts et al. 2008). Moretti and Pizzi (2009) suggested that the ONSD threshold for detection of an ICP elevated .20 mm Hg was 5.2 mm in adult patients diagnosed with intracranial hemorrhage. In addition, there is a lack of information on cutoff values of ONSD predicting an elevated ICP in children (Helmke et al. 2000). In particular, a comparative study between ONSD values and ICP measured with an invasive tool has not been performed in pediatric patients (Moretti and Pizzi 2011). Given the available data, ONSD has limited predictive in predicting the exact ICP, and the assessment of ONSD may instead indicate the overall trend in ICP change. In this study, although ONSD values greater than the upper normal limits were observed in some cases, no neurologic complications occurred during the peri-operative period. Thus, the effect of this modest
Optic nerve sheath diameter during pediatric laparoscopy d J. Y. MIN et al.
increase in ICP may be limited in children with normal intracranial compliance. However, in pediatric patients with brain lesions such as tumors or hemorrhage, ICP may increase abruptly after the initiation of pneumoperitoneum. Josephs et al. (1994) reported that there was a significant elevation in ICP from 22.6 to 27.4 mm Hg when inducing pneumoperitoneum in an animal model having intracranial injuries. Therefore, special management regarding elevated ICP should be considered in pediatric patients with abnormal intracranial compliance undergoing laparoscopy. There are some limitations when interpreting our results. First, insufficient experience with ocular ultrasonography might be a possible limitation of this technique. However, Tayal et al. (2007) reported that 25 scans might be required before an inexperienced physician is capable of obtaining an adequate ONSD image, which is a quite steep learning curve. On the basis of these results, the investigator in the present study measured ONSD after sufficient practice with more than 25 scans. Second, variability in ONSD values assessed by ultrasonography should be taken into consideration. As described by Ballantyne et al. (2002), ultrasonographic ONSD assessment is easily learned and reproducible and the average inter-observer variation is 60.2 mm, which is similar to variability intrinsic to the ultrasound machine. We observed an approximately 0.3-mm difference in mean ONSD after inducing CO2 pneumoperitoneum, which is slightly larger than the reported inter-observer variation. Therefore, our results detailing the severity of ICP elevation should be validated with additional studies, although the laparoscopic ICP elevation can be fully predicted based on previous studies (Halverson et al. 1998; Gainsburg 2012). CONCLUSIONS We ascertained an increase in ONSD during CO2 pneumoperitoneum using ultrasonography in children undergoing laparoscopy. In addition, approximately 30% of the enrolled patients had ONSD values greater than the upper normal limit, and these children did not experience any neurologic complications in the perioperative period. Thus, ICP during CO2 pneumoperitoneum is not likely to adversely affect pediatric patients undergoing laparoscopy. The clinical implication of the elevated ICP during pediatric laparoscopy still needs to be confirmed through further research. REFERENCES Ballantyne J, Hollman AS, Hamilton R, Bradnam MS, Carachi R, Young DG, Dutton GN. Transorbital optic nerve sheath ultrasonography in normal children. Clin Radiol 1999;54:740–742.
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Ballantyne SA, O’Neill G, Hamilton R, Hollman AS. Observer variation in the sonographic measurement of optic nerve sheath diameter in normal adults. Eur J Ultrasound 2002;15:145–149. Bannister CF, Brosius KK, Wulkan M. The effect of insufflation pressure on pulmonary mechanics in infants during laparoscopic surgical procedures. Paediatr Anaesth 2003;13:785–789. Drummond JC, Todd MM, Scheller MS, Shapiro HM. A comparison of the direct cerebral vasodilating potencies of halothane and isoflurane in the New Zealand white rabbit. Anesthesiology 1986;65:462–467. Dubost C, Le Gouez A, Jouffroy V, Roger-Christoph S, Benhamou D, Mercier FJ, Geeraerts T. Optic nerve sheath diameter used as ultrasonographic assessment of the incidence of raised intracranial pressure in preeclampsia: A pilot study. Anesthesiology 2012;116: 1066–1071. Dubost C, Le Gouez A, Zetlaoui PJ, Benhamou D, Mercier FJ, Geeraerts T. Increase in optic nerve sheath diameter induced by epidural blood patch: A preliminary report. Br J Anaesth 2011; 107:627–630. Dubourg J, Javouhey E, Geeraerts T, Messerer M, Kassai B. Ultrasonography of optic nerve sheath diameter for detection of raised intracranial pressure: A systematic review and meta-analysis. Intensive Care Med 2011;37:1059–1068. Fitch W, McDowall DG. Effect of halothane on intracranial pressure gradients in the presence of intracranial space-occupying lesions. Br J Anaesth 1971;43:904–912. Gainsburg DM. Anesthetic concerns for robotic-assisted laparoscopic radical prostatectomy. Minerva Anestesiol 2012;78:596–604. Geeraerts T, Merceron S, Benhamou D, Vigue B, Duranteau J. Non-invasive assessment of intracranial pressure using ocular sonography in neurocritical care patients. Intensive Care Med 2008;34:2062–2067. Girisgin AS, Kalkan E, Kocak S, Cander B, Gul M, Semiz M. The role of optic nerve ultrasonography in the diagnosis of elevated intracranial pressure. Emerg Med J 2007;24:251–254. Grubb RL Jr, Raichle ME, Eichling JO, Ter-Pogossian MM. The effects of changes in PaCO2 on cerebral blood volume, blood flow, and vascular mean transit time. Stroke 1974;5:630–639. Halverson A, Buchanan R, Jacobs L, Shayani V, Hunt T, Riedel C, Sackier J. Evaluation of mechanism of increased intracranial pressure with insufflation. Surg Endosc 1998;12:266–269. Hansen HC, Helmke K. Validation of the optic nerve sheath response to changing cerebrospinal fluid pressure: Ultrasound findings during intrathecal infusion tests. J Neurosurg 1997;87:34–40. Helmke K, Burdelski M, Hansen HC. Detection and monitoring of intracranial pressure dysregulation in liver failure by ultrasound. Transplantation 2000;70:392–395. Hill SJ, Koontz CS, Langness SM, Wulkan ML. Laparoscopic versus open reduction of intussusception in children: Experience over a decade. J Laparoendosc Adv Surg Tech A 2013;23:166–169. Josephs LG, Este-McDonald JR, Birkett DH, Hirsch EF. Diagnostic laparoscopy increases intracranial pressure. J Trauma 1994;36:815–819. Kim JY, Shin CS, Kim HS, Jung WS, Kwak HJ. Positive end-expiratory pressure in pressure-controlled ventilation improves ventilatory and oxygenation parameters during laparoscopic cholecystectomy. Surg Endosc 2010;24:1099–1103. Kim JY, Shin CS, Lee KC, Chang YJ, Kwak HJ. Effect of pressureversus volume-controlled ventilation on the ventilatory and hemodynamic parameters during laparoscopic appendectomy in children: A prospective, randomized study. J Laparoendosc Adv Surg Tech A 2011;21:655–658. Matta BF, Heath KJ, Tipping K, Summors AC. Direct cerebral vasodilatory effects of sevoflurane and isoflurane. Anesthesiology 1999; 91:677–680. McAuley D, Paterson A, Sweeney L. Optic nerve sheath ultrasound in the assessment of paediatric hydrocephalus. Child’s Nerv Syst 2009;25:87–90. Moretti R, Pizzi B. Optic nerve ultrasound for detection of intracranial hypertension in intracranial hemorrhage patients: Confirmation of previous findings in a different patient population. J Neurosurg Anesthesiol 2009;21:16–20. Moretti R, Pizzi B. Ultrasonography of the optic nerve in neurocritically ill patients. Acta Anaesthesiol Scand 2011;55:644–652.
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Volume 41, Number 5, 2015 Ostlie DJ, Ponsky TA. Technical options of the laparoscopic pediatric inguinal hernia repair. J Laparoendosc Adv Surg Tech A 2014;24: 194–198. Tayal VS, Neulander M, Norton HJ, Foster T, Saunders T, Blaivas M. Emergency department sonographic measurement of optic nerve sheath diameter to detect findings of increased intracranial pressure in adult head injury patients. Ann Emerg Med 2007;49:508–514.
