Surg Endosc DOI 10.1007/s00464-014-3892-0

and Other Interventional Techniques

Safety of carbon dioxide insufflation during gastric endoscopic submucosal dissection in patients with pulmonary dysfunction under conscious sedation Jun Takada • Hiroshi Araki • Fumito Onogi • Takayuki Nakanishi • Masaya Kubota • Takashi Ibuka Masahito Shimizu • Hisataka Moriwaki



Received: 28 April 2014 / Accepted: 8 September 2014 Ó Springer Science+Business Media New York 2014

Abstract Background Carbon dioxide (CO2) insufflation is effective for gastric endoscopic submucosal dissection (ESD). However, its safety is unknown in patients with pulmonary dysfunction. This study aimed to investigate the safety of CO2 insufflation during gastric ESD in patients with pulmonary dysfunction under conscious sedation. Methods We analyzed 322 consecutive patients undergoing ESD using CO2 insufflation (1.4 L/min) for gastric lesions. Pulmonary dysfunction was defined as a forced expiratory volume in 1.0 s/forced vital capacity (FEV1.0%) \70 % or vital capacity \80 %. Transcutaneous partial pressure of CO2 (PtcCO2) was recorded before, during, and after ESD. Results In total, 127 patients (39 %) had pulmonary dysfunction. There were no significant differences in baseline PtcCO2 before ESD, peak PtcCO2 during ESD, and median PtcCO2 after ESD between the pulmonary dysfunction group and normal group. There was a significant correlation between PtcCO2 elevation from baseline and ESD procedure time (r = 0.22, P \ 0.05) only in the pulmonary dysfunction group. In patients with FEV1.0% \60 %, the correlation was much stronger (r = 0.39, P \ 0.05). Neither the complication incidences nor the hospital stay differed between the two groups. CO2 narcosis or gas embolism was not reported in either group.

J. Takada  H. Araki (&)  F. Onogi  T. Nakanishi  M. Kubota  T. Ibuka  M. Shimizu  H. Moriwaki Department of Gastroenterology/Internal Medicine, Gifu University Graduate School of Medicine, 1-1 Yanagido, Gifu 501-1194, Japan e-mail: [email protected] J. Takada e-mail: [email protected]

Conclusions CO2 insufflation during gastric ESD in patients with pulmonary dysfunction under conscious sedation is safe with regard to complication risk and hospital stay. However, in patients with severe obstructive lung disease, especially in those with FEV1.0% \60 %, longer procedure time may induce CO2 retention, thus requiring CO2 monitoring. Keywords Carbon dioxide  Endoscopic submucosal dissection  Pulmonary dysfunction  Transcutaneous partial pressure of CO2  Gastric cancer

Endoscopic submucosal dissection (ESD) for gastric neoplasms provides high clinical benefits by enabling en bloc resection of even an extensive superficial lesion [1–8]. On the other hand, gastric ESD requires a longer procedure time because of its technical difficulty, and thus, a greater amount of gas insufflation is required to maintain adequate visualization. Air has been most commonly used for insufflation, but the amount of residual gas after ESD is large. Residual gas in the gastrointestinal tract can induce post-ESD pain or discomfort. In addition, it possibly leads to rare but life-threatening complications such as air embolism and tension pneumothorax [9–15]. It is well known that carbon dioxide (CO2) is absorbed faster in the body than air and is also rapidly excreted through the lungs, except in cases of pulmonary dysfunction. Therefore, CO2 insufflation is expected to reduce patient pain and abdominal discomfort associated with endoscopic examination and therapy [16–22]. CO2 insufflation is also supposed to minimize ESD-related complications such as perforation or vascular injury. The safety and efficacy of CO2 insufflation during ESD for lesions of the esophagus, stomach, and colorectum have been

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demonstrated in randomized controlled trials and prospective studies [23–26]. However, these studies excluded patients with pulmonary dysfunction, and the possible effect of CO2 insufflation on these patients has not been addressed yet. In clinical practice, many ESD patients are of advanced age, and pulmonary dysfunction prevails in these patients. Considering its efficacy, if the safety is confirmed, CO2 insufflation could be used during ESD in patients with pulmonary dysfunction under conscious sedation. Our hypothesis in this study is that CO2 insufflation during gastric ESD in such patients is safe on the basis of both the incidence of complication and blood gas analysis. Intra-arterial CO2 monitoring is considered necessary to maintain safety during CO2 insufflation. However, direct measurement of the partial pressure of CO2 in arterial blood (PaCO2) is an invasive procedure and, therefore, impractical to use as a continuously monitoring system for ESD. Recently, transcutaneous partial pressure of CO2 (PtcCO2) is considered to be one of the most reliable parameters for estimating PaCO2 in sedated patients [27, 28]. PtcCO2 is correlated with PaCO2 better than the partial pressure of end-tidal CO2 (PetCO2) [27, 29], suggesting that this noninvasive monitoring system may be useful for evaluating the safety of CO2 insufflation. The aim of this study was to evaluate the safety and efficacy of CO2 insufflation during ESD for gastric neoplasms in patients with pulmonary dysfunction. To achieve this purpose, we measured the levels of PtcCO2 during gastric ESD in patients under conscious sedation and investigated the utility of the PtcCO2 monitoring system for maintaining safety during CO2 insufflation in these patients.

Patients and methods Patients and respiratory function test A series of 322 patients who underwent ESD for gastric lesions at Gifu University Hospital in Japan between January 2010 and December 2012 were enrolled in this study. All ESDs were conducted using CO2 insufflation under conscious sedation. All patients provided written informed consent before enrollment. The study protocol was approved by the institutional ethics committee of Gifu University Hospital, and the study has, therefore, been performed in accordance with the ethical standards laid down in the 1964 Declaration of Helsinki and its later amendments. Respiratory function was examined before ESD. Pulmonary dysfunction was defined as a forced expiratory volume in 1.0 s/forced vital capacity (FEV1.0%) \70 % or vital capacity (%VC) \80 % [30, 31].

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Examination schedule for study events before and after ESD ESD was conducted in the afternoon on the day of admission. On the second hospital day, blood examinations, esophagogastroduodenoscopy, and computed tomography (CT) of the chest and abdomen were performed. Blood examinations for leukocyte count and C-reactive protein (CRP) were repeated on the third hospital day. Axillary temperature, which is sanitarily sound and simple compared to other methods for measurement of body temperature, was checked at 1 h after ESD and at 06:00, 14:00, and 20:00 daily thereafter. ESD procedure and conscious sedation method The standard ESD procedure was carried out using a gastroscope with a single working channel and water jet function (GIF-Q260 J; Olympus Optical Co., Tokyo, Japan) and a cap attachment (D-201-11804; Olympus). The gastric lesion was resected using either the Dual-KnifeTM (KD-630L; Olympus) or IT2 KnifeTM (KD-611L; Olympus), depending on the location of the lesion. Highmolecular-weight hyaluronic acid solution containing epinephrine was injected into the submucosal layer to lift-up the lesion. Incision of the mucosal layer outside the marking dots and subsequent direct dissection of the submucosal layer were carried out with the Dual-Knife and IT2-Knife. Patients received diazepam for conscious sedation and pentazocine for analgesia. At the start of the ESD procedure, 5–10 mg of diazepam and 7.5–15 mg of pentazocine were injected intravenously for induction of anesthesia and analgesia, with an additional 5 mg of diazepam or 7.5 mg of pentazocine administered repeatedly as necessary. When the combination of diazepam and pentazocine could not achieve conscious sedation, intravenous midazolam was administered. Oxygen was administered nasally at 2.0 L/ min during ESD, and the flow volume was adjusted by monitoring transcutaneous oxygen saturation (SpO2). CO2 insufflation and transcutaneous gas analysis In this study, CO2 was delivered using a CO2 regulation unit (OLYMPUS UCRTM; Olympus). The TOSCA measurement system and TOSCA 500 monitor (Linde Medical Sensors, Basel, Switzerland) were used to measure the PtcCO2 noninvasively and continuously. We used the lowflow gas tube (MAJ-1742; Olympus) of the UCR for CO2 insufflation, which was set at a constant rate of 1.4 L/min, for all patients. The TOSCA measurement system and TOSCA 500 monitor measure PtcCO2 using an earlobe sensor attached by a low pressure clip. We used a default

Surg Endosc

temperature setting of 42 °C for the sensor and recalibrated the system before each ESD. The main outcome measurements were PtcCO2 level, correlation between PtcCO2 and operation time, and complications. PtcCO2 was recorded every fifteen minutes before, during, and after each ESD procedure. Curative resection was defined based on the Japanese classification of gastric cancer by the Japanese Gastric Cancer Association [32].

Definitions of outcome parameters and complications Operation time was measured from the start of circumferential marking to resection completion. A diagnosis of perforation was made by direct endoscopic observation during ESD or by the presence of free air on a plain chest radiography. Evidence of aspiration pneumonia was determined by the appearance of an obvious pneumonia shadow on a plain chest CT 1 day after ESD. Bleeding was defined as clinical evidence of bleeding after ESD, as shown by hematemesis or melena that required endoscopic treatment. Mallory–Weiss syndrome was defined as a mucosal tear or laceration near the esophagogastric junction with active bleeding, either spurting or oozing during ESD.

Statistical analysis

Table 1 Patients and examination characteristics Pulmonary dysfunction group

Normal group

P value

Patients

127 (39)

195 (61)

Age (years)

73 (52–89)

69 (34–90)

\0.001

Sex (male/female) FEV1.0%

104/23 62 (37–98)

143/52 76 (70–96)

0.081 \0.001

%VC

102 (43–146)

111 (80–181) \0.001

Location of gastric lesion (upper/middle/lower/ remnant)

16/56/51/4

42/70/77/6

NS

En bloc resection

127 (100)

195 (100)

NS

Histopathologic type (tub1/tub2/pap/por/sig/ adenoma/cartinoid/ hyperplastic polyp)

70/18/8/2/0/ 28/0/1

101/29/11/3/ 2/46/1/2

NS

Histological depth (M/SM1/SM2) Histopathologically curative resection

114/6/7

180/5/10

NS

116 (91)

175 (90)

NS

Tumor size (mm)

19 (3–75)

20 (3–77)

NS

Resection size (mm)

44 (12–100)

45 (18–100)

NS

Procedure time (min)

57 (10–233)

64 (12–301)

NS

Dose of diazepam (mg)

18 (5–40)

18 (5–30)

NS

Dose of pentazocine (mg)

21 (7.5–22.5)

21 (7.5–22.5)

NS

Patients receiving midazolam Dose of midazolam (mg)

17 (13)

28 (14)

NS

7 (2–20)

8 (2–20)

NS

Data are presented as n, n (%), or median (range)

Values are expressed as the number of patients (%) or median (range). Differences in categorical variables between two groups were examined by the Chi square test or by Fisher’s exact test when required. The non-parametric Mann–Whitney U test was used for comparing continuous variables. A P value \ 0.05 was considered significant. All statistical analyses were conducted with JMP version 10 (SAS Institute, Cary, NC, USA).

Results Pulmonary function and clinicopathological features Among the 322 patients, 127 (39 %) had pulmonary dysfunction. Among them, 117 patients had a FEV1.0% \70 %, 21 had %VC\80 %, and 11 fulfilled both criteria. The median FEV1.0% of the pulmonary dysfunction group and normal group was 62 and 76 % (P \ 0.001), and the median %VC was 102 and 111 % (P \ 0.001), respectively (Table 1). Among the 127 pulmonary dysfunction patients, the FEV1.0% was \70, \60, and \50 %, in 117, 29, and 11 patients, respectively.

FEV1.0% forced expiratory volume 1.0 s/forced vital capacity, %VC vital capacity, M tumor confined to the mucosa, SM1 tumor confined to the submucosa and tumor invasion within 0.5 mm of the muscularis mucosae, SM2 tumor confined to the submucosa and tumor invasion of 0.5 mm or more into the muscularis mucosae, NS not significant

Baseline characteristics and related factors are presented in Table 1. The median age was 73 and 69 years in the pulmonary dysfunction group and normal group, respectively (P \ 0.001). There was no significant difference in sex, location of gastric lesion, resection size, or tumor size between the two groups. The median procedure time was 57 min in the dysfunction group and 64 min in the normal group; however, the difference was not statistically significant (Table 1). Curative resection rates were 91 % in the pulmonary dysfunction group and 90 % in normal group (Table 1). Sedative drugs used in the study Table 1 shows the sedative drugs administered to the patients and the median doses; no significant differences were observed between both groups.

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Surg Endosc Table 2 Transcutaneous carbon dioxide tension values, transcutaneous oxygen saturation values, and oxygen flow rate Pulmonary dysfunction group (n = 127)

Normal group (n = 195)

P value

Baseline PtcCO2 (mmHg)

41 (23–62)*

42 (21–58)*

NS

PtcCO2 after ESD (mmHg)

50 (39–72)*

50 (24–74)*

NS

Peak PtcCO2 (mmHg)

51 (41–78)

51 (28–74)

NS

PtcCO2 [ 60 mmHg during ESD

9 (7)

19 (9)

NS

Minimum SpO2 (%)

98 (90–100)

98 (89–100)

NS

Oxygen flow rate (L/min)

2 (1–5)

2 (2–4)

NS

Data are presented as n (%) or median (range) ESD, endoscopic submucosal dissection; PtcCO2, transcutaneous carbon dioxide tension; SpO2, transcutaneous oxygen saturation * P \ 0.001

PtcCO2 and SpO2 The median (range) PtcCO2 before (baseline) and after the procedure was 41 mmHg (23–62) and 50 mmHg (39–72) in the pulmonary dysfunction group and 42 mmHg (21–58) and 50 mmHg (24–74) in the normal group, respectively; there were no significant differences between the groups. The PtcCO2 increased significantly (P \ 0.001) after the procedure in both groups. The median minimum SpO2 level and oxygen flow rate were similar between both groups (98 % and 2.0 L/min, respectively) (Table 2). Correlations between ESD procedure time and PtcCO2 elevation from baseline are shown in Fig. 1A and B. In the pulmonary dysfunction group, but not in the normal group, PtcCO2 elevation from baseline significantly correlated with procedure time (r = 0.22, P \ 0.05). Furthermore, in the pulmonary dysfunction group with FEV1.0% \60 %, the correlation was stronger (r = 0.39, P \ 0.05). Incidence of post-ESD complications and hospital stay ESD-related complications and hospital stay are shown in Table 3. CO2 insufflation did not cause any adverse events such as CO2 narcosis or gas embolism in either group. No significant difference was observed between the two groups in the incidence of fever (body temperature, [37.5 °C), pneumonia, perforation, post-ESD hemorrhage, or Mallory–Weiss Syndrome. Serum levels of CRP on days 1 and 3 after ESD and white blood cell count on day 1 after ESD were not significantly different between both groups. The median hospital stay was the same in both groups.

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Fig. 1 A Correlation between procedure time and PtcCO2 elevation from baseline in patients who received gastric endoscopic submucosal dissection. B Correlation between procedure time and PtcCO2 elevation from baseline in patients with FEV1.0% \60 %. Gray area: 95 % confidence interval. PtcCO2 transcutaneous partial pressure of CO2, ESD endoscopic submucosal dissection, FEV1.0%, forced expiratory volume in 1.0 s/forced vital capacity

Discussion The usefulness and safety of CO2 as an alternative to air have been demonstrated in several randomized controlled trials for various kinds of endoscopic procedures [20–24], but these studies excluded patients with pulmonary dysfunction because of the possible risk of CO2 retention and complications. However, many ESD patients are of advanced age, and pulmonary dysfunction prevails in these patients. In the present study, pulmonary dysfunction was found in 39 % of the 322 patients undergoing gastric ESD, and the median age in the pulmonary dysfunction group was significantly higher than that of the normal group. To the best of our knowledge, the present study is the first to investigate the safety and efficacy of CO2 insufflation in gastric ESD patients with pulmonary dysfunction.

Surg Endosc Table 3 Complications, blood parameters, and hospital stay

Data are presented as n, n (%), or median (range) ESD endoscopic submucosal dissection, CRP C-reactive protein, WBC white blood cell

Pulmonary dysfunction group (n = 127)

Normal group (n = 195)

P value

Fever (body temperature, [ 37.5 °C)

34 (26.8)

57 (29.2)

NS

Pneumonia

12 (9.4)

25 (12.8)

NS

Perforation

1 (0.8)

1 (0.5)

NS

Post-procedure hemorrhage

2 (1.6)

4 (2.0)

NS

Mallory–Weiss Syndrome

1 (0.8)

4 (2.0)

NS

CRP on day 1 after ESD (mg/dL)

0.7 (0.04–6.91)

0.6 (0.03–5.09)

NS

CRP on day 3 after ESD (mg/dL) WBC on day 1 after ESD (/lL)

3.1 (0.14–14.85) 8,210 (3,310–18,460)

3.3 (0.12–21.4) 8,510 (3,620–17,470)

NS NS

Hospital stay (days)

9 (7–18)

9 (5–15)

NS

In similar ESD conditions regarding procedure time, sedative drug dose, and minimum SpO2, both the median PtcCO2 after the procedure and the median peak PtcCO2 did not differ between the pulmonary dysfunction group and normal group in this study. These findings suggest that pulmonary dysfunction may not be directly associated with PtcCO2 elevation. Because hypoventilation caused by conscious sedation significantly raises the risk of hypercapnia [33], we speculate that the elevated PtcCO2 in both groups after the procedures is probably due to respiratory depression associated with conscious sedation. Several trials have also demonstrated that respiratory depression caused by deep sedation is involved in the elevation of PaCO2 or PtcCO2 in patients undergoing endoscopic treatment [23, 25, 26, 34]. In the present study, the maximum PtcCO2 reached 78 mmHg in the pulmonary dysfunction group and 74 mmHg in the normal group. However, no adverse events such as acidosis, CO2 narcosis, or SpO2 depression possibly caused by CO2 retention were reported in either group. The overall incidence of ESD complications and hospital stay did not differ between the two groups. These results indicate that CO2 insufflation is safe for gastric ESD in patients with pulmonary dysfunction under the following treatment conditions: a CO2 insufflation rate of 1.4 L/min and a median procedure time of 57 min. Similar to our results, Yoshida et al. [35] reported that in a colorectal ESD series of patients under conscious sedation with a mean procedure time of 54 min, there was no significant change in PetCO2 level in both the normal pulmonary function group and obstructive ventilatory disturbance group. On the other hand, there was a significant correlation between PtcCO2 elevation and procedure time in the pulmonary dysfunction group in the present study. Particularly in the patients with FEV1.0% \60 %, the correlation was stronger. In these patients, PtcCO2 could increase by

20 mmHg if the procedure time exceeds over 120 min (Fig. 1B). Therefore, in patients with severe obstructive lung disease, a longer ESD procedure would raise the risk of CO2 retention. Suzuki et al. [34] reported that in an esophagogastroduodenal ESD series of patients under conscious sedation, FEV1.0% \70 % was a relative enhancement factor of PaCO2. Hence, continuous PtcCO2 monitoring is essential, and every effort should be exerted to maintain the procedure time as short as possible in this subgroup. In the present study, no CO2 embolism was reported in either group. CO2 embolism is a rare but potentially lifethreatening complication. It has not been reported in digestive endoscopic procedures including ESD, but has mainly been reported in laparoscopic procedures [36]. Because of its high solubility in blood, entry of a large amount of CO2 into the circulation in a short time might be essential for CO2 embolism [37, 38]. In any case, CO2 embolism is a very rare complication, and a large number of patients would be required to detect a possible difference in its incidence between the two groups. The number of patients of our study is small to give a sufficient statistical power for this aim. The present study has some limitations. First, it was a single-center, uncontrolled study, and future studies are required to address this issue. Second, the correlation between PtcCO2 and PaCO2 is unclear because no blood gas samples were obtained in this study. It is reported that PtcCO2 is usually higher than PaCO2 by 5–6 mmHg [39, 40]; however, in the future, blood gas analysis should be conducted to clarify the relationship between the PtcCO2 and PaCO2 or pH. On the other hand, one of the strengths of this study was that our results indicating the safety of gastric ESD in patients with pulmonary dysfunction, who tend to be older, are especially noteworthy when considering the clinical setting of candidate patients.

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In conclusion, this study strongly suggests that CO2 insufflation is safe and effective during gastric ESD in patients with pulmonary dysfunction under conscious sedation as long as appropriate conditions are met (CO2 insufflation rate, 1.4 L/min; median procedure time, 57 min). However, in patients with severe obstructive lung disease, a longer procedure time may raise the risk of CO2 retention, and PtcCO2 should be carefully monitored in these patients to avoid complications.

Disclosures Drs. Jun Takada, Hiroshi Araki, Fumito Onogi, Takayuki Nakanishi, Masaya Kubota, Takashi Ibuka, Masahito Shimizu, and Hisataka Moriwaki have no conflicts of interest or financial ties to disclose.

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Safety of carbon dioxide insufflation during gastric endoscopic submucosal dissection in patients with pulmonary dysfunction under conscious sedation.

Carbon dioxide (CO2) insufflation is effective for gastric endoscopic submucosal dissection (ESD). However, its safety is unknown in patients with pul...
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