Comparison of blood flow assessment between laser doppler velocimetry and the hydrogen gas clearance method in ischemic intestine in dogs

Comparison of blood flow assessment between laser doppler velocimetry and the hydrogen gas clearance method in ischemic intestine in dogs

Comparison of Blood Flow Assessment Between Laser Doppler Velocimetry and the Hydrogen Gas Clearance Method in Ischemic Intestine in Dogs Yoshihiro Oo...

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Comparison of Blood Flow Assessment Between Laser Doppler Velocimetry and the Hydrogen Gas Clearance Method in Ischemic Intestine in Dogs Yoshihiro Oohata, MD, Ryuichi Mibu, MD, Masayuki Hotokezaka, MD, Shinichi Ikeda, MD, Shosaku Nakahara, MD, Hideaki Itoh, MD, Fukuoka,Japan

Blood flow of the colon and the ileum was measured before and after intestinal devascularization by laser Doppler velocimetry and the hydrogen gas clearance technique in 10 dogs in order to evaluate the clinical usefulness of laser Doppler velocimetry. The submucosal blood flow of the colon and the ileum measured by the hydrogen gas clearance method was significantly decreased, as was the subserosal blood flow of both sites measured by laser Doppler velocimetry. There was a linear relationship between the flow values using the two methods both in the colon (r = 0 . 7 1 9 2 , p < 0 . 0 0 1 ) and in the ileum (r = 0.7646, p < 0 . 0 0 1 ) . These data suggested laser Doppler velocimetry may be a useful m e t h o d to assess the degree of intestinal ischemia because of its noninvasiveness and good correlation with submucosal blood flow by the hydrogen gas clearance technique.

r arious methods are currently used to determine gastrointestinal blood flow [1-14]. The hydrogen gas clearance method is widely accepted to measure the submucosal blood flow of the intestine, but has limited clinical application because of its invasiveness [1-5]. Laser Doppler velocimetry permits continuous, real-time, and noninvasive measurement of tissue blood flow by the simple application of a probe to the serosa or mucosa of intestines [1,6-9]. In the present study, we compared subserosal blood flow measured by laser Doppler velocimetry with submucosal blood flow measured by the hydrogen gas clearance method in the same ischemic intestine in dogs to assess whether the former can substitute for the latter.

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From the Department of Surgery I, Kyushu University Faculty of Medicine, Fukuoka, Japan. Requests for reprints should be addressed to Yoshihiro Oohata, MD, Department of Surgery I, Kyushu University Faculty of Medicine, Fukuoka 812, Japan. Manuscript submitted February 13, 1989, and accepted in revised form May 3, 1990.

MATERIAL AND M E T H O D S Surgical preparation: Ten adult mongrel dogs of both sexes, weighing between 10 and 16 kg, were fasted for 24 hours and anesthetized with intravenous pentobarbital sodium, 25 mg/kg, with induction of intramuscular ketamine hydrochloride, 10 mg/kg. The dogs were intubated and ventilated artificially with room air at a tidal volume of 20 mL/kg, and supplemental doses were given as necessary to maintain adequate surgical anesthesia. The right external jugular vein was eannulated with a polyethylene catheter for hydration, thereby maintaining a stable blood pressure. The body temperature of the animals was maintained at approximately 37~ using an electrically heated warming blanket. Laparotomy was performed through a transverse incision, and the loops of transverse colon and the ileum were carefully exposed. After the measurement of control blood flow, the intestinal loops were devascularized for 10 cm by dividing the mesentery between the intestine and the marginal vessel. After the contraction of the bowel due to devascularization or denervation was released, the measurements of blood flow of the ischemic segments were performed at the mid-portion of the devascularized segment, the distal edge of the devascularized segment, and finally, in the middle of the two sites. At first, the submucosal blood flow was measured by the hydrogen gas clearance method; then the subserosal blood flow at three sites adjacent to the point recorded by the hydrogen gas clearance method were measured using laser Doppler velocimetry, and the mean value was calculated. The measurements were carried out at the antimesenteric side of the intestine. On the third postoperative day, the intestinal blood flow of the devascularized segments was evaluated in the same manner in the six surviving dogs. Hydrogen gas clearance: A platinum electrode needle 0.3 mm in diameter was placed into the submucosal layer through the serosal surface, and the electrode was connected to the tissue flowmeter model no. P H G 201 (Unique Medical Co., Tokyo, Japan). The reference electrode was placed under the skin in the right thigh of the animal and connected to the tissue flowmeter [2-5]. Laser Doppler velocimetry: The measurements were performed using a laser Doppler flowmeter A L F 2100 (Advance Co., Tokyo, Japan). This instrument contains a 2 mW He-Ne laser that generates monochromatic light of 632.8 nm wavelength with a penetration depth of 1 mm. The fiberoptic guide system is 1.5 meters in length and has a flow probe 0.1 mm in diameter with a holder 3 cm in diameter. Blood flow values were obtained from the

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TABLE I

Blood Flow of the Transverse Colon (mean 4- SD)" Before Devascularization (n = 10)

After Devascularization (n = 10) Mid-portion Distal edge

SM: 133.9 4- 33.6 SS: 58.6 4- 20.4

Middle of two sites

SM: SS: SM: SS: SM: SS:

24.0 7.9 99.7 27.4 56.7 11.2

Third Postoperative Day (n = 6)

4- 30.5 t 4- 3.9 t 4- 33.2t -I- 11.3 t 4- 47.6 t 4- 5.5 ~

SM: SS: SM: SS: SM: SS:

25.1 4- 39.0 t 8.6 4- 10.2 t 119.6 4- 26.0 25.2 4- 7.3 t 68.9 -4- 28.5 t 15.8 4- 7.2 t

" Blood flow = rnL/minute/100 g of tissue. t p < 0 . 0 0 1 versus before devascularization and after devascularization or the third postoperative day. t p < 0 . 0 0 5 versus before and after devascularization at the submucosal blood flow. SM = submucosal blood flow by hydrogen gas clearance method; SS = subserosal blood flow by laser Doppler velocimetry.

digital electronic display as absolute flow values: m L / minute/100 g of tissue. The flow probe with a holder was applied manually on the serosal surface with the minimal pressure necessary to maintain constant optical coupling between the probe and the bowel wall. Major vessels were avoided to obtain more accurate tissue flow values. The probe was applied at the three points adjacent to the site chosen for the hydrogen gas clearance technique. Continuous measurement for 30 seconds at one point was performed, and the mean value for the three points was calculated as the subserosal blood flow. Statistics: All flow values were expressed as mean 4standard deviation. Statistical analysis was done by using Student's t test for unpaired data. Linear regression analysis was used to determine the correlation of the flow values obtained by laser Doppler velocimetry and the hydrogen gas clearance method. RESULTS The submucosal and subserosal blood flow values of the transverse colon were 133.9 4- 33.6 and 58.6 4- 20.4 mL/minute/100 g of tissue, respectively. After devascularization, both the submucosal and subserosal blood flow

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values at the mid-portion of the ischemic segment were significantly decreased (p <0.001). The submucosal and subserosal blood flow values at the distal edge of the ischemic segment and in the middle of the two sites were also significantly decreased (p <0.001 and p <0.005, respectively), The submucosal and subserosal blood flow values at the mid-portion of the colonic segment on the third postoperative day are shown in Table I. Figure 1 indicates the correlation between the two flow values of the transverse colon obtained by laser Doppler velocimetry and the hydrogen gas clearance method. There was a significant linear relationship between the two values (r = 0.7192, n = 58, p <0.001). The submucosal and subserosal blood flow values of the ileum were 112.6 4- 46.8 and 61.4 4- 21.2 mL/minute/100 g of tissue, respectively. After devascularization, both the submucosal and subserosal flow values at the mid-portion of the ischemic segment were significantly decreased (p <0.001). On the third postoperative day, both the submucosal and the subserosal flow values at the same site were significantly lower than those before devascularization, but not significantly lower than those after devascularization (Table II). The correlation be-

y - 1.8651 + 0.2804x r = 0.T192 p < 0.001 n = 58

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6'0

8'0

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120

140

160

Submucosal blood flow by hydrogen gas clearance method (mlJmin.Jl00g of tissue)

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Figure 1. Correlation between s u b m u c o sal blood f l o w measured by the hydrogen gas clearance method and subserosal blood f l o w measured by laser D o p p l e r v e l o c i m e t r y in the transverse colon.

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BLOOD FLOW ASSESSMENT IN ISCHEMIC INTESTINE

T A B L E II

Blood Flow of the Ileum (mean • SO)" Before Devascularization (n = 10)

After Devascularization (n = 10) Mid-portion Distal edge

SM: 112.6 4- 46.8 SS: 61.4 4- 21.2

Middle of two sites

SM: SS: SM: SS: SM: SS:

18.2 8.7 96.2 33.6 43.6 14.7

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Third Postoperative Day (n = 6) 28.2 t 3.7 t 43.4 14.2 t 28.7 t 7.6 t

SM: SS: SM: SS: SM: SS:

0t 1.0 491.7 421.i 440,1 410.3 4-

1.8 t 29.3 9.1 t 37.8 ~ 7.6 t

9 Blood flow = rnL/minute/100 g of tissue. t p <0.001 versus before devascularization and after devascularization or the third postoperative day. SM = submucosal blood flow by hydrogen gas clearance method; SS = subserosal blood flow by laser Doppler velocimetry.

tween the two flow values of the ileum obtained by laser Doppler velocimetry and the hydrogen gas clearance method is shown in Figure 2. There was a significant linear relationship between the two values (r = 09 n = 58, p <0.001).

COMMENTS It is very important to determine the viability of ischemic bowel at the time of surgical exploration. Many methods have been used to evaluate intestinal viability-including measurement of surface temperature, electromyography, fluorescein dye, and Doppler ultrasonography--and to measure blood flow--including radioactive microspheres, photoplethysmography, the hydrogen gas clearance method, and laser Doppler velocimetry [ 1-14]. Laser Doppler velocimetry has the advantage of providing noninvasive, real-time, continuous measurement not affected by countercurrent flow [1,6-9]. The depth of tissue penetration by laser light is 1 mm, and the blood flow of 1 mm 3 of tissue can be monitored [6-911 The Doppler shift of the laser light is proportional to the velocity of red blood cells in the microcirculation. However, when a major vessel is included in the area, the flow

value obtained does not reflect exact tissue blood flow. Therefore, it is mandatory to avoid major vessels to obtain accurate flow values. In the present study, the probe was applied tO the serosal side of the intestine at three points adjacent to the site chosen for the hydrogen gas clearance technique. Another problem is the maintenance of the constant optical coupling without any tissue compression. A miniature suction cup and a syringe adapter were useful to diminish the problem [7-8]. We used a probe holder successfully to obtain stable and reproducible flow values9 The hydrogen gas clearance technique is widely used to measure submucosal blood flow [1-5] but has limited clinical application because it provides only discontinuous measurement, requires constant flow during the measurement, and damages tissue by electrode insertion. Furthermore, the clinical use of hydrogen gas is often limited in various situations. The submucosal blood flow of the intestine, which is thought to be important in the healing of anastomosis, has the most value if determined, but its measurement is difficult intraoperatively. In the present study, laser Doppler velocimetry was found to be useful in determin-

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y = 3.5505 + 0.3362x r = 07646 p < 0.001 n = 58

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== F i g u r e 2. Correlation b e t w e e n submucosal blood f l o w measured by the hydrogen gas clearance method and subserosal blood flow measured b y laser Doppler v e l o c l m e t r y in the ileum.

Submucosal blood f l o w by hydrogen gas clearance (ml/min./100g of tissue)

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ing blood flow in the acute and subacute phases of ischemic intestine because of its good linear relationship to submucosal blood flow obtained by the more standard h y d r o g e n gas c l e a r a n c e technique. Therefore, laser Doppler velocimetry m a y be a more useful and practical technique in assessing intestinal viability during operations than other methods.

The viability o f the bowel is often directly proportional to the viability o f the organism. This paper represents another effort to make the calls in grey areas more objective. REFERENCES 1. Granger DN, Kvietys PR. Recent advances in measurement of gastrointestinal blood flow. Gastroenterology 1985; 88: 1073-6. 2. Shikata J, Shida T, Satoh S, Furuya K, Kamiyama A. The effect of local flood flow on the healing of experimental intestinal anastomoses. Surg Gynecol Obstet 1982; 154: 657-61. 3. Aukland K, Bower BF, Berliner RW. Measurement of local blood flow with hydrogen gas. Circ Res 1964; 15: 164-87. 4. Mackie B, Chir M, Turner MD. The effect of truncal vagotomy on jejunal and ileal blood flow. J Surg Res 1971; 11: 356-63. 5. Bussemaker JB~ Lideman J. Comparison of methods to deter-

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mine viability of small intestine. Ann Surg 1972; 176: 97-101. 6. Shepherd AP, Riedel GL. Continuous measurement of intestinal mucosal blood flow by laser Doppler velocimetry. Am J Physiol 1982; 242: G668-72. 7. Feld AD, Fondacaro JD. Halloway G, Jacobsen ED. Measurement of mucosal blood flow in the canine intestine with laser Doppler velocimetry. Life Sci 1982; 31: 1509-17. 8. Chung RS. Blood flow in colonic anastomoses. Ann Surg 1987; 206: 335-9. 9. Lynch TG, Hobson RW II, Kerr JC, et al. Doppler ultrasound, laser Doppler fluorometry in bowel ischemia. Arch Surg 1988; 123: 483-6. 10. Katz S, Wahab A, Murray W, Williams LF. New parameters of viability in ischemic bowel disease. Am J Surg 1974; 127: 13641. 11. Zarins CK, Skinner DB, Rhodes BA, Everette James A. Prediction of the viability of revascularized intestine with radioactive microspheres. Surg Gynecol Obstet 1974; 138: 576-80. 12. Wright CB, Hobson W. Prediction of intestinal viability uSing Doppler ultrasound techniques. Am J Surg 1975; 129: 642-5. 13. Carter MS, Fantini GA, Sammartano RJ, Mitsudo S, Silverman DG, Boley SJ. Qualitative and quantitative fluorescein fluorescence in determining intestinal viability. Am J Surg 1984; 147: 117-23. 14. Pearce WH, Jones DN, Warren GH, et al. The use of infrared photoplethysmography in identifying early intestinal ischemia. Arch Surg 1987; 122: 308-10.

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