Transcutaneous oxygen monitoring in shock and resuscitation

Transcutaneous Oxygen Monitoring in Shock and Resuscitation By M a r c I. R o w e and Gerard W e i n b e r g

Miami, Florida 9 Transcutaneous oxygen tension (TcP02), arterial oxygen tension, pulse, blood pressure, cardiac output and base excess or deficit w e r e serially measured in 18 piglets, 7 to 14 days of age, subjected t o a 3 5 % hemorrhage and reinfusion of shed blood. Eight of 18 pigs died, There is a strong correlation b e t w e e n TcPO 2 and PaO~ during n o r m a l f l o w . b u t a marked discrepancy develops during hemorrhage. Cardiac output, base deficit, and TcPOz all f o l l o w a similar pattern during hemorrhage, but TcPO z decreases more rapidly and remains at a l o w level in the nonsurviving animals. TcPO 2, therefore, appears to be a sensitive, noninvasive indicator of l o w f l o w and t h e adequacy of resuscitation.

INDEX W O R D S : Transcutaneous oxygen tension; cardiac output; hemorrhagic shock; monitoring t e c h niques.

T H E MOST life-threatening probO NElemsOFfacing the newborn patient is inadequate tissue oxygenation-hypoxia. The recognition and management of the hypoxic infant require an effective method of monitoring oxygenation. Over the past 20 yr, serial determinations of arterial oxygen tension (PaO2) measured from fresh arterial blood specimens have become the primary tool for the clinical evaluation of the status of tissue oxygenation. This technique is helpful, despite the fact that arterial oxygen tension is but one of a multitude of factors that determine the adequacy of oxygenation at the cellular level. There are, however, several practical disadvantages to PaO: measurements. Samples must be drawn from accessible arteries, either by direct puncture or through an indwelling catheter. Arterial punctures are difficult to perform on the tiny baby and may result in vascular injury. Indwelling cannulae are associated with serious and sometimes fatal complications. In the small infant, repeated blood sampling can lead to a significant degree of hypovolemia. Also, since each sample must be individually measured, only intermittent rather than continuous monitoring of PaO, is possible. The quest for safe, noninvasive methods to continuously measure arterial oxygen levels has recently led to the development of a transcutaneous PO2 monitor that continuously measures Journal of Pediatric Surgery, Vol. 14, No. 6 (December), 1979

the cutaneous oxygen level (TcPO2). The technique is based on the principle that oxygen diffuses readily from the dermal vessels through the skin to the outer surface where it can be measured. Under normal conditions, TcPO2 is usually zero because blood flow is regulated so that the amount of oxygen released is about that necessary to match cutaneous oxygen consumption. With maximum dilatation of the skin vasculature, increased amounts of oxygen diffuse from the arterialized capillaries to the skin surface. The oxygen that then reaches the skin has a partial pressure that approaches arterial oxygen tension (PaO,_). As early as 1851, Von Gerlach studied oxygen diffusion through the human skin] Baumberger and Goodfriend] and later Rooth et all studied skin PO2 as a method of measuring arterial oxygen tension. They used an immersion technique, but the oxygen sensors were unreliable and the method too cumbersome for clinical use. In 1968, Huch and coworkers 4 began the development of a transcutaneous oxygen monitor. They modified the Clark electrode and experimented with various agents to cause vasodilatation and increased skin blood flow under the oxygen sensor. Initially, local chemical applications were tried but failed to elevate skin PO2 above 38 tort. It was then found that by raising skin temperature to between 42 ~ and 44~ local hyperemia resulted, and the TcPO2 closely approximated PaO> The present Huch electrode consists of a ringshaped, silver anode heated by a coil and contains three platinum cathodes. The elements From the Division of" Pediatric Surgery, University o f Miami School o f Medicine, Miami, Fla. Supported in part b)' NIH Grant No. HD04154-10, Veterans Administration Grant No. 049801, and Project Newborn. Presented before the lOth Annual Meeting o f the American Pediatric Surgical Association, Los Angeles, California, March 25 28, 1979. Address reprint requests to Marc" 1. Rowe, MD., Division o f Pediatric Surgery, University of Miami School o f Medicine, Miami, Fla. 9 1979 by Grune & Stratton, Inc. 0022-3468/79/1406-0028501.00/0 773

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a r e e n c a s e d in plastic and f a c e d by a d o u b l e m e m b r a n e o f teflon and c e l l o p h a n e . T h e o x y g e n sensor is c o n n e c t e d to e l e c t r o n i c e q u i p m e n t t h a t m e a s u r e s c u r r e n t flow b e t w e e n t h e silver a n o d e a n d the p l a t i n u m c a t h o d e s . C u r r e n t is t h e n c o n v e r t e d to o x y g e n tension in m i l l i m e t e r s of m e r c u r y a n d the v a l u e s d i s p l a y e d and r e c o r d e d . A f e e d b a c k c i r c u i t allows h e a t e n e r g y to be v a r i e d so t h a t skin t e m p e r a t u r e b e n e a t h the sensor c a n be c o n s t a n t l y m a i n t a i n e d at a p r e s e n t level. A l a r g e n u m b e r of clinical studies h a v e been c o n d u c t e d on h e a l t h y a n d sick infants u t i l i z i n g the H u c h e l e c t r o d e . 5-~ T h e c o r r e l a t i o n b e t w e e n PaO2 a n d T c P O 2 u n d e r n o r m a l c o n d i t i o n s is close ( R = > 0.9). H o w e v e r , in sick infants, p a r t i c u l a r l y babies w i t h low flow states, t h e d i f f e r e n c e b e t w e e n the two m e a s u r e m e n t s is often large. S i n c e t h e a m o u n t of o x y g e n r e a c h i n g t h e skin is d i r e c t l y r e l a t e d to the i n t e n s i t y o f the s k i n - b l o o d flow, this was p r e d i c t a b l e . A l t h o u g h s o m e a u t h o r s h a v e p o i n t e d out t h a t low flow states a r e a l i m i t a t i o n of t r a n s c u t a n e o u s PO2 as a m o n i t o r of a r t e r i a l PO2, 9 none has s t u d i e d t h e PaO2--TcPO2 relationship under controlled e x p e r i m e n t a l c o n d i t i o n s , or e v a l u a t e d t h e possibility t h a t c h a n g e s in T c P O 2 in r e l a t i o n to PaO2 m a y s e r v e as a sensitive n o n i n v a s i v e m e a s u r e of t h e low-flow s t a t e a n d effectiveness of t h e r a p y . T h e p u r p o s e of this s t u d y is (1) to d e t e r m i n e how closely T c P O 2 reflects PaO2 u n d e r n o r m a l conditions and during the low-flow state p r o d u c e d by h e m o r r h a g e ; (2) to s t u d y the c h a n g e s in T c P O 2 , a r t e r i a l blood p r e s s u r e , c a r d i a c o u t p u t , pulse rate, and base excess d u r i n g t h e low-flow s t a t e a n d t h e r e l a t i o n s h i p s of t h e s e m e a s u r e m e n t s to e a c h other, and (3) to a s c e r t a i n t h e v a l u e of T c P O 2 as a g u i d e to t h e a d e q u a c y o f r e s u s c i t a t i o n of t h e low flow state.

MATERIALS AND METHODS

Experimental Subjects Eighteen purebred, Yorkshire piglets, 7-14 days of age, were studied. Before the animal was accepted as an experimental subject, the mother had to be free of disease and the piglet's initial measurements of body weight, blood pressure, cardiac output, hematocrit, and PaO2 within the normal range. Vascular cannulation had to be accomplished without significant blood loss. The age group of 7-14 days was chosen because the ductus arteriosus is closed, and the absence of a significant shunt across the ductus simplifies cardiac output measurements and eliminates the possibility of hypoxemia developing as a result of a large right-to-left shunt.

Hemorrhage and Reinfusion Hemorrhage was chosen as the insult because it is measurable and reproducible, and hypovolemia is a frequently encountered cause of the low flow state. Experience in this laboratory has indicated that the blood volume of the l 2-wk-old piglet is approximately 80 ml/kg and that hemorrhage of 35% of the total blood volume produces a significant change in physiologic measurements and a 50% mortality. Warm heparinized-shed blood was rein fused 30 min after the hemorrhage.

Environmental Temperature Control Control of environmental temperatures is essential during the study of transcutaneous oxygen monitoring because of the direct relationship between skin-blood flow and skin temperature. Animals were maintained in an environmental temperature of 28~ during the experiment. Previous studies have demonstrated that piglets 7 days to 3 wk of age at an average environmental temperature of 28~ maintain a constant skin temperature of 36~ _+ I~ and a rectal temperature of 38.8~ -+ 1.2~ '~

Cannulations All cannulations were performed under general anesthesia achieved by the intraperitoneal injection of 20 mg/kg of pentobarbital. A thermodilution pediatric No. 4 French catheter (Subramanian Catheter, Edwards Laboratories, Santa Ana, Calif.) was passed through the left femoral artery into the aortic arch to measure cardiac output. The left external jugular vein was cannulated and a catheter then passed under pulse control into the right atrium or ventricle. This catheter was used as the injection site for cold normal saline solution during cardiac output measurements. A polyethylene catheter was passed from the right femoral artery into the lower abdominal aorta to a point just above the bifurcation to measure blood pressure and to serve as a sample site for arterial blood specimens. The right femoral vein was cannulated and the catheter passed into the inferior vena cava for obtaining venous blood samples and to serve as an inlet for reinfusion of shed blood. A thermometer was inserted into the rectum and a thermistor probe secured to the abdominal skin for body and skin temperature measurements.

Measurements Arterial blood pressure. Arterial blood pressure was measured continuously by a Statham gauge. Pulse rate. Pulse rate was determined from the arterial pulse waves inscribed on an oscillographic recorder. Cardiac output. Cardiac output was measured by the thermodilution technique using an Edwards 9500 thermodilution cardiac output computer (Edwards Laboratories, Santa Ana, Calif.). Because of the relatively small size of the piglet, the single catheter technique of Ganz and Swan had to be modified in a manner similar to that described by Mathier et al." Blood and serum studies. Arterial blood pH, PCO2 and PO2 were measured serially using a gas analyzer (Instrument Laboratories, Inc., Boston, Mass.). Base excess or deficit was calculated using a Severinghaus slide rule.

TRANSCUTANEOUS OXYGEN MONITORING

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In order to clearly present the specific results of this experiment, we have organized the data to deal with the three questions raised in the introduction.

Cutaneous oxygen tension. The transcutaneous oxygen monitor of the Huch design (Litton Medical Electronics Oxymoniton, Model SM 361, Elk Grove Village, Ill.) was utilized. The oxygen sensor was applied to the shaved upper abdominal skin of the piglet and held in place with an adhesive ring that creates an air-tight seal. The controls were then set to regulate heat output to achieve a temperature of 44~ under the electrode. A new membrane was used before each experiment and the electrode calibrated. Before the first reading, the sensor was allowed to stabilize in place for 45 min. TcPO2 was then continuously recorded. In order to prevent skin burns, the oxygen sensor was removed and placed on a new site every two hours.

Question 1 How closely does TcPO2 reflect PaO2 under normal conditions and during the low flow state produced by hemorrhage?--To answer the first part of the question, simultaneous measurements o f T c P O 2 and P a O 2 o f normal animals were analyzed. The mean difference between PaO2 and TcPO2 was 13.2 _* 7.8 m m / H g . There was a close correlation between these two measures r = 0.98 (Fig. 1). The TcPO2 - PaO2 ratio was 0.83. The relationship between TcPO2 and PaO2 during the low flow state was examined by comparing these measurements during hemorrhage. PaO2 increased slightly during the bleed, while TcPO2 fell rapidly to 10.3% of baseline immediately after hemorrhage (Fig. 2). The TcPO2-PaO 2 fell from 0.83 to 0.01.

PROTOCOL

Baseline measurements were made immediately and 30 min after cannulation. The animals were then bled 35% of their total blood volume over a 10-min period. Measurements were made every 2.5 rain during the bleed, at the completion of the hemorrhage and 30 rain posthemorrhage. Warm, shed-heparinized blood was then reinfused over a 10-rain period with measurements recorded every 2.5 rain. Serial measurements were made immediately after infusion, at 30 min, and then every hour until death, or to 10 hr after reinfusion. Animals who were hemodynamically stable at ten hours post infusion were considered survivors.

Question 2 What are the changes in TcPO2, blood pressure, cardiac output, pulse rate, and base excess during the low-flow state, and the relationships of these measurements to each other?--Serial measurements of TcPO> blood pressure, cardiac output, pulse rate and base excess were made during hemorrhage and 30 rain after completion of the bleed. There was little change in pulse rate

RESULTS

The piglets averaged 13,5 + 5.9 days of age and weighed 1.96 kg • 500 g. Eight of 18 animals (44.4%) died. The average time of death was 5 hr and 34 rain after hemorrhage. 100 PAO2

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during the entire period studied. Blood pressure and cardiac output fell 40% and 30%, respectively, by the end of hemorrhage. The base deficit increased from - 3 m E q / l i t e r to - 1 4 . 0 mEq/liter during the bleeding period. The most striking decrease was in TcPO2. The TcPO 2 fell 63% when hemorrhage was three-quarters complete, decreased 90% by the end of hemorrhage and 97% 30 min after the hemorrhage was over (Fig. 3).

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There were only minimal differences in pulse rate between surviving and nonsurviving animals until death. The blood pressure of the surviving and nonsurviving piglets followed the same pattern until just before death (Fig. 4). The cardiac output of both the surviving and nonsurviving piglets were similar during hemorrhage and reinfusion. However, by three hours post infusion the cardiac output of the nonsurviving animals was significantly lower than that of the survivors (p < .05). Like cardiac output, base deficit was similar in the survivors and nonsurvivors until three hours after infusion when the dying animals had a significantly lower base deficit (p < .05) (Fig. 5). TcPO2 followed a similar pattern as cardiac output and base deficit, but TcPO~ of the nonsurviving animals became significantly lower at 1 hr postinfusion (p < .05) (Fig. 6).

Question 3 What is the value of TcPO2 as a guide to the adequacy of resuscitation of the low flow state compared to the usual physiologic measurements?--To answer this question, serial measurements of blood pressure, pulse rate, cardiac output, base deficit or excess and TcPO~ of surviving and nonsurviving animals were compared during hemorrhage, reinfusion, and postreinfusion. HEMORRHAGE - - ~ I

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DISCUSSION

T h e results of this e x p e r i m e n t s u g g e s t

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TcPO2 closely reflects PaO2 under normal conditions, but that a marked difference develops between PaO2 and TcPO2 during the low-flow state. There appears to be no relationship between pulse rate and TcPO2 with hemorrhage. Blood pressure, cardiac output, base deficit, and TcPO2 similarly decrease during the low-flow state. However, TcPO2 falls more rapidly and to a greater extent than the other three variables. TcPO2, cardiac output and base deficit all appear to be indicators of physiologic deterioraHEMORRHAGE q ~ ,,,IpI 120 ~-i RE IINFUSIONI q 14""~l I

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tion and the adequacy of resuscitation, but TcPO~ may be an earlier and more sensitive indicator. There are several important clinical implications from this study. When using the transcutahe 9 oxygen monitor initially, PaO2 and TcPO 2 should be measured simultaneously. A close correlation between the two measurements suggests adequate tissue perfusion. If, during the course of transcutaneous oxygen monitoring, TcPO2 falls, a repeat PaO2 should be measured. A low PaO2 indicates hypoxemia. If PaO2 has not changed significantly, this suggests inadequate tissue perfusion. A persistent low TcPO 2 with treatment of the low-flow state suggests insufficient resuscitation. REFERENCES

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1. Von Gerlach: Ober das Hautatmen. Arch Anat Physiol (Leipzig) 431-479, 1851 2. Baumberger JP, Goodfriend RB: Determination of arterial oxygen tension in man by equilibration through intact skin. Fed Proc Fed Am Soc Exp Blot 10:10 11, 195I 3. Root G, Stostedt S, Caligara F: Bloodless determination of arterial oxygen tension by polarography. Science Tools. LKW Instruments J 4:37 45, 1957 4. Huch A, und Huch R: Klinische und physiologische Aspekte der transcutanen Sauerstoffdruckmessung in der Perinatalmedizin. Z Geburish Perinat 179:235 249, 1975 5. SwSinstrom S, et al: Transcutaneous PO~ measurements in seriously ill newborn infants. Arch Dis Child 5 0 : 9 1 3 - 9 1 9 , 1975 6. Rooth G: Transcutaneous oxygen tension measurements in newborn infants. Pediatrics 55:232-235, 1975

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7. Fenner A, et al: Transcutaneous determination of arterial oxygen tension. Pediatrics 55:224-231, 1975 8. Peabody JL, et al: Transcutaneous oxygen tension in sick infants. Am Rev Resp Dis 118:83 87, 1978 9. Versmold HT, et al: Limits to TcPO2 moniloring in sick neonates: Relation to blood pressure, blood volume, periph-

eral blood flow and acid base status. Acta Anesthesiol Scand Suppl 68:88-90, 1978 10. Rowe MI, Weinberg G: The newborn piglet as an experimental animal. (In press) 11. Mathier M, et al: Measurement of cardiac output by thermodilution in infants and children after open-heart operations. J Thor Cardiovasc Surg 72:221-225, 1976

Discussion W. L. Buntain (Birmingham): The experimental evidence to support this is essentially as you've heard. Most of the evidence in the literature is clinical evidence on newborn babies, primarily in Europe. I think this excellent study clearly documents from an experimental standpoint what we are trying to show from our studies: that low-flow states, particularly babies with shock or with necrotizing enterocolitis, present with a decreased peripheral profusion that can be monitored with a TcPO2 monitor. The effects of resuscitation certainly are well shown in this study. This is a significant contribution on a valuable method of monitoring. E. T. Boles, Jr. (Columbus, Ohio): This study establishes beyond question that low perfusion states can be accurately monitored by this transcutaneous technique. Dr. Gerald Lucey has been working with this device for a number of years. One of the more interesting things that he has learned is that right to left shunting through a patent ductus arteriosus can be accurately and continuously monitored by the use of two of these devices. For this purpose, one is placed high on the anterior chest and the other on the lower part of the abdomen. Many stimuli, particularly hypoxia, may be responsible for transient shunting through the ductus. Such monitoring obviously would be very helpful in following babies who have had repair of diaphragmatic hernias. He also found that there are many stimuli which occur to sick babies that produce rather dramatic, often transient, reductions in the PO2. These include poor feeding position with the head flexed, rapid gavage feedings, and noxious stimuli such as arterial sticks, bladder sticks, etc. Dr. Lucey has estimated that approximately 80 percent of the hypoxic episodes that

occurred in sick newborns were iatrogenic. The National Foundation is putting out a monograph on TcPO2 which will be published shortly. J. C. German (Orange. Calif.): We are currently studying TcPO2 in an open chest rabbit preparation looking at cardiac outputs in response to increased peak expiratory pressures. We found TcPO2 to be the most sensitive parameter reflecting decreased cardiac output. More important is the finding that a persistently low TcPO2 may reflect irreversibility of resuscitation. When the TcPO2 does not improve following whatever technique we use to resuscitate the animal it may turn out to be of great prognostic value. N. R. Feins (Boston): A word of caution, if you are giving a large amount of oxygen and the infant has a significant right left shunt at the ductus level the PO2 over the abdomen may be 50 mm Hg. J. A. San Fillipo (Valhalla, N.Y.): Were the authors able to correlate cardiac output with differences in the PaO2 and the TcPO2? D. Tapper (Boston): Were there any skin burns or any skin sloughs underneath the electrode? G. Weinberg (closure): I would like to thank the discussants for their comments and suggestions. We chose hemorrhage for our experiment because it is a simple technique that is easily reproducible. Next we plan on studying TcPO2 response to other low-flow states, such as PEEP. In clinical situations where a patent ductus arteriousus is suspected we place the probe over the scalp or right chest to determine the preductal arterial tension. By limiting probe placement to 3 or 4 hr at 43~ on a given spot we have not had any skin burns.