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(Hypertension. 1997;29:1114-1118.)
© 1997 American Heart Association, Inc.

Articles

Neural Circulatory Responses to Carbon Monoxide in Healthy Humans

Martin Hausberg; ; Virend K. Somers

From the Department of Internal Medicine and Cardiovascular Center, University of Iowa College of Medicine, Iowa City.

Correspondence to Virend K. Somers, MD, DPhil, Department of Internal Medicine, University of Iowa Hospitals and Clinics, Iowa City, IA 52242-1081.

	Abstract

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Abstract The contribution of carbon monoxide (CO) to the acute cardiovascular effects of smoking is not clear. Using a double-blind, randomized, vehicle-controlled study design, we examined the sympathetic and vascular responses to modest increases in carboxyhemoglobin in 10 healthy humans. We measured muscle sympathetic nerve activity (microneurography), forearm blood flow (plethysmography), heart rate, blood pressure, and minute ventilation at baseline and during 60 minutes of CO inhalation (1000 ppm during the first 30 minutes and 100 ppm during the last 30 minutes). The same measurements were made in a vehicle session (room air inhalation) on a separate day. During the first 30 minutes of CO inhalation, carboxyhemoglobin levels increased progressively from 0.2±0.1% to 8.3±0.5% and were maintained at about this level for a further 30 minutes. Forearm vascular resistance did not change with CO but increased slightly with vehicle; the effects of CO on muscle sympathetic nerve activity, forearm blood flow, blood pressure, heart rate, and minute ventilation were not significantly different from the effects of vehicle. Modest increases in carboxyhemoglobin levels equivalent to those resulting from cigarette smoking are unlikely to contribute to the acute sympathetic and hemodynamic effects of smoking in healthy humans.

Key Words: carbon monoxide • carboxyhemoglobin • sympathetic nervous system • smoking

	Introduction

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Globally, at least 250 million tons of CO are emitted from industrial and natural sources every year. However, the leading source of inhaled CO is tobacco smoke.¹ Several studies suggest that CO originating from tobacco smoke may contribute to the development of atherosclerotic disease.^{2 3} CO, even in modest concentrations, acutely decreases tissue oxygen saturation.^{1 4 5} This may result in reduced myocardial contractility and exercise performance and may induce arrhythmias in patients with coronary artery disease.^{4 6 7 8 9} Ayres et al⁴ observed an increase in cardiac output and minute ventilation at COHb levels of 9%. However, other studies in healthy humans suggest that modest levels of CO have little effect on exercise performance, cardiac output, HR, BP, or minute ventilation.^{1 5 10 11 12}

Recent data from animal studies indicate that CO acts to modulate vasomotor control.^{13 14 15 16} CO in high concentrations may elicit vasodilation^{14 15 16 17} and sympathetic activation.^{15 16} Increased sympathetic activation and consequent hemodynamic effects of CO may have implications for understanding the relationship between atmospheric CO pollution and fatality rates in patients with acute myocardial infarction.¹⁸ COHb levels of between 6% and 10% have been shown to decrease the threshold for ventricular fibrillation in monkeys with experimental acute myocardial infarction.^{19 20} Heavy cigarette smokers with coronary artery disease have an increased incidence of sudden death.²¹ The effects of modest carboxyhemoglobinemia, similar to that produced by cigarette smoking, on vascular resistance and sympathetic activity in humans are not known.

Smoking acutely increases BP, HR, vascular resistance, and cardiac output and decreases MSNA.^{22 23} This decrease in MSNA is thought to be baroreflex-mediated; however, smoking may decrease baroreflex sensitivity.²² This suggests that other mechanisms may contribute to the smoking-induced sympathetic inhibition. Indeed, a recent study in animals suggests that very low concentrations of CO may inhibit sympathetic outflow.¹³

We performed the present study to define the sympathetic and hemodynamic responses to CO inhalation and to determine whether carboxyhemoglobinemia may contribute to the acute sympathetic and hemodynamic effects of smoking.

	Methods

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Subjects
We studied 10 healthy normotensive subjects (age, 27±5 years [mean±SD]; mean body mass index, 26±6 kg/m²; eight men and two women). Except for one man who smoked 10 cigarettes per week, all subjects were nonsmokers. None of the subjects was taking any medication or had a history of chronic disease. All subjects had BP less than 130/80 mm Hg measured in the sitting position on three different occasions. The study design was vehicle-controlled, randomized, and double-blinded. All subjects underwent a CO and vehicle inhalation session. Each session was carried out on a separate day. The studies were approved by the Institutional Review Board on Human Investigation, and written informed consent was obtained.

Measurements
HR was measured continuously by an electrocardiogram. BP was measured each minute with an automatic sphygmomanometer (Life Stat 200, Physio Control Corp). FBF was measured by venous-occlusion plethysmography with an air plethysmograph.²⁴ Respiration was monitored by a strain-gauge pneumotach and end-tidal PCO₂ by a Hewlett-Packard 47210A Capnometer. Minute ventilation was determined with a Wright Respirometer (Ferraris Development & Engineering Co Ltd).

Microneurography
Intraneural recording techniques were used to obtain multifiber recordings of postganglionic MSNA. A tungsten microelectrode (200-µm diameter shaft; 1- to 5-µm uninsulated tip) was inserted into a sympathetic nerve fascicle of the peroneal nerve posterior to the fibular head so that recordings of efferent sympathetic traffic to muscle blood vessels could be obtained. A reference electrode was inserted subcutaneously 1 to 3 cm from the recording electrode. Electrodes were connected to a preamplifier (gain, 1000) and amplifier (variable gain, 30 to 90). Neural activity was fed to a band-pass filter (width, 0.7 to 2.0 kHz) and resistance-capacitance integrating network (time constant, 0.1 second) to obtain a mean voltage neurogram. In all subjects, the muscle sympathetic nerve recordings met standard criteria.^{25 26} The technique is described in more detail elsewhere.^{25 26}

Protocol
Subjects were studied while they were in the supine position. An intravenous catheter was placed in the left antecubital vein for blood sampling. FBF was measured in the right arm. A satisfactory sympathetic nerve recording site was then achieved.

The gas mixtures (1000 and 100 ppm CO in room air, and room air as vehicle control) were stored in a Douglas bag. The subjects breathed from the Douglas bag through 1-inch tubing, an Otis-McKerrow valve, and a large mouthpiece. A nose clip was placed to ensure exclusive mouth breathing.

After instrumentation, 5 minutes of resting measurements were obtained while the subjects inhaled room air through the mouthpiece. Blood samples were taken for hemoglobin and COHb. Subjects then inhaled either room air or 1000 ppm CO from the Douglas bag for 30 minutes. Subjects then continued to inhale room air or 100 ppm CO for another 30 minutes. During the period of exposure to either CO or vehicle, measurements were obtained during 5 out of every 10 minutes, and COHb was measured every 10 minutes.

Assays
Immediately after the blood samples were taken, COHb was determined by spectrophotometry with an OSM3 Hemoximeter (Radiometer America Inc).

Analyses
Sympathetic neurograms, electrocardiograms, and tracings of respiration and FBF were recorded on a physiological recorder (model TW11, Gould Inc) at a paper speed of 5 mm/s and simultaneously on a computerized data-acquisition system (MacLab, AD Instruments Inc) in combination with a Macintosh Quadra 950 Computer (Apple Computer Inc). Sympathetic activity, which occurs in bursts, was identified while blinded to the intervention (CO or vehicle). Sympathetic nerve activity was measured as bursts per minute and as integrated activity, ie, the integral of bursts of activity per minute. Interobserver and intraobserver variabilities in identifying bursts were approximately 6% and 5%, respectively.²⁵ FBF is expressed as milliliters per minute per 100 mL forearm volume. FVR is calculated as mean arterial pressure (measured by the automatic sphygmomanometer) divided by FBF and is expressed in arbitrary units.

For each variable (MSNA, HR, BP, FBF, etc), every 5-minute period of data collection was averaged to a single value. Data are presented as mean±SE.

For statistical analysis, we used repeated measures ANOVA with session as the between and time as the within factor. The key variable was the session-by-time interaction. Comparisons within a session (baseline versus inhalation) were made by post hoc tests (planned contrasts). A value of P<.05 was considered significant.

	Results

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The subjects had an average hemoglobin concentration of 13.8±0.4 g/dL. Baseline COHb levels of 0.2±0.1% increased to 8.3±0.5% after 30 minutes of 1000 ppm CO inhalation (P<.05) and were maintained at about this level during the 30 minutes of 100 ppm CO inhalation (Fig 1, Table). Vehicle (room air) inhalation did not change COHb levels (Table).

View larger version (38K): [in this window] [in a new window]   Figure 1. COHb levels at baseline and during 60 minutes of CO inhalation. CO in a concentration of 1000 ppm (0.1%) raised COHb levels linearly from 0.2±0.1% to 8.3±0.5% over 30 minutes. This level was maintained by 100 ppm (0.01%) CO inhalation. *P<.05 vs baseline; #P<.05 vs preceding value (n=10; data are mean±SE).

View this table: [in this window] [in a new window]   Table 1. Effects of Carbon Monoxide or Vehicle Inhalation on Resting Measurements

Baseline minute ventilation averaged 6.9±0.5 and 6.9±0.3 L/min during CO and vehicle sessions, respectively, and was not changed by CO or vehicle inhalation (Table). Neither CO nor vehicle inhalation changed end-tidal PCO₂ (Table).

BP, FBF, and HR did not change with CO or vehicle inhalation (Figs 2 and 3, Table). FVR increased slightly during vehicle inhalation but did not change during CO inhalation; the session-by-time interaction reached statistical significance. MSNA during CO was not significantly different from that during vehicle (Figs 2 and 3, Table).

View larger version (29K): [in this window] [in a new window]   Figure 2. Electrocardiographic (EKG) tracings, mean voltage neurograms, and forearm plethysmograms at baseline and after 60 minutes of CO inhalation in one subject. COHb increased from 0.1% to 8.2%. This increase did not appreciably change HR, mean arterial pressure (MAP), FBF (FoBF in figure) or FVR.

View larger version (27K): [in this window] [in a new window]   Figure 3. Time course of measurements of integrated MSNA, HR, mean arterial pressure (MAP), and FVR at baseline and during CO () or vehicle () inhalation. CO did not produce any changes different from those seen with vehicle, with the exception of FVR, which was lower during CO than vehicle. *P<.05, CO vs vehicle. Data are mean±SE; n=10.

We further analyzed these data excluding the one subject who was an occasional smoker. In this subject, COHb levels at baseline on both study occasions were low (0.4%). Excluding this subject from the data analysis did not change any of the above findings. None of the measured variables (MSNA, BP, HR, and minute ventilation) changed significantly with CO compared with vehicle. The session-by-time interaction for FVR remained statistically significant.

	Discussion

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Exposure of humans to increased levels of CO is widespread. This occurs through atmospheric pollution, environmental exposure, and cigarette smoking. High CO levels have been implicated in arrhythmias, decreased ventricular fibrillation thresholds,^{19 20} and increased mortality after myocardial infarction.¹⁸ Our study examined the effects of CO on sympathetic and hemodynamic measurements in healthy humans.

The initial 30 minutes of CO inhalation produced an increase in COHb levels similar to that achieved by the successive smoking of 5 to 9 cigarettes.^{27 28} The plateau COHb levels maintained over 30 minutes were similar to those observed in people smoking 20 cigarettes or more a day.²⁹ The plateau levels were also similar to those that have been associated with a decreased threshold for ventricular fibrillation in monkeys with experimental myocardial infarction.^{19 20} Neither the lower blood concentrations of CO during the first part of the inhalation nor the higher maintenance CO concentrations affected BP, HR, MSNA, or ventilation. The unchanged FVR with CO compared with the increase in FVR with vehicle may indicate a slight vasodilator action of CO, which opposes the vasoconstriction seen during the control or vehicle session. Thus, modest increases in COHb levels have little effect on sympathetic activity and hemodynamics. CO alone does not appear to contribute to the acute sympathetic and hemodynamic effects of smoking.

COHb levels as low as 5% cause a considerable loss in the oxygen-carrying capacity of blood.¹ Tissues most sensitive to oxygen deprivation, such as the brain and myocardium, are most affected by CO. Visual discrimination, motor coordination, and psychological performance are significantly impaired at COHb concentrations as low as 3%.^{4 30 31 32} Similar COHb levels may decrease exercise performance and induce arrhythmias in patients with coronary artery disease.^{4 6 7 8 9} It has been estimated that the consequent reduction in venous or tissue oxygen tension (not measured in our study) may be similar to that caused by the reduction of arterial oxygen tension at an altitude of 8000 to 10 000 feet.¹ This level of hypoxia acutely elicits increases in HR, BP, ventilation, and MSNA.³³

However, in contrast to hypoxia, modest carboxyhemoglobinemia has not been found to stimulate carotid or aortic chemoreceptors.^{14 34 35} COHb levels achieved in our study (approximately 8%) are well below levels that elicit increases in chemoreceptor afferent discharge (about 50%). The carotid chemoreceptors in particular, which are the chemoreflex sensors in humans, appear to be sensitive mainly to the partial pressure of oxygen and less sensitive to oxygen delivery.³⁴ Unless an increase in COHb was induced abruptly,⁴ most studies have failed to show an effect of modest carboxyhemoglobinemia on resting BP, HR, cardiac output, or ventilation.^{1 5 11 12} Neither sympathetic activity nor vascular resistance was measured in these earlier studies. Evidence for sympathetic activation by CO arises thus far only from animal studies involving high CO concentrations.^{15 16}

This is the first study directly assessing the effects of modest carboxyhemoglobinemia on sympathetic nerve activity and peripheral vascular resistance in humans. Smoking induces similar COHb levels^{27 28 29} and acutely increases BP, HR, cardiac output, and peripheral vascular resistance but decreases central sympathetic outflow.^{22 23} A recent animal study suggests that very low CO concentrations may reduce sympathetic outflow.¹³ Our data indicate that CO does not contribute to the reduction in central sympathetic outflow or to other hemodynamic changes seen with smoking in humans.

Our data also suggest that changes in sympathetic neural activity and hemodynamics are unlikely to explain the increase in fatality rates¹⁸ and decreased ventricular fibrillation threshold^{19 20} reported in association with increased COHb levels. Thus, other cardiovascular effects of CO, not measured in our study, are likely to be implicated in the effect of CO on myocardial infarction fatalities¹⁸ and ventricular fibrillation thresholds^{19 20} and in the effect of cigarette smoking increasing sudden death in people with coronary artery disease.²¹

Limitations of the present study include, first, the fact that except for one subject, only nonsmokers were studied. It is conceivable that smokers may show different reactions to increases in COHb. To our knowledge, there are no reports of different cardiovascular responses to CO in smokers versus nonsmokers. Second, the BP measurements have an accuracy of ±5 mm Hg and the FBF measurements have an error of 10% to 15%. Hence, small changes in BP and FBF may have been missed.

Conclusion
Modest increases in COHb levels, equivalent to that resulting from cigarette smoking, do not have any appreciable acute effects on MSNA, BP, HR, or FBF and thus are unlikely to contribute to the acute sympathetic and hemodynamic effects of smoking in healthy humans. The unchanged FVR with CO as opposed to a slight increase in FVR with vehicle may indicate a peripheral vasodilator action of even modest CO levels.

	Selected Abbreviations and Acronyms

 

BP = blood pressure CO = carbon monoxide COHb = carboxyhemoglobin FBF = forearm blood flow FVR = forearm vascular resistance HR = heart rate MSNA = muscle sympathetic nerve activity

	Acknowledgments

 
These studies were supported by the University of Iowa Environmental Health Sciences Research Center (National Institutes of Health/National Institute of Environmental Health Sciences [NIH/NIEHS] P30 ES05605) and by a training grant from the German Research Association. Other support includes an American Heart Association Grant-in-Aid, the Council for Tobacco Research, and NIH grants HL-43514, HL-44546, HL-24962, and HL-14388, Division of Research Resources, NIH. Virend K. Somers is a Sleep Academic Awardee of the NIH. We acknowledge the technical assistance of Diane E. Davison, MA, RN, and Chadi Abou-Assaly. We also appreciate assistance with statistical analysis from Bridget Zimmerman, PhD. Carboxyhemoglobin and hemoglobin levels were measured by the Critical Care Laboratory at the University of Iowa. We thank Dr Allyn L. Mark for support and advice and for reviewing this manuscript.

Received August 29, 1996; first decision September 20, 1996; accepted November 18, 1996.

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This Article Abstract Alert me when this article is cited Alert me if a correction is posted Citation Map Services Email this article to a friend Similar articles in this journal Similar articles in PubMed Alert me to new issues of the journal Download to citation manager Request Permissions Citing Articles Citing Articles via HighWire Citing Articles via Google Scholar Google Scholar Articles by Hausberg, M. Articles by Somers, V. K. Search for Related Content PubMed PubMed Citation Articles by Hausberg, M. Articles by Somers, V. K. Pubmed/NCBI databases Compound via MeSH Substance via MeSH Hazardous Substances DB CARBON MONOXIDE Medline Plus Health Information Smoking