Plasticity of central chemoreceptors: effect of bilateral carotid body resection on central CO2 sensitivity.

Human breathing is regulated by feedback and feed-forward control mechanisms, allowing a strict matching between metabolic needs and the uptake of oxygen in the lungs. The most important control mechanism, the metabolic ventilatory control system, is fine-tuned by two sets of chemoreceptors, the per...

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Main Authors: Albert Dahan, Diederik Nieuwenhuijs, Luc Teppema
Format: Article
Language:English
Published: Public Library of Science (PLoS) 2007-07-01
Series:PLoS Medicine
Online Access:http://europepmc.org/articles/PMC1925127?pdf=render
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spelling doaj-c637901d44bd4577a78b0ce6c5257b422020-11-25T00:58:01ZengPublic Library of Science (PLoS)PLoS Medicine1549-12771549-16762007-07-0147e23910.1371/journal.pmed.0040239Plasticity of central chemoreceptors: effect of bilateral carotid body resection on central CO2 sensitivity.Albert DahanDiederik NieuwenhuijsLuc TeppemaHuman breathing is regulated by feedback and feed-forward control mechanisms, allowing a strict matching between metabolic needs and the uptake of oxygen in the lungs. The most important control mechanism, the metabolic ventilatory control system, is fine-tuned by two sets of chemoreceptors, the peripheral chemoreceptors in the carotid bodies (located in the bifurcation of the common carotid arteries) and the central CO2 chemoreceptors in the ventral medulla. Animal data indicate that resection of the carotid bodies results, apart from the loss of the peripheral chemoreceptors, in reduced activity of the central CO2 sensors. We assessed the acute and chronic effect of carotid body resection in three humans who underwent bilateral carotid body resection (bCBR) after developing carotid body tumors.The three patients (two men, one woman) were suffering from a hereditary form of carotid body tumors. They were studied prior to surgery and at regular intervals for 2-4 y following bCBR. We obtained inspired minute ventilation (Vi) responses to hypoxia and CO2. The Vi-CO2 responses were separated into a peripheral (fast) response and a central (slow) response with a two-compartment model of the ventilatory control system. Following surgery the ventilatory CO2 sensitivity of the peripheral chemoreceptors and the hypoxic responses were not different from zero or below 10% of preoperative values. The ventilatory CO2 sensitivity of the central chemoreceptors decreased by about 75% after surgery, with peak reduction occurring between 3 and 6 mo postoperatively. This was followed by a slow return to values close to preoperative values within 2 y. During this slow return, the Vi-CO2 response shifted slowly to the right by about 8 mm Hg.The reduction in central Vi-CO2 sensitivity after the loss of the carotid bodies suggests that the carotid bodies exert a tonic drive or tonic facilitation on the output of the central chemoreceptors that is lost upon their resection. The observed return of the central CO2 sensitivity is clear evidence for central plasticity within the ventilatory control system. Our data, although of limited sample size, indicate that the response mechanisms of the ventilatory control system are not static but depend on afferent input and exhibit a large degree of restoration or plasticity. In addition, the permanent absence of the breathing response to hypoxia after bCBR may aggravate the pathological consequences of sleep-disordered breathing.http://europepmc.org/articles/PMC1925127?pdf=render
collection DOAJ
language English
format Article
sources DOAJ
author Albert Dahan
Diederik Nieuwenhuijs
Luc Teppema
spellingShingle Albert Dahan
Diederik Nieuwenhuijs
Luc Teppema
Plasticity of central chemoreceptors: effect of bilateral carotid body resection on central CO2 sensitivity.
PLoS Medicine
author_facet Albert Dahan
Diederik Nieuwenhuijs
Luc Teppema
author_sort Albert Dahan
title Plasticity of central chemoreceptors: effect of bilateral carotid body resection on central CO2 sensitivity.
title_short Plasticity of central chemoreceptors: effect of bilateral carotid body resection on central CO2 sensitivity.
title_full Plasticity of central chemoreceptors: effect of bilateral carotid body resection on central CO2 sensitivity.
title_fullStr Plasticity of central chemoreceptors: effect of bilateral carotid body resection on central CO2 sensitivity.
title_full_unstemmed Plasticity of central chemoreceptors: effect of bilateral carotid body resection on central CO2 sensitivity.
title_sort plasticity of central chemoreceptors: effect of bilateral carotid body resection on central co2 sensitivity.
publisher Public Library of Science (PLoS)
series PLoS Medicine
issn 1549-1277
1549-1676
publishDate 2007-07-01
description Human breathing is regulated by feedback and feed-forward control mechanisms, allowing a strict matching between metabolic needs and the uptake of oxygen in the lungs. The most important control mechanism, the metabolic ventilatory control system, is fine-tuned by two sets of chemoreceptors, the peripheral chemoreceptors in the carotid bodies (located in the bifurcation of the common carotid arteries) and the central CO2 chemoreceptors in the ventral medulla. Animal data indicate that resection of the carotid bodies results, apart from the loss of the peripheral chemoreceptors, in reduced activity of the central CO2 sensors. We assessed the acute and chronic effect of carotid body resection in three humans who underwent bilateral carotid body resection (bCBR) after developing carotid body tumors.The three patients (two men, one woman) were suffering from a hereditary form of carotid body tumors. They were studied prior to surgery and at regular intervals for 2-4 y following bCBR. We obtained inspired minute ventilation (Vi) responses to hypoxia and CO2. The Vi-CO2 responses were separated into a peripheral (fast) response and a central (slow) response with a two-compartment model of the ventilatory control system. Following surgery the ventilatory CO2 sensitivity of the peripheral chemoreceptors and the hypoxic responses were not different from zero or below 10% of preoperative values. The ventilatory CO2 sensitivity of the central chemoreceptors decreased by about 75% after surgery, with peak reduction occurring between 3 and 6 mo postoperatively. This was followed by a slow return to values close to preoperative values within 2 y. During this slow return, the Vi-CO2 response shifted slowly to the right by about 8 mm Hg.The reduction in central Vi-CO2 sensitivity after the loss of the carotid bodies suggests that the carotid bodies exert a tonic drive or tonic facilitation on the output of the central chemoreceptors that is lost upon their resection. The observed return of the central CO2 sensitivity is clear evidence for central plasticity within the ventilatory control system. Our data, although of limited sample size, indicate that the response mechanisms of the ventilatory control system are not static but depend on afferent input and exhibit a large degree of restoration or plasticity. In addition, the permanent absence of the breathing response to hypoxia after bCBR may aggravate the pathological consequences of sleep-disordered breathing.
url http://europepmc.org/articles/PMC1925127?pdf=render
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