Splenectomy impairs diffusive oxygen transport in the lung of dogs.
Abstract: The spleen acts as an erythrocyte reservoir in highly aerobic species such as the dog and horse. Sympathetic-mediated splenic contraction during exercise reversibly enhances convective O2 transport by increasing hematocrit, blood volume, and O2-carrying capacity. Based on theoretical interactions between erythrocytes and capillary membrane (Hsia CCW, Johnson RL Jr, and Shah D. J Appl Physiol 86: 1460-1467, 1999) and experimental findings in horses of a postsplenectomy reduction in peripheral O2-diffusing capacity (Wagner PD, Erickson BK, Kubo K, Hiraga A, Kai M, Yamaya Y, Richardson R, and Seaman J. Equine Vet J 18, Suppl: 82-89, 1995), we hypothesized that splenic contraction also augments diffusive O2 transport in the lung. Therefore, we have measured lung diffusing capacity (DL(CO)) and its components during exercise by a rebreathing technique in six adult foxhounds before and after splenectomy. Splenectomy eliminated exercise-induced polycythemia, associated with a 30% reduction in maximal O2 uptake. At any given pulmonary blood flow, DL(CO) was significantly lower after splenectomy owing to a lower membrane diffusing capacity, whereas pulmonary capillary blood volume changed variably; microvascular recruitment, indicated by the slope of the increase in DL(CO) with respect to pulmonary blood flow, was also reduced. We conclude that splenic contraction enhances both convective and diffusive O2 transport and provides another compensatory mechanism for maintaining alveolar O2 transport in the presence of restrictive lung disease or ambient hypoxia.
Publication Date: 2006-04-06 PubMed ID: 16601302DOI: 10.1152/japplphysiol.01600.2005Google Scholar: Lookup
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- Journal Article
- Research Support
- N.I.H.
- Extramural
Summary
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The research article explores how removing the spleen (splenectomy) in dogs can negatively affect their lungs’ ability to transport oxygen. The study finds that the spleen helps distribute oxygen, particularly during exercise, and its removal can reduce oxygen uptake by 30%.
Research Context
- The study begins by discussing how some species, notably dogs and horses, use their spleens as an ‘erythrocyte reservoir’. Erythrocytes, or red blood cells, are responsible for carrying oxygen in the bloodstream.
- The authors explain that during exercise, the spleen contracts (a process driven by the sympathetic nervous system) which increases hematocrit (the proportion of blood that is made up of red blood cells), blood volume, and overall oxygen-carrying capacity.
Hypothesis
- Based on prior studies, the researchers form the hypothesis that spleenic contraction does not only enhance ‘convective’ oxygen transport (i.e., the direct movement of oxygen-carrying blood from the heart to the rest of the body) but also assists ‘diffusive’ transport. ‘Diffusive’ transport involves the movement of oxygen from the bloodstream into body tissues and cells.
Methodology
- To test their hypothesis, the researchers turned to a breed of hunting dog known as a foxhound. The team compared the dogs’ lung diffusing capacity (DL(CO)) during exercise both before and after splenectomy. DL(CO) refers to how efficiently the lungs can transfer oxygen from the air into the bloodstream.
- The post-splenectomy dogs showed a significant reduction in DL(CO) at any given level of pulmonary blood flow. This lower capacity was due to a reduced ‘membrane diffusing capacity’ (the ability of the lung’s cell membranes to allow oxygen to pass through), Albeit, the pulmonary capillary blood volume changed variably.
- Removing the spleen also lowered the degree of ‘microvascular recruitment’. This term refers to the body’s ability to increase the number of small blood vessels that are actively supplying oxygen to tissues during periods of high demand, such as during exercise.
- The study concludes that the contraction of the spleen enhances both convective and diffusive oxygen transport. Furthermore, this function represents a compensatory mechanism for maintaining alveolar O2 transport when facing restrictive lung disease or ambient hypoxia.
Findings
Conclusions
Cite This Article
APA
Dane DM, Hsia CC, Wu EY, Hogg RT, Hogg DC, Estrera AS, Johnson RL.
(2006).
Splenectomy impairs diffusive oxygen transport in the lung of dogs.
J Appl Physiol (1985), 101(1), 289-297.
https://doi.org/10.1152/japplphysiol.01600.2005 Publication
Researcher Affiliations
- Department of Internal Medicine, University of Texas Southwestern Medical Center, 5323 Harry Hines Blvd., Dallas, Texas 75390-9034, USA.
MeSH Terms
- Animals
- Blood Volume / physiology
- Carbon Monoxide / blood
- Dogs / physiology
- Erythrocyte Volume / physiology
- Hematocrit
- Hemoglobins / analysis
- Hypoxia / blood
- Hypoxia / physiopathology
- Lung / blood supply
- Lung / physiology
- Male
- Oxygen / blood
- Oxygen Consumption / physiology
- Physical Conditioning, Animal / physiology
- Polycythemia / blood
- Polycythemia / physiopathology
- Pulmonary Diffusing Capacity / physiology
- Respiratory Transport / physiology
- Rest / physiology
- Spleen / physiology
- Splenectomy
Grant Funding
- HL-062873 / NHLBI NIH HHS
- HL-040070 / NHLBI NIH HHS
- R01 HL-045716 / NHLBI NIH HHS
- R01 HL054060 / NHLBI NIH HHS
- HL-054060 / NHLBI NIH HHS
- R01 HL045716 / NHLBI NIH HHS
- R01 HL062873 / NHLBI NIH HHS
- R01 HL040070 / NHLBI NIH HHS
Citations
This article has been cited 9 times.- Lodin-Sundström A, Holmström P, Ekstam M, Söderberg D, Schagatay E. Splenic contraction is enhanced by exercise at simulated high altitude.. Eur J Appl Physiol 2021 Jun;121(6):1725-1732.
- Storz JF, Cheviron ZA. Physiological Genomics of Adaptation to High-Altitude Hypoxia.. Annu Rev Anim Biosci 2021 Feb 16;9:149-171.
- Hanadhita D, Rahma A, Prawira AY, Mayasari NLPI, Satyaningtijas AS, Hondo E, Agungpriyono S. The spleen morphophysiology of fruit bats.. Anat Histol Embryol 2019 Jul;48(4):315-324.
- Lee M, Park J, Choi H, Lee H, Jeong SM. Presurgical assessment of splenic tumors in dogs: a retrospective study of 57 cases (2012-2017).. J Vet Sci 2018 Nov 30;19(6):827-834.
- Hsia CC, Hyde DM, Weibel ER. Lung Structure and the Intrinsic Challenges of Gas Exchange.. Compr Physiol 2016 Mar 15;6(2):827-95.
- Ravikumar P, Bellotto DJ, Hsia CC. Persistent structural adaptation in the lungs of guinea pigs raised at high altitude.. Respir Physiol Neurobiol 2015 Mar;208:37-44.
- Yilmaz C, Ravikumar P, Bellotto DJ, Unger RH, Hsia CC. Fatty diabetic lung: functional impairment in a model of metabolic syndrome.. J Appl Physiol (1985) 2010 Dec;109(6):1913-9.
- Schuler B, Arras M, Keller S, Rettich A, Lundby C, Vogel J, Gassmann M. Optimal hematocrit for maximal exercise performance in acute and chronic erythropoietin-treated mice.. Proc Natl Acad Sci U S A 2010 Jan 5;107(1):419-23.
- Hsia CC, Wagner PD, Dane DM, Wagner HE, Johnson RL Jr. Predicting diffusive alveolar oxygen transfer from carbon monoxide-diffusing capacity in exercising foxhounds.. J Appl Physiol (1985) 2008 Nov;105(5):1441-7.
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