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Hematological Changes Arising from Spleen Contraction During Apnea and Altitude in Humans

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Hematological Changes Arising from Spleen Contraction During Apnea and Altitude in Humans Thesis for the degree of Doctorate in Biology, Östersund 2008 HEMATOLOGICAL CHANGES ARISING FROM SPLEEN CONTRACTION DURING APNEA AND ALTITUDE IN HUMANS Matt X. Richardson Supervisors: Prof. Erika Schagatay Dr. Johan Andersson Department of Natural Sciences, Engineering and Mathematics Mid Sweden University, Östersund, Sweden ISSN 1652-893X, Mid Sweden University Doctoral Thesis 57 ISBN 978-91-86073-03-9 Akademisk avhandling som med tillstånd av Mittuniversitetet i Östersund framläggs till offentlig granskning för avläggande av doktorsexamen i Biologi, den 19e september 2008, kl. 10 i sal F234, Ridhuset, Mittuniversitetet, Östersund. Seminariet kommer att hållas på engelska. HEMATOLOGICAL CHANGES ARISING FROM SPLEEN CONTRACTION DURING APNEA AND ALTITUDE IN HUMANS Matt X. Richardson © Matt X. Richardson, 2008 Department of Natural Sciences, Engineering and Mathematics Mid Sweden University, Östersund Sweden Telephone: +46 (0)771-975 000 Printed by Kopieringen Mid Sweden University, Sundsvall, Sweden, 2008 Cover photographs by Annelie Pompe (World freediving championships, Egypt) and Mike Callaghan (Lobuche Peak, Nepal). i HEMATOLOGICAL CHANGES ARISING FROM SPLEEN CONTRACTION DURING APNEA AND ALTITUDE IN HUMANS Matt X. Richardson Department of Natural Sciences, Engineering and Mathematics Mid Sweden University, Östersund, Sweden ISSN 1652-893X, Mid Sweden University Doctoral Thesis 57; ISBN 978-91-86073-03-9 ABSTRACT The spleen acts as a storage site for red blood cells, and contraction of the spleen is for many mammals a way of coping with situations where increased blood oxygen storage is beneficial. This ability has also recently been found in humans, where most individuals respond with an increase in circulating erythrocytes in response to environmental or physiological stress, the majority of which can be attributed to the spleen. The initiation of this response, however, is unclear, as is the variability of the response’s development among individuals. This thesis identifies that there is a strong correlation between spleen contraction and circulating hemoglobin (Paper I), that release of these erythrocytes from the spleen is more pronounced in those trained in breath-hold diving than in elite cross-country skiers and untrained persons (Paper II), and that the response develops even in oxygen-poor environments such as at high altitude (Paper III). This is due to the hypoxic stimulus that exists such environments, which acts as an initiator of the response (Paper IV), although even high levels of carbon dioxide are important (Paper V). The size of world championship apnea divers’ spleens is also predictive of their apneic performance, showing that spleen contraction is an important factor in natural diving ability (Paper VI). In conclusion, the contractile response of the spleen, along with the previously described “diving response” helps humans to better endure low-oxygen situations, but despite their common function these responses are not initiated and do not develop in the same manner (Paper VII). Keywords: hypoxia, hypercapnia, hemoglobin, hematocrit, breath-hold diving ii SAMMANDRAG Mjälten innehåller ett extra lager av röda blodkroppar, och mjälteskontraktion är ett sätt för många däggdjur att anpassa sig till situationer där en ökad lagring av syre i blodet är en fördel. Denna förmåga har relativt nyligen upptäckts hos människan där flesta personer svarar på fysiologisk eller omgivningsrelaterad stress med en ökning av mängden erytrocyter i cirkulationen vilket till stor del antas komma från mjälten. Det är dock inte känt hur responsen startas och varför den är olika väl utvecklad hos olika personer. Denna avhandling visar att det finns ett nära samband mellan mjälteskontraktionen och blodets Hb (Paper I), att utsöndring av erytrocyter är större bland tränade apnédykare än bland elitskidåkare och otränade personer (Paper II) och att responsen uppstår även i syrefattig miljö t ex på hög höjd (Paper III). Det beror på att syrebristen i sig är en viktig stimulus för att initiera responsen (Paper IV), men även höjd koldioxidnivån är en viktig faktor (Paper V). En korrelation upptäcktes mellan storleken på apnédykares mjältar och deras resultat på ett världsmästerskap vilket visar att mjälteskontraktionen är viktig för människans naturliga dykförmåga (Paper VI). Slutsatsen är att mjältesresponsen tillsammans med den tidigare beskrivna ”dykresponsen” hjälper oss att bättre klara perioder med syrebrist, och att dessa responser samverkar funktionellt men inte startas på samma sätt (Paper VII). Nyckelord: hypoxi, hyperkapni, hemoglobin, hematokrit, apnédykning iii TABLE OF CONTENTS ABSTRACT ..............................................................................................................................II SAMMANDRAG...................................................................................................................III TABLE OF CONTENTS......................................................................................................IV LIST OF PAPERS ..................................................................................................................VI INTRODUCTION.................................................................................................................... 1 What is apnea?.................................................................................................................... 1 What is hypobaria?............................................................................................................. 4 Differences in adaptation to hypoxia in humans .............................................................. 4 Morphology of the spleen................................................................................................... 5 Functions of the spleen....................................................................................................... 6 Contraction of the spleen in non-human species.............................................................. 8 Contraction of the spleen in humans............................................................................... 10 Initiation of spleen contraction........................................................................................ 11 Effects of the spleen on cardiovascular function............................................................ 13 AIM OF THE THESIS.......................................................................................................... 14 METHODS.............................................................................................................................. 14 MEASUREMENT OF BLOOD VARIABLES................................................................................. 14 Venous capillarisation for Hb/Hct................................................................................... 14 MEASUREMENT OF SPLEEN SIZE............................................................................................ 15 MEASUREMENT OF OTHER PARAMETERS.............................................................................. 16 Arterial oxygen saturation ............................................................................................... 16 Mean arterial pressure..................................................................................................... 17 Skin blood flow.................................................................................................................. 17 Respiration and gases....................................................................................................... 18 APNEA AND HYPOXIA EXPERIMENTAL PROTOCOLS ............................................................. 19 Apnea series ...................................................................................................................... 19 Inspired gases and hyperventilation................................................................................ 20 STATISTICAL APPROACHES.................................................................................................... 20 Publication statistical analysis method........................................................................... 20 Additional statistical analysis method............................................................................. 21 SUMMARY OF RESULTS ................................................................................................. 23 OCCURRENCE OF SPLEEN CONTRACTION.............................................................................. 23 iv INITIATION OF SPLEEN CONTRACTION .................................................................................. 25 CONSEQUENCES AND APPLICATIONS OF SPLEEN CONTRACTION ......................................... 27 DISCUSSION.......................................................................................................................... 28 OCCURRENCE OF SPLEEN CONTRACTION.............................................................................. 28 INITIATION OF SPLEEN CONTRACTION .................................................................................. 29 Stimulus detection by chemoreception ............................................................................ 30 Output following chemoreception.................................................................................... 31 Other potential output mechanisms................................................................................. 34 CONSEQUENCES AND APPLICATIONS OF SPLEEN
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