SPECIAL ARTICLE European Heart Journal 2014 35 2322 2332 doi 10 1093 eurheartj ehu222 Is our heart a well designed pump The heart along animal evolution Dominique A Bettex1 Rene Pre tre 2 and Pierre Guy Chassot 3 1 Anesthesiology University Hospital Zu rich Ra mistrasse 100 Zurich ZH 8091 Switzerland 2Cardiac Surgery University Hospital of Lausanne Lausanne Switzerland and Anesthesiology University Hospital of Lausanne Lausanne Switzerland 3 Received 4 February 2014 revised 14 April 2014 accepted 7 May 2014 online publish ahead of print 10 June 2014 Keywords Animal evolution Heart anatomy Haemodynamics Translational perspective To assess if our heart is a good pump we should study the heart along the animal evolution From the worms through the arthropods the mollusks and the reptiles to the vertebrates and the birds the heart has followed a logical evolution which brought it to our own complex physiology This evolution allowed the passage from submarine to terrestrial life and offered different cardiovascular solutions to complex adaptive problems Facing ventricular failure we might wonder if our heart is really a good pump A possible answer to this question can be found by looking back at animal evolution Nature has experimented many different circulatory systems By comparing human heart with these various achievements we might evaluate the pump inherited from our animal ancestors The tree of evolution The animal evolution is classically represented as a tree rooted on the first eukaryotic cells appeared 1 5 billion years ago Figure 1 1 2 After 700 million years emerged organized animals with a radial symmetry sponges jellyfish followed by creatures with a bilateral symmetry and a dorsoventral axis These Bilateria gave two divergent branches Protostoma invertebrates and Deuterostoma vertebrates 3 The first tubular heart appeared probably in Bilateria 4 The embryogenesis shows that animals share a common step consisting in a primary cardiac tube derived from mesodermal precursors converging at the midline 5 with peristaltic movements pushing fluid into pericellular spaces without vessels 3 As long as living beings were only small clusters of cells simple diffusion was adequate But as soon as the organisms grew in size a carrying system became mandatory to transport O2 and nutrients and to remove waste products There are two possible configurations Open system high output but low pressure like a fan in a room well performing over short distances used in the peripheral circulation of worms or insects Blood lymph and extracellular fluid are mixed together haemolymph flow from arteries into the interstitial space and are directed into venous collectors The volume of circulating fluid is large 20 50 of body weight and its velocity is low Corresponding author Email dominique bettex usz ch Published on behalf of the European Society of Cardiology All rights reserved The Author 2014 For permissions please email journals permissions oup com Downloaded from by guest on October 22 2014 A carrier system for gases and nutrients became mandatory when primitive animals grew larger and developed different organs The first circulatory systems are peristaltic tubes pushing slowly the haemolymph into an open vascular tree without capillaries worms Arthropods developed contractile bulges on the abdominal aorta assisted by accessory hearts for wings or legs and by abdominal respiratory motions Two chamber heart atrium and ventricle appeared among mollusks Vertebrates have a multi chamber heart and a closed circulation with capillaries Their heart has two chambers in fishes three chambers two atria and one ventricle in amphibians and reptiles and four chambers in birds and mammals The ventricle of reptiles is partially divided in two cavities by an interventricular septum leaving only a communication of variable size leading to a variable shunt Blood pressure increases progressively from 15 mmHg worms to 170 70 mmHg birds according to the increase in metabolic rate When systemic pressure exceeds 50 mmHg a lower pressure system appears for the circulation through gills or lungs in order to improve gas exchange A four chamber heart allows a complete separation of systemic and pulmonary circuits This review describes the circulatory pumping systems used in the different classes of animals their advantages and failures and the way they have been modified with evolution 2323 Is our heart a well designed pump Downloaded from by guest on October 22 2014 Figure 1 Illustration of a simplified tree of evolution Blue arrows invertebrates Red arrows vertebrates reproduced from Chassot et al 43 Closed system moving blood rapidly over long distances inside arteries capillaries and veins lined with endothelial cells used in cephalopods octopus and in all vertebrates Blood volume is lower 6 8 of body weight but pressure is higher The presence of an O2 carrier pigment increases O2 delivery 20 40 times Haeme pigments are found in practically all classes of living beings They evolved from enzymes such as cytochromes primarily used to detoxify oxygen when it appeared in atmosphere with photosynthesis 6 Haemocyanin is a copper containing molecule giving a greenish colour to the blood of mollusks crustaceans and some arachnids existing only in solution and transporting 4 5 vol of O2 7 Haemoglobin is more efficient It is present in all vertebrates but locked inside erythrocytes this allows an increase in concentration and a decrease in toxicity Lower invertebrates Worms have two peristaltic tubes one dorsal where the blood is pumped forwards and one ventral where it flows backwards Distally the system is open with no capillaries These vessels carry haemolymph between the tissues and the skin where gas exchange takes place The perfusion is slow six to eight peristaltic waves per minute and the pressure is low 10 20 mmHg The most evolved among them have an iron containing pigment and a peristaltic dorsal vessel pushing blood pressure 20 mmHg towards five pairs of lateral hearts in the five frontal segments When they contract these accessory hearts push blood into the ventral vessel at a pressure up to 70 mmHg 8 Arthropods Insects have a series of pulsatile abdominal bulbs along the aorta Their synchronized contraction 300 600 b p m initiated near the blind caudal extremity propels blood in the anterior direction at a low pressure 20 10 mmHg 9 The filling of these hearts in diastole is achieved by suction provided by the
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