Skip to main content
SpringerLink
Log in

Frequency of decompression illness among recent and extinct mammals and “reptiles”: a review

  • Review
  • Published:
The Science of Nature Aims and scope Submit manuscript

Abstract

The frequency of decompression illness was high among the extinct marine “reptiles” and very low among the marine mammals. Signs of decompression illness are still found among turtles but whales and seals are unaffected. In humans, the risk of decompression illness is five times increased in individuals with Patent Foramen Ovale; this condition allows blood shunting from the venous circuit to the systemic circuit. This right-left shunt is characteristic of the “reptile” heart, and it is suggested that this could contribute to the high frequency of decompression illness in the extinct reptiles.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2

Similar content being viewed by others

References

  • Andersson JPA, Biasoletto-Tjellström G, Schagatayet EKA (2008) Pulmonary gas exchange is reduced by the cardiovascular diving response in resting humans. Respir Physiol Neurobiol 160:320–324

    Article  PubMed  Google Scholar 

  • Bajpai S, Gingerich PD (1998) A new Eocene archaeocete (Mammalia, Cetacea) fom India and the time of origin of whales. Proc Natl Acad Sci 95:15464–15468

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Beatty BL, Rothschild BM (2008) Decompression syndrome and the evolution of deep diving physiology in the cetacea. Naturwissenschaften 95:793–801

    Article  CAS  PubMed  Google Scholar 

  • Bell GL (1997) Part IV A phylogenetic revision of North American and Adriatic Mosasauroidea. In: Callaway JM, Nicholls EL (ed) Ancient Marine Reptiles. Academic Press, pp 293–327

  • Benedictis D, Marcucci M (2009) Association between PFO and neurological decompression illness. Ital J Pediatr 35:1

    Article  PubMed  PubMed Central  Google Scholar 

  • Benton MJ (1997) Vertebrate palaeontology. 2nd edition. Chapman & Hall, 452 pp.

  • Berkson H (1967) Physiological adjustments to deep diving in the pacific green turtle (Chelonia mydas agassizii). Comp Biochem Physiol 21:507–524

    Article  CAS  PubMed  Google Scholar 

  • Bernaldo de Quirós Y, Seewald JS, Sylva SP, Greer B, Niemeyer M et al (2013) Compositional discrimination of decompression and decomposition gas bubbles in bycaught seals and dolphins. PLoS One 8(12):e83994

    Article  PubMed  PubMed Central  Google Scholar 

  • Bolte H, Koch A, Tetzlaff K, Bettinghausen E, Heller M, Reuter M (2005) Detection of dysbaric osteonecrosis in military divers using magnetic resonance imaging. Eur Radiol 15:368–375

    Article  CAS  PubMed  Google Scholar 

  • Caldwell MW (1999) Squamate phylogeny and the relationships of snakes and mosasauroids. Zool J Linnean Soc 125:115–147

    Article  Google Scholar 

  • Cartoni D, De Castro S, Valente G, Costanzo C, Pelliccia A, Beni S, DiAngelantonio E, Papetti F, Serdoz LV, Fedele F (2004) Identification of professional scuba divers with patent foramen ovale at risk for decompression illness. Am J Cardiol 94:270–273

    Article  PubMed  Google Scholar 

  • Daniels CB, Orgeig S, Smits AW (1995) The evolution of the vertebrate pulmonary surfactant system. Physiol Zool 68:539–566

    Article  CAS  Google Scholar 

  • Danil K, St. Leger JA, Dennison S, Bernaldo de Quiros Y et al (2014) Clostridium perfringens septicemia in a long-beaked common dolphin Delphinus capensis: an etiology of gas bubble accumulation in cetaceans. Dis Aquat Org 111(3):183–190

    Article  PubMed  Google Scholar 

  • Decompression Sickness Central Registry and Radiological Panel (1981) Aseptic bone necrosis in divers. Lancet 318:384–388

    Article  Google Scholar 

  • Denison DM, Kooyman GL (1973) The structure and function of the small airways in pinniped and sea otter lungs. Respir Physiol 17:l–1

    Article  Google Scholar 

  • Ellis R (2003) Sea dragons. Predators of the prehistoric oceans. University Press of Kansas, 313 pp

  • Emile J, De Bray JM, Bernat M, Morer T, Allain P (1981) Ostearticular complications in bismuth encephalopathy. Clin Toxicol 18(11):1285–1290

    Article  CAS  PubMed  Google Scholar 

  • Fahlman A, Olszowkab A, Bostrom B, Jones DR (2006) Deep diving mammals: dive behavior and circulatory adjustments contribute to bends avoidance. Respir Physiol Neurobiol 153:66–77

    Article  CAS  PubMed  Google Scholar 

  • Fahlman A, Hooker SK, Olszowka A, Bostrom BL, Jones DR (2009) Estimating the effect of lung collapse and pulmonary shunt on gas exchange during breath-hold diving, the Scholander and Kooyman legacy. Respir Physiol Neurobiol 165:28–39

    Article  CAS  PubMed  Google Scholar 

  • Falke KJ, Hill RD, Qvist J, Schneider RC, Guppy M, Liggins GC, Hochachka PW, Elliott RE, Zapol WM (1985) Seal lungs collapse during free diving, evidence from arterial nitrogen tensions. Science 229:556–558

    Article  CAS  PubMed  Google Scholar 

  • Fernandez A, Arbelo M (2013) No mass strandings since sonar ban. Nature 497:317

    Article  CAS  PubMed  Google Scholar 

  • Foot NJ, Orgeig S, Daniels CB (2006) The evolution of a physiological system: the pulmonary surfactant system in diving mammals. Respir Physiol Neurobiol 154:118–138

    Article  CAS  PubMed  Google Scholar 

  • Garcia-Parraga D, Crespo-Picazo JL, Bernaldo de Quiros Y, Cervera V (2014) Decompression sickness (‘the bends’) in sea turtles. Dis Aquat Org 111:191–205

    Article  CAS  PubMed  Google Scholar 

  • Gempp E, Blatteau J-E, Simon O, Stephant E (2009) Musculoskeletal decompression sickness and risk of dysbaric osteonecrosis in recreational divers. Diving Hyperb Med 39(4):200–204

    PubMed  Google Scholar 

  • Germonpre P, Dendale P, Unger P, Balestra C (1998) Patent foramen ovale and decompression sickness in sports divers. J Appl Physiol 84:1622–1626

    CAS  PubMed  Google Scholar 

  • Germonpre P, Hastir F, Dendale P, Marroni A, Nguyen AF, Balestra C (2005) Evidence for increasing patency of the foramen ovale in divers. Am J Cardiol 95:912–915

    Article  PubMed  Google Scholar 

  • Greg PJ, Walder DN (1986) Caisson disease of bone. Clin Othop 210:43–54

    Google Scholar 

  • Hasan SS, Romeo AA (2002) Nontraumatic osteonecrosis of the humeral head. J Shoulder Elb Surg 11(3):281–298

    Article  Google Scholar 

  • Hirayama R (1998) Oldest known sea turtle. Nature 392:705–708

  • Hooker SK, Baird RW, Fahlman A (2009) Could beaked whales get the bends? Effect of diving behaviour and physiology on modelled gas exchange for three species: Ziphius cavirostris, Mesoplodon densirostris and Hyperoodon ampullatus. Respir Physiol Neurobiol 167:235–246

    Article  PubMed  Google Scholar 

  • Hooker SK, Fahlman M, Moore MJ, Aguilar de Soto N et al (2012) Deadly diving? Physiological and behavioural management of decompression stress in diving animals. Proc R Soc B 279:2041–2050

    Article  Google Scholar 

  • Houser DS, Howard R, Ridgway S (2001) Can diving-induced tissue nitrogen supersaturation increase the chance of acoustically driven bubble growth in marine mammals. J Theor Biol 213:183–195

    Article  CAS  PubMed  Google Scholar 

  • Hughes GM (1963) Comparative physiology of vertebrate respiration. Heinemann, Harvard

    Book  Google Scholar 

  • Hutter CDD (2000) Dysbaric osteonecrosis: a reassessment and hypothesis. Med Hypotheses 54(4):585–590

    Article  CAS  PubMed  Google Scholar 

  • Jepson PD, Arbelo M, Deaville R, Patterson IAP et al (2003) Gas-bubble lesions in stranded cetaceans. Was sonar responsible for a spate of whale deaths after an Atlantic military exercise? Nature 425:575–576

    Article  CAS  PubMed  Google Scholar 

  • Johnston RP, Broom JR, Hunt PD, Benton PJ (1996) Patent foramen ovale and decompression illness in divers. Lancet 348:1515

    Article  CAS  PubMed  Google Scholar 

  • Jones JP (2001) Alcoholism, hypercortisonism, fat embolism and osseous avascular necrosis. Clin Orthop 393:4–12

    Article  Google Scholar 

  • Kear BP, Lee MSY (2006) A primitive protostegid from Australia and early sea turtle evolution. Biol Lett 2:116–119

    Article  PubMed  Google Scholar 

  • Kooyman GL (2009) Diving physiology. In: Perrin WF, Wursig B, Thewissen J (eds) Encyclopedia of marine mammals, 2nd edn. Academic Press, San Diego, pp 339–344

    Google Scholar 

  • Laden GD (1997) Patent foramen ovale and decompression illness in divers. Lancet 349:288

    Article  CAS  PubMed  Google Scholar 

  • Laden GDM, Grout P (2004) Aseptic bone necrosis in an amateur scuba diver. Br J Sports Med 38:1–3

    Article  Google Scholar 

  • Lafforgue P (2006) Pathophysiology and natural history of avascular necrosis of bone. Joint Bone Spine 73:500–507

    Article  CAS  PubMed  Google Scholar 

  • Langton P (1996) Patent foramen ovale in underwater medicine. SPUMS 26:186–191

    CAS  Google Scholar 

  • Lee MSY (2005) Molecular evidence and marine snake origins. Biol Lett 1:227–230

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Leith DE (1989) Adaptations to deep breath-hold diving, respiratory and ciculatory mechanics. Undersea Biomed Res 16(5):345–354

    CAS  PubMed  Google Scholar 

  • Libicher M, Appelt A, Berger I, Baier M, Meeder P-J, Grafe I, DaFonseca K, Nöldge G, Kasperk C (2007) The intravertebral vacuum phenomen, compression fractures results from a radiological and histological study. Eur Radiol 17:2248–2252

    Article  PubMed  Google Scholar 

  • Lindholm P, Lundgren CEG (2009) The physiology and pathophysiology of human breath-hold diving. J Appl Physiol 106:284–292

    Article  PubMed  Google Scholar 

  • Liu J, Hu S, Rieppel O, Jiang D et al (2014) A gigantic nothosaur (Reptilia: Sauropterygia) from the Middle Triassic of SW China and its implication for the Triassic biotic recovery. Sci Rep 4(7142):1–9

    Google Scholar 

  • Lutz PL, Bentley TB (1985) Respiratory physiology of diving in the sea turtle. Copeia 1985:671–679

    Article  Google Scholar 

  • Magno L, Lundgren CEG, Ferrigno M (1999) Neurological problems after breath-hold diving. Undersea Hyperbar Med 26(Suppl):28–29

    Google Scholar 

  • McCallum RI, Walder DN (1966) Bone lesions in compressed air workers. J Bone Joint Surg 48B:207–235

    Google Scholar 

  • Milius S (2003) Bad bubbles. Could sonar give whales the bends? Sci News 164:228

    Article  Google Scholar 

  • Miyanischi KY, Ihara H, Naka T, Hirakawa M, Sugioka Y (2006) Risk factors for dysbaric osteonecrosis. Rheumatology 45:855–858

    Article  Google Scholar 

  • Moon RE, Camporesi EM, Kisslo JA (1989) Patent foramen ovale and decompression sickness in divers. Lancet 333:513–514

    Article  Google Scholar 

  • Moore MJ, Early GA (2004) Cumulative sperm whale bone damage and the bends. Science 306:2215

    Article  CAS  PubMed  Google Scholar 

  • Motani R (2005) Evolution of fish-shaped reptiles (Reptilia: Ichthyopterygia) in their physical environments and constraints. Annu Rev Earth Planet Sci 33:395–420

    Article  CAS  Google Scholar 

  • Motani R (2009) The evolution of marine reptiles. Evo Edu Outreach 2:224–235

    Article  Google Scholar 

  • Motani R, Rothschild BM, Wahl WJ (1999) Large eyeballs in diving ichthyosaurs. Nature 402:747 and supplementary information 1-3

    Article  CAS  Google Scholar 

  • Otha Y, Matsunaga H (1974) Bone lesions in divers. J Bone Joint Surg 56B:3–16

    Google Scholar 

  • Paulev P (1965) Decompression sickness following repeated breath-hold dives. J Appl Physiol 20:1028–1031

    CAS  PubMed  Google Scholar 

  • Piccillo GA, Panto A, Manfre L, Mondati EGM, Polosa R, Miele L, Gasbarrini G (2008) Decompression sickness in a sea-hedgehog diver. Oral Commun / Eur J Intern Med 19S:S50

    Article  Google Scholar 

  • Resnick DR, Niwayama G, Guerra J, Vint V, Usselman J (1981) Spinal vacuum phenomena: anatomical study and review. Radiology 139:341–348

    Article  CAS  PubMed  Google Scholar 

  • Rothschild BM (1987) Decompression syndrome in fossil marine turtles. Ann Carnegie Museum 56:253–358

    Google Scholar 

  • Rothschild BM (1990) Absence of decompression syndrome in recent and fossil mammalia and reptilia. Ann Carnegie Museum 59:287–293

    Google Scholar 

  • Rothschild BM (1991) Stratophrenic analysis of avascular necrosis in turtles: affirmation of the decompression syndrome hypothesis. Comp Biochem Physiol 100A:529–535

    Article  Google Scholar 

  • Rothschild BM (2005) What causes lesions in sperm whale bones? Science 308:631–632

    Article  CAS  PubMed  Google Scholar 

  • Rothschild BM, Martin LD (1987) Avascular necrosis: occurrence in diving Cretaceous Mosasaurs. Science 236:75–77

    Article  CAS  PubMed  Google Scholar 

  • Rothschild BM, Martin LD (2005) Mosasaur ascending: the phylogeny of bends. Geol Mijnb 84:341–344

    Article  Google Scholar 

  • Rothschild BM, Naples V (2015) Decompression syndrome and diving behavior in Odontochelys, the first turtle. Acta Palaeontol Pol 60(1):163–167

    Google Scholar 

  • Rothschild BM, Storrs GW (2003) Decompression syndrome in plesiosaurs (Sauropterygia: Reptilia). J Vertebr Paleontol 23:324–328

    Article  Google Scholar 

  • Rybczynski N, Dawson MR, Tedford RH (2009) A semi-aquatic arctic mammalian carnivore from the Miocene epoch and origin of Pinnipedia. Nature 458:1021–1024

    Article  CAS  PubMed  Google Scholar 

  • Scheyer TM, Romano C, Jenks J, Bucher H (2014) Early Triassic marine biotic recovery: the predators’ perspective. PLoS One 9:1–20

    Article  Google Scholar 

  • Schipke JD, Gams E, Kallweit O (2006) Decompression sickness following breath-hold diving. Res Sports Med 14(3):163–178

    Article  CAS  PubMed  Google Scholar 

  • Shinoda S, Hasegawa Y, Kawasaki S, Tagawa N, Iwata H (1997) Magnetic resonance imaging of osteonecrosis in divers comparison with plain radiographs. Skelet Radiol 26:354–359

    Article  CAS  Google Scholar 

  • Steeman M, Hebsgaard MB, Fordyce RE, Ho SYW, Rabosky DL, Nielsen R, Rahbek C, Glenner H, Sørensen MV, Willerslev E (2009) Radiation of extant cetaceans driven by restructuring of the oceans. Syst Biol 58(6):573–585

    Article  PubMed  PubMed Central  Google Scholar 

  • Sykes O, Clark JE (2013) Patent foramen ovale and scuba diving, a practical guide for physicians on when to refer for screening. Extreme Physiol Med 2:10

    Article  Google Scholar 

  • Theodorou DJ (2001) The intravertebral vacuum cleft sign. Radiology 221:787–788

    Article  CAS  PubMed  Google Scholar 

  • Torti SR, Billinger M, Schwerzmann M, Vogel R, Zbinden R, Windecker S, Seiler C (2004) Risk of decompression illness among 230 divers in relation to the presence and size of patent foramen ovale. Eur Heart J 25:1014–1020

    Article  PubMed  Google Scholar 

  • Turner M (1996) Patent foramen ovale and decompression illness in divers. Lancet 348:1515

    Article  CAS  PubMed  Google Scholar 

  • Varghese G, Ravi Kumar R, Verma R, Rao LVV (2010) Long bone radiology and screening for dysbaric osteonecrosis. J Marine Med Soc 12(2):78–80

    Google Scholar 

  • Vaughn PP, Dawson MR (1956) On the occurrence of calcified tympanic membranes in the mosasaur Platecarpus. Trans Kans Acad Sci 59:382–384

    Article  Google Scholar 

  • Wade CE, Hayashi EM, Cashman TM, Beckman EL (1978) Incidence of dysbaric osteonecrosis in Hawaii’s diving fishermen. Undersea Biomed Res 5(2):137–147

    CAS  PubMed  Google Scholar 

  • White FN (1970) Central vascular shunts and their control in reptiles. Fed Proc 29:1149–1153

    CAS  PubMed  Google Scholar 

  • White FN, Hicks JW, Ishimatsu A (1989) Relationship between respiratory state and intracardiac shunts in turtles. Am J Physiol Regul Integr Comp Physiol 256:R240–R247

    CAS  Google Scholar 

  • Wilmshurst P, Ross K (1998) Dysbaric osteonecrosis of the shoulder in a sport scuba diver. Br J Sports Med 32:344–345

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Wilmshurst PT, Byrne JC, Webb-Peploe MM (1989) Relation between interatrial shunts and decompression sickness in divers. Lancet 334:1302–1306

    Article  Google Scholar 

  • Wilmshurst P, Walsh K, Morrison L (1996) Transcatheter occlusion of foramen ovale with a button device after neurological decompression illness in professional divers. Lancet 348:752

    Article  CAS  PubMed  Google Scholar 

  • Witmer LM (1995) The extant phylogenetic bracket and the importance of reconstructing soft tissues in fossils. In: Thomason J. Functional morphology in vertebrate paleontology. Cambridge University Press, pp 19–33

  • Wong RM (1999) Taravana revisited decompression illness after breath-hold diving. SPUMS J 29(3):36–42

    Google Scholar 

  • Wyneken J (2009) Normal reptile heart morphology and function. Vet Clin N Am Exot Anim Pract 12:51–63

    Article  Google Scholar 

Download references

Acknowledgements

I thank Bent Lindow and Gilles Cuny (The Natural History Museum of Denmark) for guiding me during the writing of the manuscript and John Bailey (Department of Geography and Geology – University of Copenhagen) for correcting the English language. I thank Jesper Milan (Geomuseum Faxe, Denmark) for helping me with drawing the figures. I am grateful to the anonymous reviewers for their constructive criticism, which improved the manuscript.

Author information

Authors and Affiliations

  1. The Natural History Museum of Denmark, Øster Voldgade 5-7, DK-1350, Copenhagen K, Denmark

    Agnete Weinreich Carlsen

Authors
  1. Agnete Weinreich Carlsen
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Agnete Weinreich Carlsen.

Additional information

Communicated by: Sven Thatje

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Carlsen, A.W. Frequency of decompression illness among recent and extinct mammals and “reptiles”: a review. Sci Nat 104, 56 (2017). https://doi.org/10.1007/s00114-017-1477-1

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • DOI: https://doi.org/10.1007/s00114-017-1477-1

Keywords

Search

Navigation