brief communications arising

Pathology nitrogen supersaturation in the tissues of diving cetaceans are normally insufficient to Whales, sonar and decompression sickness initiate bubble formation, a theoretical pos- Arising from: Jepson, P. D. et al. Nature 425, 575–576 (2003). sibility remains that cetaceans with nitrogen- supersaturated tissues could experience e do not yet know why whales cetaceans that they investigated, even when bubble growth or formation as a result of occasionally strand after sonar has the body’s gas burden is very large. Bubbles intense acoustic exposure4,5. There was a Wbeen deployed nearby, but such have been observed in hepatic sinusoids and clear spatial and temporal link with active information is important for both naval in the portal vein, but large encapsulated naval sonar exposure in the case of the undersea activities and the protection of bubbles have not been reported6.Liver beaked whales in the Canary Islands, as well marine mammals. Jepson et al. suggest that lesions are equally unexpected in ‘recurrent’ as in previously reported beaked-whale a peculiar gas-forming disease afflicting DCS, in which chronic lesions are found strandings 6,7. some stranded cetaceans could be a type of only in the long bones and the central The lesions in the Canary Island beaked decompression sickness (DCS) resulting nervous system. It is unlikely that fibrotic whales and in the UK cases (mainly dol- from exposure to mid-range sonar1.How- hepatic lesions of the type described by Jep- phins) differed. The beaked whales had ever, neither decompression theory nor son et al.,which would require days or weeks acute, systemic and widely disseminated observation support the existence of a natu- to develop, could be caused by a brief expo- lesions consistent with, although not diag- rally occurring DCS in whales that is char- sure to sonar. nostic of, DCS8. The large hepatic cavities acterized by encapsulated, gas-filled cavities We agree with Jepson et al. that further found exclusively in the UK cases are atypical in the liver. Although gas-bubble formation investigation is needed,including an analysis of DCS in humans and experimental ani- may be aggravated by acoustic energy, more of the composition of the gas in the bubbles. mals. For logistical reasons, the central ner- rigorous investigation is needed before But we believe that identifying the cetacean vous system was examined in only two UK sonar can be firmly linked to bubble forma- gas disease with DCS is premature because cases and the bones were not examined in tion in whales. its pathology not only differs from that any. We cannot therefore confirm or refute On the basis of the available information, underlying the syndrome in other mam- the presence of lesions consistent with gas the DCS hypothesis of Jepson et al. contains mals, but it also cannot be explained by any embolism in bone or the central nervous sys- two flaws. First, whales do not develop suffi- physiological mechanism related to diving. tem. However, large numbers of gas bubbles cient gas supersaturation in the tissues on Claude A. Piantadosi, Edward D. Thalmann were seen in portal veins and sinusoids in the ascent to cause extensive bubble formation Center for Hyperbaric Medicine and Environmental livers from all UK cases examined micro- in the liver.The gas available for supersatura- Physiology, Duke University Medical Center, scopically,consistent with DCS in humans8. tion is limited to that present in the lungs Durham, North Carolina 27710, USA As cetaceans differ from humans behav- at the onset of each held breath. During e-mail: [email protected] iourally (as obligate, repetitive breath-hold descent, the thorax is compressed2, and the doi:10.1038/nature02527 divers),physiologically (for example,in their 9 residual gas volume in the compliant lungs is 1. Jepson, P. D. et al. Nature 425, 575–576 (2003). diving reflex) and anatomically (as in their forced, by Boyle’s law contraction and alveo- 2. Williams, T. M. et al. Science 288, 133–136 (2000). retia mirabilia, large portal veins and 3. Houser, D. S., Howard, R. & Ridgway, S. J. Theor. Biol. 213, 10,11 lar collapse, into non-respiratory conduct- 183–195 (2001). diaphragmatic sphincters) , it may be too ing airways, where it is sequestered from the 4. Falke, K. J. et al. Science 229, 556–558 (1985). simplistic to assume that the distribution, circulation3. Not enough gas is taken up to 5. Kooyman, G. L. & Ponganis, P. J. Annu. Rev. Physiol. 60, 19–32 severity and chronicity of lesions induced by produce bubbles, except possibly during (1998). gas emboli will be similar in both human 6. Francis, T. J. R. & Mitchell, S. J. in Bennett and Elliott’s Physiology multiple rapid dives to depths approaching and Medicine of Diving (eds Brubakk, A. O. & Neuman, T. S.) divers and free-living cetaceans. Extensive 3 that of the lung’s closing volume . 5th edn 530–556 (Saunders, Philadelphia, 2003). sublethal bubble formation in human DCS Once nitrogen uptake is blocked by lung is an acute medical emergency. Without collapse, the partial pressure of nitrogen in medical intervention, a free-living cetacean the bloodactually decreases for the rest of the Jepson et al. reply — We did not, as Pianta- suffering the same fate would continue div- dive as nitrogen is distributed to tissues4. dosi and Thalmann suggest1, present our ing for days, weeks or months afterwards However,nitrogen accumulation in the liver, findings as conclusive evidence of decom- unless death or stranding intervened. intestines and other visceral organs is limited pression sickness (DCS). We stated neither Lesion pathogenesis in the stranded by the diving response,which directs arterial that DCS occurs naturally in cetaceans, nor cetaceans2 may ultimately be explained by blood away from these organs to the brain that exposure to active sonar increases its bubble formation, possibly in response to and heart5.On ascent,bubbles leaving super- occurrence2. However, we restate that there either rapid decompression or acoustic expo- saturated tissues must enter the venous is now a generally accepted link between sure of nitrogen-supersaturated tissues5; blood and return to the lungs.These bubbles some beaked-whale strandings and sonar however,it is not clear how marine mammals cannot pass into the liver (except in the use, and that lesions in some cetaceans mitigate the accumulation of nitrogen gas unlikely event that they are of portal origin) demonstrate that in vivo bubble formation while diving and defend themselves against unless they bypass the lung, which serves (embolus) can occur and persist. nitrogen-bubble formation.These uncertain- as a bubble trap. Jepson et al. do not explain Progressively increasing concentrations ties do indeed argue for caution in interpret- why DCS, if it did occur in the whales they of nitrogen in cetacean tissues after repetitive ing the limited studies available. investigated, should affect the liver dispro- diving have been studied empirically in A. Fernández*, M. Arbelo, R. Deaville, portionately. bottlenose dolphins (Tursiops truncatus)3 I. A. P.Patterson, P.Castro, J. R. Baker, Second, large gas-filled cavities in the and higher levels are predicted for northern E. Degollada, H. M. Ross, P.Herráez, liver, many encapsulated in dense fibrous bottlenose whales (Hyperoodon ampullatus) A. M. Pocknell, E. Rodríguez, F. E. Howie, tissue, are inconsistent with the pathology on the basis of their rate of descent or ascent A. Espinosa, R. J. Reid, J. R. Jaber, V.Martin, of DCS in humans and other mammals in and depth of diving4. Nitrogen supersatura- A. A. Cunningham, P.D. Jepson which the bones, joints, lungs and central tion could be further increased by an acceler- *Histology and Pathology Unit, Institute for Animal nervous system are primarily affected. The ated rate of ascent,possibly to a critical point Health, Veterinary School, Montana liver is rarely involved, and never to the where bubbles form. Cardones–Arucas, University of Las Palmas de Gran extent described by Jepson et al. in the Even if naturally occurring levels of Canaria, Gran Canaria, Spain

NATURE | 15 APRIL 2004 | www.nature.com/nature © 2004 Nature Publishing Group 1 brief communications arising e-mail: [email protected] Interim_Bahamas_Report.pdf (2001). doi:10.1038/nature02528 7. Frantzis, A. Nature 392, 29 (1998). 8. Francis, T. J. R. & Mitchell, S. J. in Bennett and Elliott’s Physiology 1. Piantadosi, C. A. & Thalmann, E. D. Nature and Medicine of Diving (eds Brubakk, A. O. & Neuman, T. S.) doi:10.1038/nature02527 (2004). 5th edn 530–556 (Saunders, Philadelphia, 2003). 2. Jepson, P. D. et al. Nature 425, 575–576 (2003). 9. Ridgway, S. H. in Mammals of the Sea: Biology and Medicine (ed. 3. Ridgway, S. H. & Howard, R. Science 206, 1182–1183 (1979). Ridgway, S. H.) 590–747 (Thomas, Springfield, Illinois, 1972). 4. Houser, D. S., Howard, R. & Ridgway, S. H. J. Theor. Biol. 213, 10.Harrison, R. J. & Tomlinson, D. W. Proc. Zool. Soc. Lond. 126, 183–195 (2001). 205–233 (1956). 5. Crum, L. A. & Mao, Y. J. Acoust. Soc. Am. 99, 2898–2907 (1996). 11.Simpson, J. G. & Gardener, M. B. in Mammals of the Sea: Biology 6. US Department of Commerce and US Navy Joint Interim Report and Medicine (ed. Ridgway, S. H.) 298–418 (Thomas, http://www.nmfs.noaa.gov/prot_res/overview/ Springfield, Illinois, 1972).

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