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Accessory spleen in cetaceans and its relevance as a secondary lymphoid organ

Abstract

The objective was to determine the prevalence of accessory spleens in cetaceans stranded on the north and northeastern coasts of Brazil and to describe their macroscopic and microscopic characteristics, thereby providing insights into the contribution of these structures to the immune system of cetaceans. Sixty-three Odontocetes and Mysticetes (total of 14 species), male and female, ranging from calves to adults, stranded from 2009 to 2013 on the Brazilian north and northeastern coasts, were evaluated. Accessory spleens were present in 38 animals (60.3 %), with 1–14 accessory spleens per animal. Their location varied among species, ranging from firmly adherent to the spleen, to the large curvature of the first stomach or both. The presence of these structures was apparently not related to age or sex. However, there was a higher prevalence in animals with a greater body size and known to make deeper dives. Both primary and accessory spleens had similar macroscopic morphology with no demarcation between cortex and medulla. Both primary and accessory spleens had similar histological characteristics. Furthermore, it was noteworthy that germinal centers became more discrete and reduced in number with increasing age. In conclusion, we inferred that accessory spleens may be an additional mechanism for adaptation to diving and that they have a complementary reservoir function and thus can be considered compensatory lymphoid organs to splenic activity.

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References

  • Bryden MM (1972) Growth and development of marine mammals. In: Harrison RJ (ed) Functional anatomy of marine mammals, 1st edn. Academic Press, New York, pp 1–79

    Google Scholar 

  • Cahalane SFN, Kiesselback N (1970) The significance of the accessory spleen. J Pathol 100:139–144. doi:10.1002/path.1711000209

    CAS  PubMed  Article  Google Scholar 

  • Carvalho VL, Motta MR, Nunes-Pinheiro DCS, Nogueira TNAG, Campello CC (2009) Ocorrência de baços acessórios em boto-cinza (Sotalia guianensis)—aspectos histológicos. Acta Sci Vet 37(2):77–180

    Google Scholar 

  • Cave AJE (1980) Note on Tursiops visceral histology. In: Pilleri G (ed) Investigations on Cetacea, 11th edn. Der Bund, Beme, pp 11–113

    Google Scholar 

  • Clark LS, Turner JP, Cowan DF (2005) Involution of lymphoid organs in bottlenose dolphins (Tursiops truncatus) from the Western Gulf of Mexico: implications for life in an aquatic environment. Anat Rec A Discov Mol Cell Evol Biol 282(1):67–73. doi:10.1002/ar.a.20147

    PubMed  Google Scholar 

  • Connell NT, Brunner AM, Kerr CA, Schiffman FJ (2011) Splenosis and sepsis. The born-again spleen provides poor protection. Virulence 2(1):4–11. doi:10.4161/viru.2.1.14611

    PubMed  Article  Google Scholar 

  • Cowan DF, Smith TL (1999) Morphology of the lymphoid organs of the bottlenose dolphin, Tursiops truncatus. J Anat 194:505–517. doi:10.1046/j.1469-7580.1999.19440505.x

    PubMed  PubMed Central  Article  Google Scholar 

  • Fox RR, Weisbroth SH, Crary DD, Scher S (1976) Accessory spleens in domestic rabbits (Oryctolagus cuniculus). I. Frequency, description and genetic factors. Teratology 13(3):243–251. doi:10.1002/tera.1420130302

    Article  Google Scholar 

  • Fremont RD, Rice TW (2007) Splenosis: a review. South Med J 100(6):589–593. doi:10.1097/SMJ.0b013e318038d1f8

    PubMed  Article  Google Scholar 

  • Geraci JR, Lounsbury VJ (2005) Marine mammals ashore: a field guide for strandings. National Aquarium, Baltimore

    Google Scholar 

  • Gigot JF, Jamar F, Ferrant A, van Beers BE, Lengele B, Pauwels S, Pringot J, Kestens PJ, Gianello P, Detry R (1998) Inadequate detection of accessory spleens and splenosis with laparoscopic splenectomy. A shortcoming of the laparoscopic approach in hematologic disease. Surg Endosc 12:101–106. doi:10.1007/s004649900607

    CAS  PubMed  Article  Google Scholar 

  • Glick B, Sato K (1964) Accessory spleens in the chicken. Poult Sci 43:1610–1612. doi:10.3382/ps.0431610

    Article  Google Scholar 

  • Green RF (1972) Observations on the anatomy of some cetaceans and pinnipeds. In: Ridgway SH (ed) Mammals of the sea: biology and medicine. Charles C, Thomas, pp 247–295

    Google Scholar 

  • Halpert B, Gyorkey F (1959) Lesions observed in accessory spleens of 311 patients. Am J Clin Pathol 32(2):165–168

    CAS  PubMed  Google Scholar 

  • Hartwig H, Hartwig HG (1985) Structural characteristics of the mammalian spleen indicating storage and release of red blood cells. Aspects of evolutionary and environmental demands. Experientia 41(2):159–163. doi:10.1007/BF02002608

    CAS  PubMed  Article  Google Scholar 

  • Herrath E (1935) Bau und Funktion der Milz. Zeitschrift fuX r Zellforschung und mikroskopische Anatomie 23(2):375–429. doi:10.1007/BF00398953

    Article  Google Scholar 

  • IUCN (2013) The IUCN Red List of Threatened Species. Version 2013.1. http://www.iucnredlist.org>. Accessed 02 November 2013

  • Janeway CA Jr, Medzhitov R (2002) Innate immune recognition. Annu Rev Immunol 20:197–216. doi:10.1146/annurev.immunol.20.083001.084359

    CAS  PubMed  Article  Google Scholar 

  • Jeneby MM, Langoi D, Mwenda JM, Chai D (2003) Ectopic splenic nodules in the olive baboon (Papio cynocephalus anubis). J Med Primatol 32(2):120–122. doi:10.1034/j.1600-0684.2003.00001.x

    CAS  PubMed  Article  Google Scholar 

  • Lau DTL (1973) Ectopic splenic nodules in the pancreas of a capuchin monkey (Cebus albifrons). J Med Primatol 2:67–70

    CAS  PubMed  Google Scholar 

  • Nakamine H, Nagata S, Yonezawa M, Tanaka Y (1992) The whale (Odontoceti) spleen: a type of primitive mammalian spleen. Kaibogaku Zasshi 67(2):69–82

    CAS  PubMed  Google Scholar 

  • Pabst DA, Rommel SA, Mclellan WA (1999) Functional anatomy of marine mammals. In: Reynolds JE, Rommel SA (eds) Biology of marine mammals. Smithsonian Institution Press, Washington, pp 15–72

    Google Scholar 

  • Pilleri G, Arvy L (1971) Aselli’s pseudopancreas (nodi lymphatici mesenterici) in two delphinids: Delphinus delphis and Stenella coeruleoalba. In: Pilleri G (ed) Investigations on Cetacea, 3rd edn. Der Bund, Berne, pp 189–193

    Google Scholar 

  • Press CMcL, Landsverk T (2006) Immune system. In: Eurell JA, Frappier BL (eds) Dellmann’s textbook of veterinary histology. Blackwell Publishing, Ames, pp 134–152

    Google Scholar 

  • Ramírez GA, Altimira J, García-González B, Vilafranca M (2013) Intrapancreatic ectopic splenic tissue in dogs and cats. J Comp Pathol 148(4):361–364. doi:10.1016/j.jcpa.2012.08.006

    PubMed  Article  Google Scholar 

  • Reynolds JE III, Rommel SA, Bolen ME (2002) Anatomical dissection: thorax and abdomen. In: Perrin WF, Würsig B, Thewissen HGM (eds) Encyclopedia of marine mammals. Academic Press, San Diego, pp 21–30

    Google Scholar 

  • Romano TA, Felten SY, Olschowka JA, Felten DL (1993) A microscopic investigation of the lymphoid organs of the beluga Delphinapterus leucas. J Morphol 215(3):261–287. doi:10.1002/jmor.1052150307

    CAS  PubMed  Article  Google Scholar 

  • Romano TA, Abella K, Cowan D, Curry B (2002) Investigation of the morphology and autonomic innervation of the lymphoid organs in the pantropical spotted, spinner, and common dolphins (Stenella attenuata, Stenella longirostris and Delphinus delphis) incidentally entangled and drowned in the tuna purse-seine fishery in the eastern tropical Pacific. La Jolla. Administrative Report. Southwest Fisheries Science Center, National Marine Fisheries Service, 25 p

  • Romer T, Wiesner W (2012) The accessory spleen: prevalence and imaging findings in 1,735 consecutive patients examined by multidetector computed tomography. JBR-BTR 95(2):61–65

    CAS  PubMed  Google Scholar 

  • Rossi F, Rabba S, Vignoli M, Haers H, Terragni R, Saunders JH (2010) B-mode and contrast-enhanced sonographic assessment of accessory spleen in the dog. Vet Radiol Ultrasound 51(2):173–177. doi:10.1111/j.1740-8261.2009.01647.x

    PubMed  Google Scholar 

  • Silva FMO, Guimarães JP, Vergara-Parente JE, Carvalho VL, Meirelles ACO, Marmontel M, Ferrão JSP, Miglino MA (2014) Morphological analysis of lymph nodes in Odontocetes from north and northeast coast of Brazil. Anat Rec (Hoboken). doi:10.1002/ar.22871

  • Simpson JG, Gardner MB (1972) Comparative microscopic anatomy of selected marine mammals. In: Ridgway SH (ed) Mammals of the sea. Biology and Medicine. Charles C, Thomas, pp 298–418

    Google Scholar 

  • Slijper EJ (1958) Organ weights and symmetry problems in porpoises and seals. Archives Neerlandaises de Zoologie 13:97–113

    Google Scholar 

  • Suttie AW (2006) Histopathology of the spleen. Toxicol Pathol 34(5):466–503. doi:10.1080/01926230600867750

    PubMed  Article  Google Scholar 

  • Swarbrick O (1968) Ectopic splenic nodules in the pancreas of a sow. Br Vet J 124:6–18

    Google Scholar 

  • Tanaka Y (1994) Microscopy of vascular architecture and arteriovenous communications in the spleen of two odontocetes. J Morphol 221(2):211–233. doi:10.1002/jmor.1052210210

    CAS  PubMed  Article  Google Scholar 

  • Timens W (1991) The human spleen and the immune system: not just another lymphoid organ. Res Immunol 142(4):316–320. doi:10.1016/0923-2494(91)90081-S

    CAS  PubMed  Article  Google Scholar 

  • Tittel K (2006) Anatomia descritiva e funcional do corpo humano. Santos, São Paulo

    Google Scholar 

  • Unver Dogan N, Uysal II, Demirci S, Dogan KH, Kolcu G (2011) Accessory spleens at autopsy. Clin Anat 24(6):757–762. doi:10.1002/ca.21146

    PubMed  Article  Google Scholar 

  • Vejlsted M (2012) Desenvolvimento do sistema imune. In: Hyttel P, Sinowatz F, Vejlsted M (eds) Embriologia Veterinária. Elsevier, Rio de Janeiro, pp 208–215

    Google Scholar 

  • Yildiz AE, Ariyurek MO, Karcaaltincaba M (2013) Splenic anomalies of shape, size, and location: pictorial essay. Sci World J 2013:321810. doi:10.1155/2013/321810

    Google Scholar 

  • Yoon Y, Shin J, Park C, Oh Y, Lee I, Lee HS, Lee J (2000) Morphological structure of accessory spleen in Chinese hamsters. J Vet Sci 1:73–75

    CAS  PubMed  Google Scholar 

  • Zwillenberg HHL (1960) Die mikroskopische Anatomie der Milz der Furchenwale. Archives Neerlandaises de Zoologie 13:595–597

    Google Scholar 

Download references

Acknowledgments

This study was funded by Fundação de Pesquisa do Estado de Sao Paulo—FAPESP (Process 2012/01964-0). We thank institutions Fundação Mamíferos Aquáticos—FMA, Associação de Pesquisa e Preservação de Ecossistemas Aquáticos—AQUASIS and Instituto de Desenvolvimento Sustentável Mamirauá—IDSM for providing samples that are used in this study. We greatly appreciate the assistance of Prof. John Kastelic in the correction of the English language in this Article. This paper employed data generated by Programa Regional de Monitoramento de Encalhes e Anormalidades na Área de Abrangência da Bacia Sergipe-Alagoas and carried out by Fundação Mamíferos Aquáticos and Petrobras, in partnership with Projeto Tamar/ICMBio, as a mitigating measure of the Federal Environmental Licensing conducted by the Brazilian Environmental Agency (IBAMA). Samples collected by IDSM’s Aquavert Project and AQUASIS’s Projeto Manatí were sponsored by Petrobras through its Petrobras Ambiental Program.

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Correspondence to Fernanda Menezes de Oliveira e Silva.

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Communicated by A. Schmidt-Rhaesa.

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e Silva, F.M.O., Carvalho, V.L., Guimarães, J.P. et al. Accessory spleen in cetaceans and its relevance as a secondary lymphoid organ. Zoomorphology 133, 343–350 (2014). https://doi.org/10.1007/s00435-014-0223-x

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  • DOI: https://doi.org/10.1007/s00435-014-0223-x

Keywords

  • Spleen
  • Cetacea
  • Lymphoid system
  • Immune system