, Volume 133, Issue 3, pp 343–350 | Cite as

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

  • Fernanda Menezes de Oliveira e SilvaEmail author
  • Vitor Luz Carvalho
  • Juliana Plácido Guimarães
  • Jociery Einhardt Vergara-Parente
  • Ana Carolina Oliveira de Meirelles
  • Miriam Marmontel
  • Maria Angelica Miglino
Original Paper


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.


Spleen Cetacea Lymphoid system Immune system 



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.


  1. 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 1–79Google Scholar
  2. Cahalane SFN, Kiesselback N (1970) The significance of the accessory spleen. J Pathol 100:139–144. doi: 10.1002/path.1711000209 PubMedCrossRefGoogle Scholar
  3. 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):77–180Google Scholar
  4. Cave AJE (1980) Note on Tursiops visceral histology. In: Pilleri G (ed) Investigations on Cetacea, 11th edn. Der Bund, Beme, pp 11–113Google Scholar
  5. 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 PubMedGoogle Scholar
  6. 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 PubMedCrossRefGoogle Scholar
  7. 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 PubMedPubMedCentralCrossRefGoogle Scholar
  8. 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 CrossRefGoogle Scholar
  9. Fremont RD, Rice TW (2007) Splenosis: a review. South Med J 100(6):589–593. doi: 10.1097/SMJ.0b013e318038d1f8 PubMedCrossRefGoogle Scholar
  10. Geraci JR, Lounsbury VJ (2005) Marine mammals ashore: a field guide for strandings. National Aquarium, BaltimoreGoogle Scholar
  11. 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 PubMedCrossRefGoogle Scholar
  12. Glick B, Sato K (1964) Accessory spleens in the chicken. Poult Sci 43:1610–1612. doi: 10.3382/ps.0431610 CrossRefGoogle Scholar
  13. 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 247–295Google Scholar
  14. Halpert B, Gyorkey F (1959) Lesions observed in accessory spleens of 311 patients. Am J Clin Pathol 32(2):165–168PubMedGoogle Scholar
  15. 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 PubMedCrossRefGoogle Scholar
  16. Herrath E (1935) Bau und Funktion der Milz. Zeitschrift fuX r Zellforschung und mikroskopische Anatomie 23(2):375–429. doi: 10.1007/BF00398953 CrossRefGoogle Scholar
  17. IUCN (2013) The IUCN Red List of Threatened Species. Version 2013.1.>. Accessed 02 November 2013
  18. Janeway CA Jr, Medzhitov R (2002) Innate immune recognition. Annu Rev Immunol 20:197–216. doi: 10.1146/annurev.immunol.20.083001.084359 PubMedCrossRefGoogle Scholar
  19. 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 PubMedCrossRefGoogle Scholar
  20. Lau DTL (1973) Ectopic splenic nodules in the pancreas of a capuchin monkey (Cebus albifrons). J Med Primatol 2:67–70PubMedGoogle Scholar
  21. Nakamine H, Nagata S, Yonezawa M, Tanaka Y (1992) The whale (Odontoceti) spleen: a type of primitive mammalian spleen. Kaibogaku Zasshi 67(2):69–82PubMedGoogle Scholar
  22. 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 15–72Google Scholar
  23. 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 189–193Google Scholar
  24. Press CMcL, Landsverk T (2006) Immune system. In: Eurell JA, Frappier BL (eds) Dellmann’s textbook of veterinary histology. Blackwell Publishing, Ames, pp 134–152Google Scholar
  25. 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 PubMedCrossRefGoogle Scholar
  26. 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 21–30Google Scholar
  27. 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 PubMedCrossRefGoogle Scholar
  28. 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 pGoogle Scholar
  29. 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):61–65PubMedGoogle Scholar
  30. 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 PubMedGoogle Scholar
  31. 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
  32. 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 298–418Google Scholar
  33. Slijper EJ (1958) Organ weights and symmetry problems in porpoises and seals. Archives Neerlandaises de Zoologie 13:97–113Google Scholar
  34. Suttie AW (2006) Histopathology of the spleen. Toxicol Pathol 34(5):466–503. doi: 10.1080/01926230600867750 PubMedCrossRefGoogle Scholar
  35. Swarbrick O (1968) Ectopic splenic nodules in the pancreas of a sow. Br Vet J 124:6–18Google Scholar
  36. 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 PubMedCrossRefGoogle Scholar
  37. 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 PubMedCrossRefGoogle Scholar
  38. Tittel K (2006) Anatomia descritiva e funcional do corpo humano. Santos, São PauloGoogle Scholar
  39. 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 PubMedCrossRefGoogle Scholar
  40. Vejlsted M (2012) Desenvolvimento do sistema imune. In: Hyttel P, Sinowatz F, Vejlsted M (eds) Embriologia Veterinária. Elsevier, Rio de Janeiro, pp 208–215Google Scholar
  41. 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
  42. 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 1:73–75PubMedGoogle Scholar
  43. Zwillenberg HHL (1960) Die mikroskopische Anatomie der Milz der Furchenwale. Archives Neerlandaises de Zoologie 13:595–597Google Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2014

Authors and Affiliations

  • Fernanda Menezes de Oliveira e Silva
    • 1
    • 2
    Email author
  • Vitor Luz Carvalho
    • 3
  • Juliana Plácido Guimarães
    • 1
    • 2
  • Jociery Einhardt Vergara-Parente
    • 2
  • Ana Carolina Oliveira de Meirelles
    • 3
  • Miriam Marmontel
    • 4
  • Maria Angelica Miglino
    • 1
  1. 1.Departamento de Cirurgia, Faculdade de Medicina Veterinária E ZootecniaUniversidade de São PauloSão PauloBrazil
  2. 2.Núcleo de Estudos dos Efeitos Antropogênicos nos Recursos MarinhosFundação Mamíferos AquáticosAracajuBrazil
  3. 3.Programa de Mamíferos MarinhosAssociação de Pesquisa e Preservação de Ecossistemas AquáticosCaucaiaBrazil
  4. 4.Grupo de Pesquisa em Mamíferos Aquáticos AmazônicosInstituto de Desenvolvimento Sustentável MamirauáTeféBrazil

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