Skip to main content

Advertisement

Log in

Persistent Organic Pollutant and Hormone Levels in Harbor Porpoise with B Cell Lymphoma

  • Published:
Archives of Environmental Contamination and Toxicology Aims and scope Submit manuscript

Abstract

B-cell lymphoma, a common morphologic variant of non-Hodgkin lymphoma, has been associated with persistent pollutants in humans, but this association is not well-characterized in top-level predators sharing marine resources with humans. We characterized and compared blubber contaminants and hormones of a pregnant harbor porpoise (Phocoena phocoena) with B-cell lymphoma, with those in two presumed healthy fishery by-caught porpoises with no lymphoma: a pregnant adult and female juvenile. Common historic use compounds, including polychlorinated biphenyls, polybrominated diphenyl ethers, and pesticides, were evaluated in blubber samples from three porpoises. In addition, blubber cortisol and progesterone levels (ng/g) were determined in all three animals. Total pollutant concentrations were highest in the juvenile porpoise, followed by the lymphoma porpoise and the nonlymphoma adult. Blubber cortisol concentrations were 191% greater in the pregnant with lymphoma porpoise compared with the pregnant no lymphoma porpoise, and 89% greater in the juvenile female compared with the pregnant no lymphoma porpoise. Although both adults were pregnant, progesterone levels were substantially greater (90%) in the healthy compared with the lymphoma adult. Health monitoring of top-level marine predators, such as porpoise, provides a sentinel measure of contaminants that serve as indicators of potential environmental exposure to humans.

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

Access this article

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

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4

Similar content being viewed by others

References

  • Belles-Isles M, Ayotte P, Dewailly É, Weber J-P, Roy R (2002) Cord blood lymphocyte functions in newborns from a remote maritime population exposed to organochlorines and methylmercury. J Toxicol Environ Health 65:165–182

    Article  CAS  Google Scholar 

  • Borrell A, Bloch D, Desportes G (1995) Age trends and reproductive transfer of organochlorine compounds in long-finned pilot whales from the Faroe Islands. Environ Pollut 88:283–292

    Article  CAS  Google Scholar 

  • Bossart GD, Ewing R, Herron AJ, Cray C, Mase B, Decker SJ et al (1997) Immunoblastic malignant lymphoma in dolphins: histologic, ultrastructural, and immunohistochemical features. J Vet Diagn Invest 9:454–458

    Article  CAS  Google Scholar 

  • Boumpas DT, Chrousos GP, Wilder RL, Cupps TR, Balow JE (1993) Glucocorticoid therapy for immune-mediated diseases: basic and clinical correlates. Ann Intern Med 119:1198–1208

    Article  CAS  Google Scholar 

  • Bräuner EV, Sørensen M, Gaudreau E, LeBlanc A, Eriksen KT, Tjønneland A et al (2012) A prospective study of organochlorines in adipose tissue and risk of non-Hodgkin lymphoma. Environ Health Perspect 120:105–111

    Article  Google Scholar 

  • Brown DW, McCain BB, Horness BH, Sloan CA, Tilbury KL, Pierce SM et al (1998) Status, correlations, and temporal trends of chemical contaminants in fish and sediment from selected sites on the Pacific Coast of the USA. Mar Pollut Bull 37(1–2):67–85

    Article  Google Scholar 

  • Calambokidis J, Barlow J (1991) Chlorinated hydrocarbon concentrations and their use for describing population discreetness in harbor porpoises from Washington, Oregon, and California. In: Reynolds JE III, Odell DK (eds) Marine mammal strandings in the United States. Proceedings of the second marine mammal stranding workshop 3–5 Dec 1987, Miami, Florida. NOAA technical report NMFS 98, pp 101--110

  • Chrousos GP (1995) The hypothalamic-pituitary-adrenal axis and immune-mediated inflammation. N Engl J Med 332:1351–1362

    Article  CAS  Google Scholar 

  • De Guise S, Lagacé A, Béland P (1994) Tumors in St. Lawrence beluga whales (Delphinapterus leucas). Vet Pathol 31:444–449

    Article  Google Scholar 

  • De Roos AJ, Hartge P, Lubin JH, Colt JS, Davis S, Cerhan JR et al (2005) Persistent organochlorine chemicals in plasma and risk of non-Hodgkin’s lymphoma. Cancer Res 65:11214–11226

    Article  Google Scholar 

  • Desforges JP, Ross PS, Loseto LL (2012) Transplacental transfer of polychlorinated biphenyls and polybrominated diphenyl ethers in arctic beluga whales (Delphinapterus leucas). Environ Toxicol Chem 31:296–300

    Article  CAS  Google Scholar 

  • Devesa SS, Fears T (1992) Non-Hodgkin’s lymphoma time trends: United States and international data. Cancer Res 52:5432–5440

    Google Scholar 

  • Durham AC, Pillitteri CA, San Myint M, Valli VE (2012) Two hundred three cases of equine lymphoma classified according to the World Health Organization (WHO) classification criteria. Vet Pathol 50(1):86–93

    Article  Google Scholar 

  • Engels EA, Cerhan JR, Linet MS, Cozen W, Colt JS, Davis S et al (2005) Immune-related conditions and immune-modulating medications as risk factors for non-Hodgkin’s lymphoma: a case-control study. Am J Epidemiol 162(12):1153–1161

    Article  Google Scholar 

  • Fair PA, Adams J, Mitchum G, Hulsey TC, Reif JS, Houde M et al (2010) Contaminant blubber burdens in Atlantic bottlenose dolphins (Tursiops truncatus) from two southeastern US estuarine areas: concentrations and patterns of PCBs, pesticides, PBDEs, PFCs, and PAHs. Sci Total Environ 408(7):1577–1597

    Article  CAS  Google Scholar 

  • Freeman MD, Kohles SS (2012) Plasma levels of polychlorinated biphenyls, non-Hodgkin lymphoma, and causation. J Environ Pub Health 2012:258981

    Google Scholar 

  • Glaser R, Padgett DA, Litsky ML, Baiocchi RA, Yang EV, Chen M et al (2005) Stress-associated changes in the steady-state expression of latent Epstein-Barr virus: implications for chronic fatigue syndrome and cancer. Brain Behav Immun 19(2):91–103

    Article  CAS  Google Scholar 

  • Godbout JP, Glaser R (2006) Stress-induced immune dysregulation: implications for wound healing, infectious disease and cancer. J Neuroimmune Pharm 1:421–427

    Article  Google Scholar 

  • Grulich AE, Vajdic C, Cozen W (2007) Altered immunity as a risk factor for non-Hodgkin lymphoma. Cancer Epidemiol Biomar 16(3):405–408

    Article  CAS  Google Scholar 

  • Hagmar L, Hallberg T, Leja M, Nilsson A, Schütz A (1995) High consumption of fatty fish from the Baltic Sea is associated with changes in human lymphocyte subset levels. Toxicol Lett 77:335–342

    Article  CAS  Google Scholar 

  • Hall AJ, Hugunin K, Deaville R, Law RJ, Allchin CR, Jepson PD (2006) The risk of infection from polychlorinated biphenyl exposure in the harbor porpoise (Phocoena phocoena): a case-control approach. Environ Health Perspect 114:704–711

    Article  CAS  Google Scholar 

  • Hardell L, Vanbavel B, Lindstrom G, Fredrikson M, Hagberg H, Liljegren G et al (1996) Higher concentrations of specific polychlorinated biphenyl congeners in adipose tissue from non-Hodgkin’s lymphoma patients compared with controls without a malignant disease. Int J Oncol 9:603–608

    CAS  Google Scholar 

  • Hardell L, Lindström G, van Bavel B, Wingfors H, Sundelin E, Liljegren G (1998a) Concentrations of the flame retardant 2,2′,4,4′-tetrabrominated diphenyl ether in human adipose tissue in Swedish persons and the risk for non-Hodgkin’s lymphoma. Oncol Res 10(8):429–432

    CAS  Google Scholar 

  • Hardell L, Lindström G, van Bavel B, Wingfors H, Sundelin E, Liljegren G et al (1998b) Do flame retardants increase the risk of non-Hodgkin lymphoma? The levels of polybrominated diphenyl ethers are increasing in the environment. Lakartidningen 95:5890–5893

    CAS  Google Scholar 

  • Hartge P, Devesa SS (1992) Quantification of the impact of known risk factors on time trends in non-Hodgkin’s lymphoma incidence. Cancer Res 52:5566–5569

    Google Scholar 

  • Hayes HM, Tarone RE, Cantor KP, Jessen CR, McCurnin DM, Richardson RC (1991) Case-control study of canine malignant lymphoma: positive association with dog owner’s use of 2,4-dichlorophenoxyacetic acid herbicides. J Natl Cancer I 83:1226–1231

    Article  CAS  Google Scholar 

  • Helleday T, Tuominen K-L, Bergman Å, Jenssen D (1999) Brominated flame retardants induce intragenic recombination in mammalian cells. Mutat Res 439:137–147

    Article  CAS  Google Scholar 

  • Hellou J, Lebeuf M, Rudi M (2013) Review on DDT and metabolites in birds and mammals of aquatic ecosystems. Environ Rev 21:53–69

    Article  CAS  Google Scholar 

  • Henson KL, Alleman AR, Cutler TJ, Ginn PE, Kelley LC (1998) Regression of subcutaneous lymphoma following removal of an ovarian granulo-theca cell tumor in a horse. J Am Vet Med Assoc 212(9):1419–1422

    CAS  Google Scholar 

  • Howard EB, Britt JO, Simpson JG (1983) Neoplasms in marine mammals. In: Howard EB (ed) Pathobiology of marine mammal diseases, vol II. CRC Press, Boca Raton, pp 95–107

    Google Scholar 

  • Ikpatt OF, Reavill D, Chatfield J, Clubb S, Rosenblatt JD, Fonte G et al (2014) Diagnosis and treatment of diffuse large B-cell lymphoma in an orangutan (Pongo pygmaeus). J Zoo Wildl Med 45(4):935–940

    Article  Google Scholar 

  • Jaber JR, Pérez J, Carballo M, Arbelo M, Espinosa de los Monteros A, Herráez P et al (2005) Hepatosplenic large cell immunoblastic lymphoma in a bottlenose dolphin (Tursiops truncatus) with high levels of polychlorinated biphenyl congeners. J Comp Pathol 132:242–247

    Article  CAS  Google Scholar 

  • Jarman WM, Norstrom RJ, Muir DCG, Rosenberg B, Simon M, Baird RW (1996) Levels of organochlorine compounds, including PCDDS and PCDFS, in the blubber of cetaceans from the west coast of North America. Mar Pollut Bull 32:426–436

    Article  CAS  Google Scholar 

  • Jepson PD, Bennett PM, Deaville R, Allchin CR, Baker JR, Law RJ (2005) Relationships between polychlorinated biphenyls and health status in harbor porpoises (Phocoena phocoena) stranded in the United Kingdom. Environ Toxicol Chem 24:238–248

    Article  CAS  Google Scholar 

  • Jepson PD, Deaville R, Barber JL, Aguilar A, Borrell A, Murphy S et al (2016) PCB pollution continues to impact populations of orcas and other dolphins in European waters. PLoS ONE 6:18573

    CAS  Google Scholar 

  • Johnson LL, Ylitalo GM, Arkoosh MR, Kagley AN, Stafford CL, Bolton JL et al (2007) Contaminant exposure in outmigrant juvenile salmon from Pacific Northwest estuaries. Environ Monit Assess 124:167–194

    Article  CAS  Google Scholar 

  • Johnson L, Bravo C, O’Neill S, West J, Myers MS, Ylitalo G et al (2010) A toxics-focused biological observing system for Puget Sound (developed by the Washington Department of Fish and Wildlife and NOAA Fisheries for the Puget Sound Partnership). Washington Department of Ecology Publication #10-10-04. http://wdfw.wa.gov/publications/01129/. Accessed 2 May 2016

  • Kellar NM, Trego ML, Marks CI, Dizon AE (2006) Determining pregnancy from blubber in three species of delphinids. Mar Mamm Sci 22:1–16

    Article  Google Scholar 

  • Kramer S, Hikel SM, Adams K, Hinds D, Moon K (2012) Current status of the epidemiologic evidence linking polychlorinated biphenyls and non-Hodgkin lymphoma, and the role of immune dysregulation. Environ Health Perspect 120:1067–1075

    Article  CAS  Google Scholar 

  • Lee JS, Bracci PM, Holly EA (2008) Non-Hodgkin lymphoma in women: reproductive factors and exogenous hormone use. Am J Epidemiol 168:278–288

    Article  Google Scholar 

  • Lockyer C (1995) A review of factors involved in zonation in odontocele teeth, and an investigation of the likely impact of environmental factors and major life events on harbour porpoise tooth structure. Rep Int Whal Comm (Spec Issue 16) 511–529

  • Ludewig G, Lehmann L, Esch H, Robertson LW (2008) Metabolic activation of PCBs to carcinogens in vivo: a review. Environ Toxicol Pharm 25(2):241–246

    Article  CAS  Google Scholar 

  • Meironyté Guvenius D, Norén K (2001) Polybrominated diphenyl ethers in Swedish human liver and adipose tissues. Arch Environ Contam Toxicol 40(4):564–570

    Article  Google Scholar 

  • Moreno-Smith M, Lutgendorf SK, Sood AK (2010) Impact of stress on cancer metastasis. Future Oncol 6(12):1863–1881

    Article  Google Scholar 

  • Mos L, Cameron M, Jeffries SJ, Koop BF, Ross PS (2010) Risk-based analysis of PCB toxicity in harbor seals. Integr Environ Assess Manage 6:631–640

    Article  CAS  Google Scholar 

  • Nelson RA, Levine AM, Bernstein L (2001) Reproductive factors and risk of intermediate- or high-grade B-cell non-Hodgkin’s lymphoma in women. J Clin Oncol 19(5):1381–1387

    Article  CAS  Google Scholar 

  • Newman SJ, Smith SA (2006) Marine mammal neoplasia: a review. Vet Pathol 43:865–880

    Article  CAS  Google Scholar 

  • Noël M, Dangerfield N, Hourston RA, Belzer W, Shaw P, Yunker MB et al (2009) Do trans-Pacific air masses deliver PBDEs to coastal British Columbia, Canada? Environ Pollut 157:3404–3412

    Article  Google Scholar 

  • O’Neill SM, West JE (2009) Marine distribution, life history traits and the accumulation of polychlorinated biphenyls (PCBs) in Chinook salmon (Oncorhynchus tshawytscha) from Puget Sound, Washington. Trans Am Fish Soc 138:616–632

    Article  Google Scholar 

  • Park H-Y, Hertz-Picciotto I, Petrik J, Palkovicova L, Kocan A, Trnovec T (2008) Prenatal PCB exposure and thymus size at birth in neonates in Eastern Slovakia. Environ Health Perspect 116:104–109

    Article  CAS  Google Scholar 

  • Prescott J, Lu Y, Chang ET, Sullivan-Halley J, Henderson KD, Clarke CA et al (2009) Reproductive factors and non-Hodgkin lymphoma risk in the California Teacher’s Study. PLoS ONE 4(12):e8135

    Article  Google Scholar 

  • Robinson EM, Jiac M, Trumble SJ, Usenko S (2013a) Selective pressurized liquid extraction technique for halogenated organic pollutants in marine mammal blubber: a lipid-rich matrix. J Chromatogr A 1385:111–115

    Article  Google Scholar 

  • Robinson EM, Trumble SJ, Subedi B, Sanders R, Usenko S (2013b) Selected pressurized liquid extraction of pesticides, polychlorinated biphenyls and polybrominated diphenyl ethers in a whale earplug (earwax): a novel method for analyzing organic contaminants in lipid-rich matrices. J Chromatogr A 1319:14–20

    Article  CAS  Google Scholar 

  • Romero LM, Raley-Susman KM, Redish DM, Brooke SM, Horner HC, Sapolsky RM (1992) Possible mechanism by which stress accelerates growth of virally derived tumors. Proc Natl Acad Sci 89:11084–11087

    Article  CAS  Google Scholar 

  • Ross PS, De Swart RL, Addison RF, Van Loveren H, Vos JG, Osterhaus ADME (1996) Contaminant-induced immunotoxicity in harbour seals: wildlife at risk? Toxicology 112:157–169

    Article  CAS  Google Scholar 

  • Ross PS, Noël M, Lambourn D, Dangerfield N, Calambokidis J, Jeffries S (2013) Declining concentrations of persistent PCBs, PBDEs, PCDEs, and PCNs in harbor seals (Phoca vitulina) from the Salish Sea. Prog Oceanog 115:160–170

    Article  Google Scholar 

  • Rotander A, van Bavel B, Polder A, Rigét F, Auðunsson GA, Gabrielsen GW et al (2012) Polybrominated diphenyl ethers (PBDEs) in marine mammals from Arctic and North Atlantic regions, 1986–2009. Environ Int 40:102–109

    Article  CAS  Google Scholar 

  • Saha A, Robertson ES (2011) Epstein-Barr virus-associated B-cell lymphomas: pathogenesis and clinical outcomes. Clin Cancer Res 17(10):3056–3063

    Article  CAS  Google Scholar 

  • Swerdlow SH, Campo E, Harris NL, Jaffe ES, Pileri SA, Stein H et al (eds) (2008) WHO classification of tumours of haematopoietic and lymphoid tissues, vol 2. WHO Press, Switzerland

    Google Scholar 

  • Tong S, Chern S-WW, Li Y, Pallansch M, Anderson LJ (2008) Sensitive and broadly reactive reverse transcription-PCR assays to detect novel paramyxoviruses. J Clin Microbiol 46(8):2652–2658

    Article  CAS  Google Scholar 

  • Trumble SJ, Robinson EM, Noren SR, Usenko S, Davis J, Kanatous SB (2012) Assessment of legacy and emerging persistent organic pollutants in Weddell seal tissue (Leptonychotes weddellii) near McMurdo Sound, Antarctica. Sci Total Environ 439:275–283

    Article  CAS  Google Scholar 

  • US Environmental Protection Agency (2016) Polychlorinated biphenyls. United States Environmental Protection Agency. https://www.epa.gov/pcbs. Accessed 12 Apr 2016

  • VanDevanter DR, Warrener P, Bennett L, Schultz ER, Coulter S, Garber RL et al (1996) Detection and analysis of diverse herpesviral species by consensus primer PCR. J Clin Microbiol 34(7):1666–1671

    CAS  Google Scholar 

  • Venn-Watson S, Benham C, Gulland FM, Smith CR, St Leger J, Yochem P et al (2012) Clinical relevance of novel Otarine herpesvirus-3 in California sea lions (Zalophus californianus): lymphoma, esophageal ulcers, and strandings. Vet Res 43:85

    Article  CAS  Google Scholar 

  • Vonderheide AP, Mueller KE, Meija J, Welsh GL (2008) Polybrominated diphenyl ethers: causes for concern and knowledge gaps regarding environmental distribution, fate and toxicity. Sci Total Environ 400:425–436

    Article  CAS  Google Scholar 

  • Vos JG, Bossart G, Fournier M, O’Shea T (eds) (2002) Toxicology in marine mammals. CRC Press, Boca Raton

    Google Scholar 

  • Waldichuk M (1983) Pollution in the Strait of Georgia: a review. Can J Fish Aquat Sci 40(7):1142–1167

    Article  CAS  Google Scholar 

  • Washington Department of Fish and Wildlife (2016) Marine toxic contaminants, species and ecosystem science http://wdfw.wa.gov/conservation/research/projects/marine_toxics/. Accessed 2 June 2016

  • West JE, O’Neill SM, Ylitalo GM (2008) Spatial extent, magnitude, and patterns of persistent organochlorine pollutants in Pacific herring (Clupea pallasii) populations in the Puget Sound (USA) and Strait of Georgia (Canada). Sci Total Environ 394:369–378

    Article  CAS  Google Scholar 

  • Word ZH, Matasar MJ (2012) Advances in the diagnosis and management of lymphoma. Blood Lymphat Cancer Targets Ther 2:29–55

    Google Scholar 

  • Ylitalo GM, Matkin CO, Buzitis J, Krahn MM, Jones L, Rowles T, Stein JE (2001) Influence of life-history parameters on organochlorine concentrations in free-ranging killer whales (Orcinus orca) from Prince William Sound, AK. Sci Total Environ 281:183–203

    Article  CAS  Google Scholar 

  • Ylitalo GM, Stein JE, Hom T, Johnson LL, Tilbury KL, Hall AJ et al (2005) The role of organochlorines in cancer-associated mortality in California sea lions (Zalophus californianus). Mar Pollut Bull 50:30–39

    Article  CAS  Google Scholar 

  • Zahm SH, Blair A (1992) Pesticides and non-Hodgkin’s lymphoma. Cancer Res 52(19 Supplement):5485s–5488s

    CAS  Google Scholar 

Download references

Acknowledgements

Essential funding for collection of these samples was provided through grants from the John H. Prescott Marine Mammal Rescue Assistance Grant Program. The marine mammal stranding network members of Washington State helped procure porpoise tissues. Aleta Hohn (NOAA Fisheries, Southeast Fisheries Science Center, Beaufort, NC) and Jennifer Olson (The Whale Museum, Friday Harbor, WA) provided age information for the lymphoma-positive case.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Stephanie A. Norman.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplementary material 1 (XLSX 9 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Norman, S.A., Winfield, Z.C., Rickman, B.H. et al. Persistent Organic Pollutant and Hormone Levels in Harbor Porpoise with B Cell Lymphoma. Arch Environ Contam Toxicol 72, 596–605 (2017). https://doi.org/10.1007/s00244-017-0404-y

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00244-017-0404-y

Keywords

Navigation