The sero-prevalence of Toxoplasma gondii in British marine mammals

Article (PDF Available)inMemórias do Instituto Oswaldo Cruz 104(2):296-8 · April 2009with22 Reads
DOI: 10.1590/S0074-02762009000200024 · Source: PubMed
Abstract
Serum samples from 101 stranded or bycatch cetaceans from British waters were screened for Toxoplasma gondii-specific antibodies using the Sabin Feldman Dye Test. Relatively high seropositivity was recorded in short-beaked Delphinus delphis and this study presents the first documented case of Toxoplasma in a humpback whale Megaptera novaeangliae.
1Mem Inst Oswaldo Cruz, Rio de Janeiro, Vol. 104(2): 000-000, March 2009
online | memorias.ioc.fiocruz.br
The sero-prevalence of Toxoplasma gondii in British marine mammals
Dan Forman/
+
, Nathan West, Janet Francis, Edward Guy
Conservation Ecology Research Team, Institute of Environmental Sustainability, School of the Environment and Society,
Swansea University, Singleton Park, Swansea, SA2 8PP, UK
Serum samples from 101 stranded or bycatch cetaceans from British waters were screened for Toxoplasma
gondii-specific antibodies using the Sabin Feldman Dye Test. Relatively high seropositivity was recorded in short-
beaked Delphinus delphis and this study presents the first documented case of Toxoplasma in a humpback whale
Megaptera novaeangliae.
Key words: cetacean - conservation - environmental contamination - protozoa - toxoplasmosis
Toxoplasma gondii is a globally ubiquitous, Apicom-
plexan protozoan parasite, capable of infecting all warm
blooded animals (Wong & Remington 1993). Toxoplas-
ma is a zoonotic parasite responsible for toxoplasmosis,
a disease which can affect the survival of many free-
living mammalian species. The only known definitive
hosts for T. gondii are members of the Felidae (cat) fami-
ly. It has frequently been demonstrated that wild animals
are important reservoirs of many infectious diseases
(e.g. SARS, H5N1 Avian influenza) and play an impor-
tant role in transmission and disease ecology (Simpson
2002). We, therefore consider it essential that baseline
measurements of T. gondii prevalence and occurrence
are determined in wild animals in order to understand
their role in T. gondii epidemiology.
Previously, Toxoplasma studies in wild animals has
been restricted to terrestrial species, however, an increas-
ing area of research has focused on marine mammals.
Of particular concern is the effect on populations of en-
dangered marine mammals such as sea otters (Enhydra
lutris nereis), a mustelid species in which toxoplasmosis
has been linked to many instances of mortality on the
Western seaboard of the United States. T. gondii posi-
tive free-living marine mammals have been identified in
many marine ecosystems including the Eastern, Central
and Western Pacific, Western Atlantic and Mediterra-
nean (Dubey et al. 2003). This study presents the initial
findings of serological screening from a range of ceta-
cean species inhabiting the Northeastern Atlantic and
provides the first documented cases of positive Toxo-
plasma in this marine region.
MATERIALS AND METHODS
Sera samples from 101 individual cetaceans were ob-
tained by postmortem examination of animals stranded
in England and Wales between 2001-2003. All postmor-
tem examinations were conducted according to stan-
+ Corresponding author: d.w.forman@swansea.ac.uk
Received 10 October 2008
Accepted 4 December 2008
dardised methodology (Law 1994) by staff at the Insti-
tute of Zoology, London. Sera were analyzed using the
Sabin Feldman Toxoplasma Cytoplasma Modifying An-
tibody Dye Test at the Toxoplasma Reference Unit (TRU
2007), National Public Health Service for Wales, Single-
ton Hospital, Swansea, United Kingdom, according to
the TRU protocol (TRU 2007). Titers deemed positive at
¼ (≥ 2 IU mL
-1
) according to TRU standards were clas-
sified as positive results. To facilitate analysis, marine
zones were demarcated using geographical areas based
upon Hammond et al. (2002).
RESULTS
A total of eight animals (7.9%) demonstrated sero-
positivity with T. gondii antibody levels ranging from 8
IU mL
-1
-250 IU mL
-1
(Table). Sero-positive animals were
recorded in three of the five marine zones from which
samples were screened (Figure).
DISCUSSION
The majority of seropositive animals were short-
beaked common dolphins (Delphinus delphis) and se-
roprevalence data revealed the first ever documented
Toxoplasma infection in a baleen whale species (hump-
back whale Megaptera novaeangliae). These findings
represent the first T. gondii-seropositive cases from
cetaceans in British waters and demonstrate that ceta-
cean populations frequenting British waters are exposed
to T. gondii at some stage, although the specific route
of transmission has not yet been confirmed. It seems
likely that infection in cetaceans is via T. gondii oocysts
in contaminated water as these animals predominantly
feed on fish, invertebrates and cold-blooded animals
which would not be expected to support the tachyzoite
and bradyzoite life-cycle stages of T. gondii. This is sup-
ported by seropositivity in a single humpback whale, as
humpback whales are primarily planktivorous and pis-
civorous (Barros & Clark 2002).
The humpback whale is generally understood to be
a seasonal migrator with Northern Atlantic populations
thought to have breeding grounds in the West Indies
(Smith et al. 1999). Known feeding grounds exist in wa-
ters off Norway, Iceland, Greenland and Canada (Ste-
vick et al. 2003). Humpback whales have been detected
consistently between October-March from the Western
Toxoplasma gondii in British marine mammals • Dan Forman et al.
2
edge of the English Channel to the Western waters of the
Shetland Islands (Charif et al. 2001). Postmortem exami-
nation indicated the infected animal in this study was a
juvenile and the probable cause of death was starvation.
The recovery location (Figure, Zone E2) is a consider-
able distance from the closest known migratory route.
It seems plausible this individual became disorientated
during migration and accidentally entered the Eng-
lish Channel. The lack of productive food sources here
could have lead to starvation. Since latent infections of
T. gondii are know to affect behavior in other animals,
the question arises as to what extent behavioral changes
contributed on this occasion. It is recognized that this is
only one of many possible explanations; but this raises
concerns about the nature of the threat posed to marine
species by T. gondii.
Many marine mammals inhabit coastal environ-
ments and most, with the exception of the planktivores
and herbivores, occupy a high position in their associ-
ated food webs. Since much of their dietary intake is of
commercial importance to humans they may be used as
important sentinels of marine environmental health (Le
Blanc 1997). Recent work in California (Miller 2004)
associated T. gondii infection with mortality in South-
ern Sea Otters. Furthermore, sub-clinical toxoplasmosis
has been linked with behavioral changes in both rodents
(Webster et al. 1994) and humans (Yolken et al. 2001).
As such it is conceivable that marine mammals may
also undergo such changes and that these changes may
have a direct impact on the fitness of the infected spe-
cies concerned. We suggest that T. gondii seroprevalence
should be routinely tested for in all postmortems of ma-
rine mammals from the UK and other national waters in
order to provide an assessment of the potential risk from
T. gondii infection in marine mammals.
ACKNOWLEDGEMENTS
To Paul Jepson and Rob Deaville (Institute of Zoology),
for providing samples for this study.
REFERENCES
Barros NB, Clarke MR 2002. Diet. In WF Perrin, B rsig, JMB
Thewissen, Encyclopaedia of marine mammals, Academic Press,
San Diego, p. 323-327.
THIS REFERENCE IS NOT LISTED AT FINAL
TABLE
Animals tested and percentage occurrence of Toxoplasma gondii, including titer range (IU mL-1)
Number Number Percentage Titer Range
Species tested positive Occurrence (IU mL-1)
Delphinus delphis
(Shot-beaked common dolphin) 21 6 28.6 8-250
Grampus griseus
(Risso’s dolphin) 1 0 0.0 < 2
Lagenorhynchus acutus
(Atlantic white-sided dolphin) 1 0 0.0 < 2
Megaptera novaeangliae
(Humpback whale) 1 1 100.0 8
Phocoena phocoena
(Harbour porpoise) 70 1 1.4 125
Stenella coeruleoalba
(Striped Dolphin) 5 0 0.0 < 2
Tursiops truncatus
(Bottlenose dolphin) 1 0 0.0 < 2
Ziphius cavirostris
(Cuvier’s Beaked Whale) 1 0 0.0 < 2
Outline map of UK and surrounding waters, number of Toxoplasma
gondii sero-positive and sero-negative cetaceans found in each ma-
rine zone.
wAITINg
FOR NEw ImAgE
3
Mem Inst Oswaldo Cruz, Rio de Janeiro, Vol. 104(2), March 2009
Charif RA, Clapham PJ, Clark CW 2001. Acoustic detections of sing-
ing humpback whales in deep waters off the British Isles. Mar
Mammal Sci 17: 751-768.
Conrad PA, Miller MA, Kreuder C, James ER, Mazet J, Dabritz H, Jes-
sup DA, Gulland F, Grigg ME 2005. Transmission of Toxoplasma:
clues from the study of sea otters as sentinels of Toxoplasma gondii
flow into the marine environment. Int J Parasitol 35: 1155-1168.
THIS REFERENCE IS NOT CITED IN THE TEXT. mAY
wE DELETE OR PLEASE LOCATE THE PROPER PLACE
IN THE TEXT. ???????????????????
Dubey JP 1994. Zoonosis update: toxoplasmosis. J Am Vet Med Asso
205: 1593-1598. THIS REFERENCE IS NOT CITED IN THE
TEXT. mAY wE DELETE OR PLEASE LOCATE THE
PROPER PLACE IN THE TEXT. ???????????????????
Dubey JP, Zarnke R, Thomas NJ, Wong SK, Van Bonn W, Briggs M,
Davis JW, Ewing R, Mense M, Kwok OCH, Romand S, Thulliez
P 2003. Toxoplasma gondii, Neospora canium, Sarcocystis neu-
rona and Sarcocystis canis-like infections in marine mammals.
Vet Parasitol 116: 275-296.
Hammond PS, Berggren P, Benke H, Borchers DL, Collet A, Heide-
Jørgensen MP, Heimlich S, Hiby AR, Leopold MF, Øien N 2002.
Abundance of harbour porpoise and other cetaceans in the North
Sea and adjacent waters. J Appl Ecol 39: 361-376.
Inskeep W, Gardiner CH, Harris RK, Dubey JP, Goldston RT 1990.
Toxoplasmosis in Atlantic bottle-nosed dolphins (Tursiops
truncatus). J Wildlife Dis 26: 377-382. THIS REFERENCE
IS NOT CITED IN THE TEXT. mAY wE DELETE OR
PLEASE LOCATE THE PROPER PLACE IN THE TEXT.
???????????????????
Law RJ 1994. Collaborative UK marine mammal project: summary of
data produced 1988-1992. Fisheries Research Technical Report,
Ministry of Agriculture, Fisheries and Food, Directorate of Fish-
eries Research, Lowestoft, 42 pp.
LeBlanc GA, Bain LJ 1997. Chronic toxicity of environmental contami-
nants: sentinels and biomarkers. Environ Health Persp 105: 65-80.
Lower WR, Kendall RJ 1990. Sentinel species and sentinel bioas-
say. In JF McCarthy, LR Shughart, Biomarkers of environmen-
tal contamination, Lewis Publishers, Chelsea, p. 309-331. THIS
REFERENCE IS NOT CITED IN THE TEXT. mAY wE DE-
LETE OR PLEASE LOCATE THE PROPER PLACE IN THE
TEXT. ???????????????????
Measures LN, Dubey JP, Labelle P, Martineau D 2004. Seroprevalence
of Toxoplasma gondii in Canadian pinnipeds. J Wildl Dis 40: 294-
300. THIS REFERENCE IS NOT CITED IN THE TEXT.
mAY wE DELETE OR PLEASE LOCATE THE PROPER
PLACE IN THE TEXT. ???????????????????
Miller 2004. PLEASE, COmPLETE. ??????????????????????
Miller MA, Gardner IA, Kreuder C, Paradies DM, Worcester KR, Jes-
sup DA, Dodd E, Harris MD, Ames JA, Packham AE, Conrad PA
2002. Coastal freshwater runoff is a risk factor for Toxoplasma
gondii infection of Southern sea otters (Enhydra lutris nereis). Int
J Parasitol 32: 997-1006. THIS REFERENCE IS NOT CITED
IN THE TEXT. mAY wE DELETE OR PLEASE LOCATE
THE PROPER PLACE IN THE TEXT. ???????????????????
Oksanen A, Tryland M, Johnsen K, Dubey JP 1998. Serosurvey of
Toxoplasma gondii in North Atlantic marine mammals by the
use of agglutination test employing whole tachyzoites and dithio-
threitol. Comp Immunol Microbiol Infect Dis 21: 107-114. THIS
REFERENCE IS NOT CITED IN THE TEXT. mAY wE DE-
LETE OR PLEASE LOCATE THE PROPER PLACE IN THE
TEXT. ???????????????????
Simpson VR 2002. Wild animals as reservoirs of infectious diseases
in the UK. Vet J 163: 128-146.
Smith TD, Allen J, Clapham PJ, Hammond PS, Katone S, Larsen F,
Lien J, Matilla D, Palsbøll PJ, Sigurjóhnssen J, Stevick PT, Øein
N 1999. An ocean-basin-wide mark-recapture study of the North
Atlantic humpback whale (Megaptera novaeangliae). Mar Mam-
mal Sci 15: 1-32.
Stevick PT, Allen J, ru M, Clapham PJ, Katona SK, Larsen F,
Lien J, Mattila DK, Palsbøll PJ, Robbins J, Sigurjøhnssen J,
Smith TD, Øein N, Hammond PJ 2003. Segragation of migra-
tion by feeding ground origin in North Atlantic humpback whales
(Megaptera novaeangliae). J Zool Lond 259: 231-237.
Tenter AM, Heckeroth AR, Weiss LM 2000. Toxoplasma gondii:
from animals to humans. Int J Parasitol 30: 1217-1258. THIS
REFERENCE IS NOT CITED IN THE TEXT. mAY wE DE-
LETE OR PLEASE LOCATE THE PROPER PLACE IN THE
TEXT. ???????????????????
TRU - Toxoplasma Reference Unit 2007. Toxoplasma Cytoplasma
Modifying Antibody Test (Dye Test). Toxoplasma Reference
Unit, National Public Health Service for Wales, Singleton Hospi-
tal, Swansea, SA2 8QA, United Kingdom.
Webster JP, Brunton CF, MacDonald DW 1994. Effect of Toxoplasma
gondii on neophobic behaviour in wild brown rats, Rattus nor-
vegicus. Parasitol 109: 37-43.
Wong SY, Remington JS 1993. Biology of Toxoplasma gondii. AIDS
7: 299-316.
Yolken RH, Bachmann S, Rouslanova I, Lillehoj E, Ford G, Torrey EF,
Schroeder J 2001. Antibodies to Toxoplasma gondii in individuals
with first-episode schizophrenia. Clin Infect Dis 32: 842-844.
    • "Antibodies against T. gondii have been detected in several species of marine mammals[5,9101112. Not only the occurrence of antibodies to T. gondii is known, but the clinical toxoplasmosis has been diagnosed in[9,10]. Studies with several species of mammals around the world bring relevant information about the presence of the parasite T. gondii in the marine environment. "
    [Show abstract] [Hide abstract] ABSTRACT: Objective: To investigate the presence of antibodies against Toxoplasma gondii (T. gondii) in Mirounga leonina (M. leonina) Linnaeus from Elephant Island, Antarctica. Methods: The animals were anesthetized, restrained, measured, weighed and had their blood collected by venipuncture of intervertebral lumbar epidural vein. Blood samples were collected from 102 individuals. Indirect hemagglutination and serum dilution at a proportion of 1:25 was used for specific immunoglobulin G anti-T. gondii detection. Results: Only one (0.98%) specimen, a newly weaned calf, was seropositive. Conclusions: This study is the highest serological survey for antibody detection against T. gondii in M. leonina. The results suggest a low level of exposure to T. gondii, probably due to the absence of felids in the study area. The seropositivity presented by the elephant seal may be related to the presence of oocysts in water or cysts in their preys. Despite being reported the presence of the parasite in fish and molluscs, there are no records of tissue cysts or oocysts in squid or fish of the diet of M. leonina. Thus, further parasitological studies focused on preys of elephant seals are needed for a better understanding of infection of M. leonina by T. gondii.
    Full-text · Article · Mar 2016
    • "Of the 30 identified marine mammal species in the Philippines, 28 are cetaceans and 22 of these are reported to strand (Aragones et al., 2010 ), providing the much needed chance to study these difficult-to-observe albeit charismatic animals. While it is not the primary aim of the study to investigate the role of pathogen or disease occurrence in sampled stranding events, the involvement of such may be suggested as done elsewhere (Lopez et al., 2002; Kreuder et al., 2003; Gonzalez-Solis et al., 2006; Stoddard et al., 2008; Fauquier et al., 2009; Forman et al., 2009; Colegrove et al., 2010). This study generally aimed to detect the occurrence of bacteria, Giardia, and Toxoplasma gondii in cetaceans stranded in the Philippines. "
    [Show abstract] [Hide abstract] ABSTRACT: The general consensus of a rapidly changing ocean ecosystem being affected by anthropogenic activities needs to be understood in relation to both wildlife and human health. The risks and challenges for the Philippines include lack of scientific information on waterborne diseases that are potentially zoonotic. The present study fills in this knowledge gap by detecting the occurrence of bacteria, Giardia, and Toxoplasma gondii in locally found cetacean species. Cetaceans (n = 30) that stranded from January 2012 through March 2013 were appropriately responded to, and biological materials were taken whenever applicable. A total of 25 bacteria were isolated from nine stranders. Phenotypic and genotypic methods of isolate identification yielded 12 consensus genera: Acinetobacter, Aeromonas, Burkholderia, Enterococcus, Moraxella, Proteus, Providencia, Rhizobium, Serratia, Sphingomonas, Staphylococcus, and Vibrio. No screened strander was positive for Giardia. Serological assay detected antibodies for T. gondii in five stranders, while nested polymerase chain reaction positively amplified the B1 gene of the parasite in two stranders. This study provides the first report on bacteria and T. gondii in cetaceans found in the Philippines. Since the detected microorganisms include species recognized to cause new infections in marine mammals worldwide, the findings of the study underscore the potential of stranded cetaceans to serve as sentinels for studying the movement of emerging pathogens in marine habitats, provide clues on the health status of their free-ranging populations, and present the health risks available to humans who share the same water resource with them.
    Full-text · Article · Jun 2015
    • "Of the 30 identified marine mammal species in the Philippines, 28 are cetaceans and 22 of these are reported to strand (Aragones et al., 2010 ), providing the much needed chance to study these difficult-to-observe albeit charismatic animals. While it is not the primary aim of the study to investigate the role of pathogen or disease occurrence in sampled stranding events, the involvement of such may be suggested as done elsewhere (Lopez et al., 2002; Kreuder et al., 2003; Gonzalez-Solis et al., 2006; Stoddard et al., 2008; Fauquier et al., 2009; Forman et al., 2009; Colegrove et al., 2010). This study generally aimed to detect the occurrence of bacteria, Giardia, and Toxoplasma gondii in cetaceans stranded in the Philippines. "
    [Show abstract] [Hide abstract] ABSTRACT: The general consensus of a rapidly changing ocean ecosystem being affected by anthropogenic activities needs to be understood in relation to both wildlife and human health. The risks and challenges for the Philippines include lack of scientific information on waterborne diseases that are potentially zoo-notic. The present study fills in this knowledge gap by detecting the occurrence of bacteria, Giardia, and Toxoplasma gondii in locally found cetacean species. Cetaceans (n = 30) that stranded from January 2012 through March 2013 were appropriately responded to, and biological materials were taken whenever applicable. A total of 25 bacteria were isolated from nine stranders. Phenotypic and genotypic methods of isolate identification yielded 12 consensus genera:. No screened strander was positive for Giardia. Serological assay detected antibodies for T. gondii in five stranders, while nested polymerase chain reaction positively amplified the B1 gene of the parasite in two stranders. This study provides the first report on bacteria and T. gondii in cetaceans found in the Philippines. Since the detected microorganisms include species recognized to cause new infections in marine mammals worldwide, the findings of the study underscore the potential of stranded cetaceans to serve as sentinels for studying the movement of emerging pathogens in marine habitats, provide clues on the health status of their free-ranging populations, and present the health risks available to humans who share the same water resource with them.
    Full-text · Article · Jan 2015 · Aquatic Mammals
Show more