toxoplasma gondii infections in hawaiian monk seals · 2020. 11. 16. · ro28 “pohaku” days 1-2...
TRANSCRIPT
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Toxoplasma gondii infections in Hawaiian monk seals
Michelle Barbieri, Katie Colegrove, Stacie Robinson, Cara Field, Angela Amlin, Gregg Levine, Charles Littnan
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HMS: The Basics
• Endangered
• Only tropical seal
• Population size 1,400
• Poor genetic diversity
• Interisland movement varies by individual
• Diverse benthic foragers
Northwestern Hawaiian Islands (NWHI)1,100 seals
Main Hawaiian Islands (MHI)300 seals
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HMS Research
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Threats: NWHI
Northwestern Hawaiian Islands (NWHI)1,100 seals
• Low human presence
• Abundant predators/competition
for prey
• Food limitation
• Poor juvenile survival
• Older age of first reproduction
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Threats: MHI
Main Hawaiian Islands (MHI)300 seals
• High human presence - fisheries interactions, intentional killing, disease*
• Fishing reduces competition for prey
• Good nutritional condition
• Primiparity as early as age 4
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Contaminants: Below concentrations shown to have effects in other species.
Reproductive Pathogens: Prevalence is 9% or less for:
Brucella, Chlamydia, Coxiella, herpesvirus, Leptospira, Toxoplasma
Specimen Archive:Blood
Swabs
Blubber biopsies
Necropsy tissues
Population Health Monitoring
Infectious Diseases:Leptospira rare
Morbillivirus none
Herpesvirus occasional
Adenovirus rare
Brucella rare
Parasites: Gastrointestinal cestodes, nematodesProtozoa
Necropsy:Trauma
Drowning
Reproductive complications
Hook ingestion
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The first live-stranded cases in 2015
• Unique - most HMS w/ toxo found dead
• Both patients died w/in 48 hr of admit
• Taught us about “logging” behavior for early detection
• Illustrated the massive inflammatory response to infection
• NOAA elevated its level of concern about the threat of toxo to species
• Pathology crucial to understanding pathogenesis
Rescuing the first live-stranded seal case of toxoplasmosis, adult female RB24, O’ahu 2015
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HMS Deaths from Protozoal Infections
2001-present: 13 known deaths
Case definition for protozoal deaths in HMS:
Gross necropsyHistopathologyImmunohistochemistrySupporting molecular data when avail.Barbieri et al. 2016
Excerpt from Table 1, Barbieri et al. 2016
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Deaths: n=13
(red/female, blue/male)
Suspect cases:
n=2 (orange)
Predominantly females
affected
More deaths go
undetected
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Population Impacts: Causes of death in the main Hawaiian Islands, 1992-2019
Anthropogenic threats…
• physical injury
• drowning/nets
• Toxoplasmosis
…have the largest impact on the population and are hampering its
growth in this region.
Harting et al. 2020 – Marine Mammal Science
(early view) https://doi.org/10.1111/mms.12742
https://doi.org/10.1111/mms.12742
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Molecular analyses & Serology
• Serology (apparently healthy animals sampled opportunistically)• Low seroprevalence in the population (4% or less)
• More likely to be seropositive in MHI than NWHI (Aguirre et al. 2007; HMSRP unpub. data)
• 2018 cases: multiple genotypes and mixed infections (predominantly Type I and III alleles) – suggests multiple oocyst sources and different strains causing lethality than in otters (Type X)
• Molecular analysis across archived stranded seal tissues ongoing and not ready for prime time
Acknowledgements/contributors: Katie Haman, Karen Shapiro, Liz VanWormer, Michael Grigg & lab
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Gross lesions
Juveniles/Adults:
▪ Adipose tissue - Firm, mottled yellow-red nodules
▪ Pericardial adipose
▪ Mesentery
▪ Lymph nodes - Enlarged, congested, edematous
▪ Fluid in abdominal cavity
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Histologic Lesions
• Mesenteric and epicardial steatitis • Lymphadenitis and splenitis• Pneumonia • Meningoencephalitis• Endometritis• Adrenalitis• Pancreatitis• Myocarditis• Myositis
Most severe and more frequent
Least severe and less frequent
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MYRIAD TACHYZOITES!!
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Adipose tissue:Inflammation, necrosis, myriad tachyzoites
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Meningoencephalitis
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Adrenalitis
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TACHYZOITES
Fetal Pneumonia
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Heart and muscle only minimally affected
Zoite cluster
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Endometritis and Necrosis –Pregnant and post parturient females
Juvenile Female – No Inflammation
Adult female that recently aborted
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Infections confirmed by Toxoplasma gondii IHC and PCR
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Severe Toxoplasma Infections in Species Not Coadapted
South America
Necrotizing lymphadenitis
From: Juan-Salles et al. JZWM 1998
Lymphohistiocytic and necrotizing encephalitis
Australia
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Marine Mammals – Toxoplasmosis in Sea Otters
- Incidental infections – cysts- Fatal meningoencephalitis – often Type X
Moderate lymphohistiocytic inflammation –variable #s of organisms
Infection can increase susceptibility to predation
Photos courtesy of Melissa Miller
Photos: M. Miller
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Marine Mammals – Toxoplasmosis in Pinnipeds
Myocarditis
California sea lions:- Infections identified
infrequently
- 1975-2009 = 9 cases @ one large rehabilitation hospital
- Myocarditis, encephalitis, few fetal infections
Pacific harbor seals:- Pacific Northwest
- Fatal meningoencephalitis observed more frequently in adults
- Typically co-infection with Sarcocystis neurona
Meningoencephalitis
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How are monk seals getting exposed?
Case definition in HMS
Impacts on population
Pathogenesis
Let’s talk a little bit about exposure risk…
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Toxoplasmosis cases
RH40M 2010
RT10F 2018+ pup
RK29M 2005sRK60F 2018
R017F 2014
RB24F 2015+ pup
R011F 2007s
RK07M 2010
KA060D03M 2006
RN36F 2015
RTX1F 2010
Toxoplasma cases (& suspects) -2019
Stacie Robinson, PhDForaging Ecologist
HMSRP
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RT10F 2018+ pup
RK29M 2005sRK60F 2018
R017F 2014
RB24F 2015+ pup
R011F 2007s
RH40M 2010
RK07M 2010
KA060D03M 2006
RN36F 2015
RTX1F 2010
MHI Cases: Space Use
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RN36F2015
RT10F 2018
RK29M2005s
RK60F2018
R017F2014
RB24F2015
Oahu Cases: Space Use +Sediment Outflow
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Monk seals exhibit far-reaching space use• Potential for wide area of exposure • Mortality site not necessarily indicative of
exposure site
Monk seals exhibit variable space use• From multiple islands to localized beaches• Variable ability to discern location pre-
mortality
Estimate of space use highly dependent on sightings effort
• Effort varies across time and islands• Potential bias against remote beaches
Conclusions on preliminary spatial risk evaluation
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CASE STUDYJanuary 22, 2020: RO28 “Pohaku”
First, a note of immense gratitude:
• The entire NOAA HMSRP and PIRO monk seal team
• Volunteers everywhere
• Ke Kai Ola & The Marine Mammal Center
• Hawaii Marine Animal Response
• Veterinary science collective: Gregg Levine, Cara Field, Katie Colegrove, Meghan Barrett, Deb Fauquier, Karen Shapiro, Pat Conrad, Teri Rowles
• United States Coast Guard
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RO28 “Pohaku” Days 1-2
Signalment Adult female, presumed pregnant (due July 2020)
Hx Lethargic behavior for 4 days, rescued 1/22/2020
PE QAR, BCS 3/5, 220 kg, no signs trauma
Imaging No foreign body (hook), uterus WNL, mild enteritis
CBC/Chemistry Mild elevations in TP, globulins, ALT, P and Na
Tx Ceftiofur, famotidine, maropitant, praziquantel
Ddx Infectious/inflammatory: toxoplasmosis vs. gastroenteritis vs. reproductive disease
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RO28 “Pohaku”
Protozoal titers T. gondii 1:40,960 (Sarco 1:80, Neo: 1:160)
Tx (SID) Ponazuril, Clindamycin, TMS, Dexamethasone
IV/SC LRS, Vitamin B12 & B complex, cerenia,famotidine, OptiMarine supplement, Vit. E, alpha lipoic acid supplement, herring slurry PO (sedated with diazepam)
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RO28 “Pohaku” Days 3-5
Protozoal titers T. gondii 1:40,960 (Sarco 1:80, Neo: 1:160)
Tx Ponazuril, Clindamycin, TMS,Dexamethasone, IV/SC LRS, Vitamin B12 & B complex, cerenia,famotidine, OptiMarine supplement, herring-electrolyte slurry PO (sedated with diazepam)
PE Mentation declined to dull and minimally responsive
Other diagnostics Morbillivirus neg, HMS herpesvirus neg
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RO28 “Pohaku” Days 3-5
Protozoal titers T. gondii 1:40,960 (Sarco 1:80, Neo: 1:160)
Tx Ponazuril, Clindamycin, TMS,Dexamethasone, IV/SC LRS, Vitamin B12 & B complex, cerenia,famotidine, OptiMarine supplement, herring-electrolyte slurry PO (sedated with diazepam)
PE Mentation declined to dull and minimally responsive
Other diagnostics Morbillivirus neg, HMS herpesvirus neg
Monk seal RKC1 (“Sole”)
• Carcass found January 26, 2020 • Juvenile male • Found dead on Oahu• Necropsy & histopathology – toxoplasmosis • Serology: T. gondii (1:40,960)
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RO28 “Pohaku” Days 5-14
PE Mentation slowly improved, but locomotion on land abnormal; unable to haul out of pool
CBC/Chemistry No significant changes from admit
Tx Tapered off dexamethasone, added carprofen, vitamin E, alpha lipoic acid
Protozoal titers (2wk) T. gondii 1:81,920 (Sarco & Neo: 1:80)
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RO28 “Pohaku” Weeks 2-6
Too difficult to handle for oral tubings ~week 3
Showed interest in herring offers in pool ~week 3
Developed unilateral keratopathy ~week 4
Locomotory abilities gradually improved; able to exit pool under own power ~week 4
Transferred to partner facility Ke Kai Ola ~week 4.5
Completed full 6 weeks of treatment for toxoplasmosis
Appetite poor but mentation BAR, locomotion WNL
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RO28 “Pohaku”
• Succumbed to congestive heart failure (week 10)
• Post-mortem: Chronic brain damage, relatively low #s of zoites, secondary heart effects
• It wasn’t the end we desired but we can (and will) try again
• Resource intense and not a feasible solution to the threat
• Media, web stories, podcast, plus more to come…
Cerebral necrosis
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ConclusionsToxoplasmosis appears to be acutely lethal to most HMS
• Greater impacts to female seals = population level impacts• Massive #s of organisms• Suggests high susceptibility & lack of immune response adaptation• Adipose involvement
• Likely inherent characteristic of T. gondii• Related to genotype? • Could this predispose pregnant seals?
• Are all exposed dying, or are we missing subclinical infections?
First wild HMS with acute toxoplasmosis treated in 2020
Two clusters of cases detected in 2018 and 2020
Exposure risks not immediately apparent given small sample size, diverse diet, varied movement patterns related to rainfall/runoff?
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Next steps
Risk model in development
Further examination of genotypes in HMS
Enhanced focus on health assessments, especially adult females, paired with instrumentation
"Logging” seals
Apparently healthy seals
Continued engagement with managers, stakeholders, partners
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Management challenges
Sheer number of cats• est. 50,000-300,000 on Oahu alone
Few laws, little enforcement
Characteristics of environment and population
Small but vocal group opposing management• Support measures that lack scientific foundation (e.g., TNR)
NOAA Fisheries is an ocean resource agency but protected species are facing terrestrial threats
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Optimism
Social scientists at NOAA PIFSC engaged
Interagency working group • NOAA initiated; meets quarterly
• Messaging campaign on keeping cats indoors
• Legislative actions
• Controlling the source (abandonment)
• Build trust with cat advocates to garner support for stronger measures
Long game: a lap for every cat
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MAHALO!