Abstract:

Bottlenose dolphins (Tursiops truncatus) in Barataria Bay, Louisiana (BB), were heavily impacted by exposure to oil following the Deepwater Horizon disaster. Previous studies have documented detriments to their pulmonary, reproductive, and endocrine health, however, the cardiac effects of oil on dolphins have not previously been examined. Techniques for comprehensive cardiac evaluation were refined with dolphins at the U.S. Navy Marine Mammal Program, including cardiac auscultation and echocardiography. The techniques were then utilized during capture-release health assessments in Sarasota Bay, Florida (SB), a non-oiled reference population, and in Barataria Bay, Louisiana in 2018. This dataset was compiled using prospective data from these three dolphin populations. Data was collected regarding murmur prevalence and characterization, echocardiographic findings, and electrocardiographic (ECG) findings. In addition, novel blood-based biomarkers assessed isoenzymes to identify the utility of blood-based cardiac biomarkers for cardiac evaluation in dolphins. Linnehan, Barbara K., Adonia Hsu, Forrest M. Gomez, Sharon M. Huston, Ryan Takeshita, Kathleen M. Colegrove, Teri K. Rowles, Ashley Barratchlough, Whitney B. Musser, Craig A. Harms, Veronica Cendejas, Eric S. Zolman, Brian C. Balmer, Forrest I. Townsend, Randall S. Wells, Eric D. Jensen, Lori H. Schwacke, and Cynthia R. Smith. 2020. Standardization of Dolphin Cardiac Auscultation and Characterization of Heart Murmurs in Managed and Free-Ranging Bottlenose Dolphins (Tursiops truncatus). Frontiers in Veterinary Science, 7:844 doi:10.3389/fvets.2020.570055.

Suggested Citation:

Linnehan, Barbara K., Forrest M. Gomez, Sharon M. Huston, Adonia Hsu, Ryan Takeshita, Kathleen M. Colegrove, Teri K. Rowles, Craig A. Harms, Whitney B. Musser, Ashley Barratclough, Eric S. Zolman, Brian C. Balmer, Forrest I. Townsend, Carolyn Cray, Jeanine S. Morey, Randall S. Wells, Eric D. Jensen, Lori H. Schwacke, and Cynthia R. Smith. 2020. Cardiac assessments of bottlenose dolphins (Tursiops truncatus) using auscultation, echocardiography, electrocardiography, and blood-based biomarkers. Distributed by: GRIIDC, Harte Research Institute, Texas A&M University–Corpus Christi. doi:10.7266/n7-b2h2-sm08

Publications:

Linnehan, B. K., Hsu, A., Gomez, F. M., Huston, S. M., Takeshita, R., Colegrove, K. M., … Smith, C. R. (2020). Standardization of Dolphin Cardiac Auscultation and Characterization of Heart Murmurs in Managed and Free-Ranging Bottlenose Dolphins (Tursiops truncatus). Frontiers in Veterinary Science, 7. doi:10.3389/fvets.2020.570055

Linnehan, B. K., Gomez, F. M., Huston, S. M., Hsu, A., Takeshita, R., Colegrove, K. M., Harms, C. A., Barratclough, A., Deming, A. C., Rowles, T. K., Musser, W. B., Zolman, E. S., Wells, R. S., Jensen, E. D., Schwacke, L. H., & Smith, C. R. (2021). Cardiac assessments of bottlenose dolphins (Tursiops truncatus) in the Northern Gulf of Mexico following exposure to Deepwater Horizon oil. PLOS ONE, 16(12), e0261112. https://doi.org/10.1371/journal.pone.0261112

Purpose:

Given the growing evidence regarding the cardiotoxic effects of Deepwater Horizon (DWH) oil on several species, this dataset was created to comprehensively assess the cardiac health of bottlenose dolphins (Tursiops truncatus) in the areas exposed to DWH oil. This data has successfully advanced cardiac diagnostic techniques and knowledge of wild dolphin cardiac health.

Data Parameters and Units:

Worksheet Column.header Description Wild.dolphin.info Date Date (dd-MON-yy) Wild.dolphin.info field_id Unique identifier for each dolphin in the dataset Wild.dolphin.info latitude Latitude in decimal degrees Wild.dolphin.info longitude Longitude in decimal degrees Wild.dolphin.info sex Sex of the dolphin Wild.dolphin.info age.yrs Age in years, when available, determined by growth layer group counts on extracted teeth Wild.dolphin.info pregnant Pregnancy status Wild.dolphin.info length.cm Total length in cm Wild.dolphin.info weight.kg Body weight in kg Murmur Dolphin.ID Unique identification number for each patient Murmur Exam.Date Calendar date that the examination was performed Murmur Exam.Location Location the examination was performed: BB- Barataria Bay, LA; SB- Sarasota, FL; Navy- San Diego, CA Murmur Sex Sex of dolphin Murmur Age.yrs Age of the dolphin in years Murmur Ausculting.Dr Cardiologist who performed auscultation (SMH or AH) or other veterinarian (BKL) Murmur HR.High.bpm Maximum heart rate in beats per minute during the tachycardic phase of the respiratory sinus arrhythmia Murmur HR.Low.bpm Minimum heart rate in beats per minute during the bradycardic phase of the respiratory sinus arrhythmia Murmur Rythm Heart rhythm (respiratory sinus arrhythmia (RSA), regular rhythm, or irregular) Murmur Murmur.Present Heart murmur present or absent Murmur Murmur.Type Type of murmur in relation to cardiac cycle (fixed or dynamic) Murmur Fixed.Grade If murmur is fixed, fixed murmur grade on scale of I-VI Murmur Dynamic.Low.HR.Grade If murmur is dynamic, dynamic murmur grade on a scale of I-VI during bradycardic phase of respiratory sinus arrhythmia Murmur Dynamic.High.HR.Grade If murmur is dynamic, dynamic murmur grade on a scale of I-VI during tachycardic phase of respiratory sinus arrhythmia Murmur Murmur.PMI.Location Location of the murmur point of maximal intensity Murmur Murmur.Timing Timing of murmur in relation to heart sounds (systolic or diastolic) Echo.and.ECG Dolphin.ID Unique identification number for each dolphin Echo.and.ECG Exam.Date Calendar date that the examination was performed Echo.and.ECG Exam.Location Location the examination was performed: BB- Barataria Bay, LA; SB- Sarasota, FL Echo.and.ECG Sex Sex of dolphin Echo.and.ECG Pregnant Pregnancy status of dolphin Echo.and.ECG Weight.kgs Weight of dolphin in kilograms Echo.and.ECG Age.yrs Age of dolphin in years Echo.and.ECG Echocardiogram.Performed Echocardiogram performed or not performed Echo.and.ECG Echo.type Type of echocardiogram: Transthoracic (TTE) or Transesophogeal (TEE) Echo.and.ECG Echo.by Cardiologist that performed the echocardiogram: SMH, AH or both Echo.and.ECG Rev.Rep.by Cardiologist that reviewed and reported the echocardiogram findings: SMH, AH, or both Echo.and.ECG Completeness Level of completion for echocardiogram: complete, nearly complete, partial, or none Echo.and.ECG Window.quality Quality of cardiac window for ultrasound: excellent, very good, good, fair, poor Echo.and.ECG Image.quality Quality of images obtained: excellent, very good, good, fair, poor Echo.and.ECG Rhythm.ECG Electrocardiogram on Vivid IQ echocardiogram machine performed: Yes IQ, No IQ, or NO IQ and arrhythmia suspected Echo.and.ECG Rhythm.sinus Respiratory sinus arrhythmia (sinus) or other heart rhythm as monitored on ECG during echocardiogram: sinus or N/A (no ECG Echo.and.ECG Rhythm.add.ons Other heart rhythms as monitored on ECG: N/A (no ECG), No other rhythms noted, ventricular premature contractions, atrial premature contractions, 1st degree AV block, 2nd degree AV block, 3rd degree AV block Echo.and.ECG Thoraic.effusion Presence of pleural effusion: no pleural effusion, yes pleural effusion or yes uncertain location Echo.and.ECG Pericardial.effusion Presence of pericardial effusion: no pericardial effusion, yes pericardial effusion or yes uncertain location Echo.and.ECG LA.visualized Left atrium (LA) visualized: visualized or not well visualized Echo.and.ECG LA/Ao.measured Left atrium/aorta (LA/Ao) measured: yes or no Echo.and.ECG LA.size Left atrium size: N/A, unremarkable, mild LA dilation, moderate LA dilation or severe LA dilation Echo.and.ECG LV.visualized Left ventricle (LV) visualized: visualized or not well visualized Echo.and.ECG LV.motion Left ventricular motion: N/A, unremarkable, hypodynamic mild, hypodynamic moderate, hypodynamic severe or hyperdynamic Echo.and.ECG LV.papillary Left ventricular papillary muscles: observed or not observed Echo.and.ECG False.tendons False tendons: observed or not observed Echo.and.ECG RA.visualized Right atrium (RA) visualized: visualized or not well visualized Echo.and.ECG RA.size Right atrium size: N/A, unremarkable, mild LA dilation, moderate LA dilation or severe LA dilation Echo.and.ECG RV.visualized Right ventricle (RV) visualized: visualized or not well visualized Echo.and.ECG RV.size Right ventricle size: N/A, decline to comment, unremarkable, mildly dilated, moderately dilated or severely dilated Echo.and.ECG RV.wall.thickness Right ventricle wall thickness: N/A, decline to comment, unremarkable, mildly increased, moderately increased, severely increased or decreased Echo.and.ECG MV.visualized Mitral valve (MV) visualized: visualized or not well visualized Echo.and.ECG MV.structure Mitral valve structure: N/A, structure not well visualized, unremarkable, mild, moderate or severe Echo.and.ECG MV.prolapse Mitral valve prolapse: N/A, decline to comment, no prolapse or prolapse Echo.and.ECG MV.regurgitation Mitral valve regurgitation (MR): N/A, color flow not well visualized, none, trace, small jet, medium jet, large jet or pre-systolic MR Echo.and.ECG MR.spectral.doppler Spectral doppler of mitral regurgitation: not performed/inadequate, no MR to interrogate, normal velocity or abnormal velocity Echo.and.ECG MV.inflow.doppler Mitral inflows: not performed, performed but not evaluated, normal inflows, abnormal inflows or summated Echo.and.ECG TV.visualized Tricuspid valve (TV) visualized: visualized or not well visualized Echo.and.ECG TV.structure Tricuspid valve structure: N/A, structure not well visualized, unremarkable, mild, moderate or severe Echo.and.ECG TV.prolapse Tricuspid valve prolapse: N/A, decline to comment, no prolapse or prolapse Echo.and.ECG TV.regurgitation Tricuspid valve regurgitation (TR): N/A, color flow not well visualized, none, trace, small jet, medium jet, large jet or pre-systolic TR Echo.and.ECG TR.spectral.doppler Spectral doppler of tricuspid regurgitation: not performed/inadequate, no TR to interrogate, normal velocity or abnormal velocity Echo.and.ECG TV.inflow.doppler Tricuspid inflows: not performed, performed but not evaluated, normal inflows, abnormal inflows or summated Echo.and.ECG AV.visualized Aortic valve (AV) visualized: visualized or not well visualized Echo.and.ECG AV.structure Aortic valve structure: N/A, structure not well visualized, unremarkable, mild, moderate or severe Echo.and.ECG AV.insufficiency Aortic valve insufficiency: N/A, inadequate, none, trace, mild, moderate or severe Echo.and.ECG LV.outflow Left ventricular outflow color Doppler: not performed/inadequate, laminar or not laminar Echo.and.ECG PV.visualized Pulmonic valve (PV) visualized: visualized or not well visualized Echo.and.ECG PV.structure Pulmonic valve structure: N/A, structure not well visualized, unremarkable, mild, moderate or severe Echo.and.ECG PV.insufficiency Pulmonic valve insufficiency: N/A, inadequate, none, trace, mild, moderate or severe Echo.and.ECG RV.outflow Right ventricular outflow color Doppler: not performed/inadequate, laminar or not laminar Echo.and.ECG HR-dependent.outflows Heart rate-dependent doppler variation: performed or not performed Echo.and.ECG HR-dependent.LS.outflows Left side HR-dependent doppler variation: N/A, decline to comment, increased outflow velocity associated with higher heart rate demonstrated within the left ventricular outflow/aorta (DLVOTO) or no increased velocity Echo.and.ECG HR-dependent.RS.outflows Right side HR-dependent doppler variation: N/A, decline to comment, increased outflow velocity associated with higher heart rate demonstrated within the right ventricular outflow/aorta (DRVOTO) or no increased velocity Echo.and.ECG PA.visualized Pulmonary artery (PA) visualized: visualized or not well visualized Echo.and.ECG PA.size Pulmonary artery size: N/A, main pulmonary artery (MPA) unremarkable, MPA/branches unremarkable, MPA dilated or MPA/branches dilated Echo.and.ECG AO.visualized Aorta (AO) visualized: visualized or not well visualized Echo.and.ECG AO.size Aortic size: N/A, AO root unremarkable, AO root and ascending aorta (AA) unremarkable, AO root dilated or AO root and AA dilated Echo.and.ECG Echo.Conclusions Cardiologists' main conclusions about the echocardiogram Echo.and.ECG 2D.IVSd.cm 2D echo measurement of intraventricular septum thickness at end-diastole in centimeters Echo.and.ECG 2D.LVIDd.cm 2D echo measurement of left ventricular internal dimension at end-diastole in centimeters Echo.and.ECG 2D.LVPWd.cm 2D echo measurement of left ventricular posterior wall thickness at end-diastole in centimeters Echo.and.ECG 2D.IVSs.cm 2D echo measurement of intraventricular septum thickness and end-systole in centimeters Echo.and.ECG 2D.LVIDs.cm 2D echo measurement of left ventricular internal dimension at end-systole in centimeters Echo.and.ECG 2D.LVPWs.cm 2D echo measurement of left ventricular posterior wall thickness at end-systole in centimeters Echo.and.ECG 2D.%FS 2D echo measurement of % fractional shortening Echo.and.ECG 2D.Ao.Diam.cm 2D echo measurement of aortic diameter in centimeters Echo.and.ECG 2D.LA.cm 2D echo measurement of left atrial size in centimeters Echo.and.ECG 2D.LA/Ao 2D echo measurement of left atrial dimension to the aortic annulus dimension Echo.and.ECG 2D.MPA.cm 2D echo measurement of the main pulmonary artery in centimeters Echo.and.ECG MV.E.Velocity.m/s Mitral valve, peak velocity of early diastolic transmitral flow in meters/sec Echo.and.ECG MV.Dec.Time.ms Mitral valve, deceleration time in meters/sec Echo.and.ECG MV.Dec.Slope.m/s2 Mitral valve, rate of decrease of E wave in meters/second^2 Echo.and.ECG MV.A.Velocity.m/s Mitral valve, peak velocity of late transmitral flow in meters/sec Echo.and.ECG MV.E/A Mitral valve, ratio of E to A Echo.and.ECG MV.MR.maxPG.mmHg Mitral valve regurgitation peak pressure gradient measured in mmHg Echo.and.ECG MV.MR.Vmax.m/s Mitral valve regurgitation maximum velocity measured in meters/sec Echo.and.ECG TR.Vmax.m/s Tricuspid valve regurgitation maximum velocity measured in meters/sec Echo.and.ECG TR.maxPG.mmHg Tricuspid regurgitation peak pressure gradient measured in mmHg Echo.and.ECG MM.IVSd.cm M-mode measurement of intraventricular septum thickness at end-diastole in centimeters Echo.and.ECG MM.LVIDd.cm M-mode measurement of left ventricular internal dimension at end-diastole in centimeters Echo.and.ECG MM.LVPWd.cm M-mode measurement of left ventricular posterior wall thickness at end-diastole in centimeters Echo.and.ECG MM.IVSs.cm M-mode measurement of intraventricular septum thickness at end-systole in centimeters Echo.and.ECG MM.LVIDs.cm M-mode measurement of left ventricular internal dimension at end-systole in centimeters Echo.and.ECG MM.LVPWs.cm M-mode measurement of left ventricular posterior wall thickness at end-systole in centimeters Echo.and.ECG MM.%FS M-mode fractional shortening Echo.and.ECG AV.Vmax.m/s Aortic valve peak systolic velocity measured in meters/sec Echo.and.ECG AV.maxPG.mmHg Aortic valve peak pressure gradient measured in mmHg Echo.and.ECG AV.high.PG.mmHg Aortic valve pressure gradient measured in mmHg at high heart rate Echo.and.ECG AV.high.Vmax.P.m/s Aortic valve peak velocity measured in meters/sec at high heart rate Echo.and.ECG AV.low.PG.mmHg Aortic valve pressure gradient measured in mmHg at low heart rate Echo.and.ECG AV.low.Vmax.P.m/s Aortic valve peak velocity measured in meters/second at low heart rate Echo.and.ECG LVOT.Vmax.P.m/s Left ventricular outflow tract peak velocity measured in meters/second Echo.and.ECG LVOT.maxPG.mmHg Left ventricular outflow tract peak pressure gradient measured in mmHg Echo.and.ECG LVOT.low.v.m/s Left ventricular outflow tract velocity measured in meters/second at low heart rate Echo.and.ECG LVOT.low.p.mmHg Left ventricular outflow tract pressure measured in mmHg at low heart rate Echo.and.ECG LVOT.high.v.m/s Left ventricular outflow tract velocity measured in meters/second at high heart rate Echo.and.ECG LVOT.high.p.mmHg Left ventricular outflow tract pressure measured in mmHg at high heart rate Echo.and.ECG RVOT.Vmax.P.m/s Right ventricular outflow tract peak velocity measured in meters/second Echo.and.ECG LVOT.low.HR.BPM Left ventricular outflow tract heart rate during bradycardic phase, beats/minute Echo.and.ECG PV.Vmax.P.m/s Pulmonic valve peak velocity measured in meters/second Echo.and.ECG PV.maxPG.mmHg Pulmonic valve peak pressure gradient measured in mmHg Echo.and.ECG PV.low.Vmax.P.m/s Pulmonic valve peak velocity measured in meters/second at low heart rate Echo.and.ECG PV.PR.Vmax.P.m/s Pulmonic valve regurgitation peak velocity measured in meters/second Echo.and.ECG PV.PR.maxPG.mmHg Pulmonic valve regurgitation peak pressure gradient measured in mmHg Echo.and.ECG RVOT.maxPG.mmHg Right ventricular outflow tract peak pressure gradient measured in mmHg Echo.and.ECG RVOT.high.maxPG.mmHg Right ventricular outflow tract peak pressure gradient measured in mmHg at high heart rate Echo.and.ECG RVOT.high.Vmax.m/s Right ventricular outflow tract peak velocity measured in meters/second at high heart rate Echo.and.ECG RVOT.low.maxPG.mmHg Right ventricular outflow tract peak pressure gradient measured in mmHg at low heart rate Echo.and.ECG RVOT.low.Vmax.m/s Right ventricular outflow tract peak velocity measured in meters/second at low heart rate Echo.and.ECG HeartRate.Calc.BPM Heart rate calculated from ECG, in beats/minute Echo.and.ECG TeleVet.ECG.Performed Telemetric ECG performed or not performed Echo.and.ECG ECG.Abnormal.Normal ECG rhythm normal or abnormal Echo.and.ECG ECG.Rhythm.Diagnosis Rhythm diagnosis from ECG Bloodbased.biomarkers Exam.ID Unique identification number for each blood sample analyzed Bloodbased.biomarkers Dolphin.ID Unique identification number for each dolphin in the dataset Bloodbased.biomarkers Exam.Date Date of the exam (month/day/year) Bloodbased.biomarkers Exam.Location Location the examination was performed: BB- Barataria Bay, LA; SB- Sarasota, FL; DK- Six Flags Discovery Kingdom; Navy- San Diego, CA Bloodbased.biomarkers Sex Sex of dolphin Bloodbased.biomarkers Age Age of the dolphin in years Bloodbased.biomarkers SAA Serum amyloid A (mg/L) Bloodbased.biomarkers Total.CK Total creatine kinase (U/L) Bloodbased.biomarkers CK.MM Creatine kinase - MM (U/L) Bloodbased.biomarkers CK.MB Creatine kinase - MB (U/L) Bloodbased.biomarkers CK.BB Creatine kinase - BB (U/L) Bloodbased.biomarkers Total.LDH Total lactate dehydrogenase (U/L) Bloodbased.biomarkers LD.1 Lactate dehydrogenase 1 (U/L) Bloodbased.biomarkers LD.2 Lactate dehydrogenase 2 (U/L) Bloodbased.biomarkers LD.3 Lactate dehydrogenase 3 (U/L) Bloodbased.biomarkers LD.4 Lactate dehydrogenase 4 (U/L) Bloodbased.biomarkers LD.5 Lactate dehydrogenase 5 (U/L) Bloodbased.biomarkers BNP Brain or B-type natriuretic peptide (ng/ml) Bloodbased.biomarkers ANP Atrial natriuretic peptide (ng/ml) ND indicates no data were collected for that parameter for that sample. NA indicates a given parameter was not applicable for the case at hand or the data were not analyzed.

Methods:

Auscultation techniques were refined with 65 dolphins cared for by the U.S. Navy Marine Mammal Program in San Diego, California. Fifteen of these dolphins also received partial echocardiography exams for technique development. Navy dolphins voluntarily participated in these procedures through positive operant conditioning, approved by the Navy Marine Mammal Program IACUC (NIWC IACUC #128-2018) and U.S. Navy Bureau of Medicine and Surgery (NRD-1157). Capture-release health assessments were performed on 19 free-ranging dolphins in Sarasota Bay, Florida (SB) in June 2018 as a non-oiled reference population, and 34 dolphins in BB in July 2018. Cardiac auscultations were performed in seawater. Six points of auscultation were standardized: sternal caudal, left caudal, left cranial, sternal cranial, right cranial, and right caudal. When a cardiac murmur was detected, it was graded by intensity using the conventional Grade I-VI scale. Murmurs were further characterized by the point of maximal intensity (PMI), timing of the murmur in relation to the heart sounds (systolic or diastolic), and type of murmur in relation to the cardiac cycle (fixed or dynamic). Seventeen SB dolphins and 29 BB dolphins received in-water transthoracic echocardiograms. The following standard echocardiogram images were examined: right parasternal long-axis, right parasternal short-axis, left parasternal apical, left parasternal cranial long-axis, left parasternal short-axis. 2D, M-mode, and spectral Doppler were utilized. Additionally, transesophageal echocardiograms were performed on 5 dolphins in SB. Telemetric ECG was performed opportunistically during capture-release health assessments on 16 dolphins in SB and 21 dolphins in BB. ECG data was analyzed for heart rate and presence of arrhythmias. In addition, this study examined blood-based biomarkers, including creatine kinase isoenzymes (CK-BB, CK-MB, and CK-MM), lactate dehydrogenase isoenzymes (LD1, LD2, LD3, LD4, and LD5), B-type natriuretic peptide (BNP), and atrial natriuretic peptide (ANP) on both managed dolphins and wild bottlenose dolphins. All blood samples were collected from the peripheral periarterial venous rete on the ventral fluke or caudal peduncle via voluntary presentation or manual restraint. Samples obtained from the fluke or peduncle were collected using a 22-gauge butterfly needle or a 20 / 18-gauge 1.5-inch needle respectively, attached to a vacutainer collection system. Blood was collected into BD serum separator tubes for analysis (BD, Franklin Lakes, NJ). Serum separator tubes were chilled for a duration of approximately 30 minutes and centrifuged within 2 hours at 21°C for 10 minutes. Banked serum samples were stored at -80°C. Analysis was performed at the University of Miami Acute Phase Proteins Laboratory (Miami, Florida) adapting commercially available ELISA-based assays for SAA, BNP and ANP and commercially available electrophoresis kits for CK and LDH isoenzymes.

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