ABDOMINAL SPLANCHNIC HAEMODYNAMICS IN A CANINE NORMOVOLAEMIC ANAEMIA MODEL AND UNCOMPLICATED CANINE BABESIOSIS: A COMPARATIVE DOPPLER STUDY. A thesis submitted to the Faculty of Veterinary Science, Onderstepoort University of Pretoria in fulfilment of the requirements of the degree of Doctor of Philosophy. By Lee Martin Palia Koli Koma BVM, Makerere University, 1980 MPhil, University of Edinburgh, 1984 March 2005
DECLARATION I, Lee M.P.K. Koma, do hereby declare that, neither I nor any other scientist has previously submitted this thesis that I am submitting to the University of Pretoria for the degree of Doctor of Philosophy, to any other university for a degree, either in part or as a whole. My promoters Prof. R.M. Kirberger, Head of the Section of Diagnostic Imaging, Prof. P. Bland van den Berg, Director of Clinical Services, Onderstepoort Veterinary Academic Hospital, and Prof. L. Scholtz, Head of the Department of Radiology, Pretoria Academic Hospital bear testimony to this. Signed this... day of in the year of our Lord.... Lee M.P.K. Koma Prof. R.M. Kirberger.. Prof. P. Bland van den Berg. Prof. L. Scholtz ii
Dedicated to my dear wife Berna, daughter Jocelyn, and sons John and Collins. I am indebted to your patience and tolerance of my long periods of absence. iii
ACKNOWLEDGEMENTS I am deeply indebted to Makerere University, and the Department of Companion Animal Clinical Studies of the Faculty of Veterinary Science, University of Pretoria who provided the funding that made it possible to accomplish this study. I would like to thank Siemens, South Africa, for providing a substitute ultrasound machine for the routine clinical work of the Section of Diagnostic Imaging during the period of this investigation. I am grateful to my promoter Prof. R.M. Kirberger, co-promoters Prof. L. Scholtz and Prof. P. Bland van den Berg, and research advisors Prof. A.L. Leisewitz and Dr. L. Jacobson for their guidance throughout this study. I wish to thank my co-worker Dr. T.C. Spotswood, all the staff and students of the Sections of Diagnostic Imaging, Small Animal Medicine, Clinical Pathology, Animal Blood Bank, Outpatients and Pharmacy for their co-operation and assistance. I am grateful to Dr. P.J. Becker of the Medical Research Council for his advice, and for performing the statistical analysis. Finally, I wish to express my gratitude to Prof. P. Stadler, Head of Department of Companion Animal Clinical Studies, Mrs. L. Oberholzer and Mrs. P. Bester of the Office of the Head of Department for their various roles in facilitating the smooth accomplishment of my PhD programme at the Department. iv
TABLE OF CONTENTS Title page i Declaration ii Dedication iii Acknowledgements iv List of figures vi List of tables vii Abstract (English) viii Abstract (Afrikaans) x Chapter 1. General introduction 1 Chapter 2. Literature review 11 Chapter 3. Influence of normovolemic anemia on Doppler characteristics of the abdominal aorta and splanchnic vessels in Beagles 63 Chapter 4. Doppler ultrasonographic changes in the canine kidney during normovolaemic anaemia 98 Chapter 5. Influence of normovolaemic anaemia on Doppler-derived blood velocity ratios of abdominal splanchnic vessels in clinically normal dogs 121 Chapter 6. Comparison of effects of uncomplicated canine babesiosis and canine normovolemic anemia on abdominal splanchnic Doppler characteristics A 142 preliminary investigation Chapter 7. General discussion 176 Chapter 8. Summary 180 Appendix A. A canine normovolaemic acute anaemia model 182 Appendix B. Selection of uncomplicated canine babesiosis cases 206 v
LIST OF FIGURES Figure 3.1 Splenic thickness during physiological and anaemic states 74 Figure 3.2 Heart rate during physiological and anaemic states 75 Figure 3.3 Doppler spectrum of the abdominal aorta in a clinically normal Beagle 79 Figure 3.4 Doppler spectrum of the abdominal aorta of a Beagle during severe anaemia 80 Figure 3.5 Blood flow velocities of various vessels during physiological and anaemic states 81 Figure 3.6 Vascular resistance indices of various vessels during physiological and anaemic states 82 Figure 4.1 Doppler spectra of the left renal artery during physiological and anaemic states 109 Figure 4.2 Doppler spectra of a renal interlobar artery during physiological and anaemic states 110 Figure 5.1-5.3 Doppler spectra of the abdominal aorta, coeliac artery and left renal artery during physiological and anaemic states 130 Figure 6.1 Resistive index of various vessels during physiological and anaemic states, and uncomplicated canine babesiosis 154 Figure 6.2 Pulsatility index of various vessels during physiological and anaemic states, and uncomplicated canine babesiosis 157 Figure 6.3 Peak systolic velocity of various vessels during physiological and anaemic states, and uncomplicated canine babesiosis 158 Figure 6.4 End diastolic velocity of various vessels during physiological and anaemic states, and uncomplicated babesiosis 160 Figure 6.5 Time-averaged mean velocity of various vessels during physiological and anaemic states, and uncomplicated babesiosis 161 Figure A.1 Daily mean haematocrit values of Beagles during the study period 194 Figure A.2 Predicted and actual blood volumes withdrawn to achieve a desired haematocrit in individual Beagles 196 vi
LIST OF TABLES Table 2.1 Ideal imaging requirements for B-mode and Doppler modalities 22 Table 3.1 Heart rate and Doppler variables during physiological and anaemic states 77 Table 4.1 Linear dimensions of the left kidney during physiological and anaemic states 107 Table 4.2 Heart rate and renal Doppler variables during physiological and anaemic states 108 Table 5.1 Comparison of peak systolic velocity and peak systolic velocity ratio between vessels during physiologic and anaemic states 131 Table 5.2 Comparison of time-averaged mean velocity and time-averaged mean velocity ratio between vessels during physiologic and anaemic states 132 Table 5.3 Comparison of end diastolic velocity between vessels during physiologic and anaemic states 133 Table 5.4 Comparison of peak systolic velocity ratio and time-averaged mean velocity ratio within vessels during physiologic and anaemic states 134 Table 6.1 Haematocrit, heart rate, and total serum protein, creatinine and urea levels in uncomplicated canine babesiosis, experimentally induced normovolaemic 152 anaemia, and the physiologic state Table 6.2 Resistance indices of various vessels during physiological and anaemic states, and uncomplicated canine babesiosis 155 Table 6.3 Blood flow velocities of various vessels during physiological and anaemic states, and uncomplicated canine babesiosis 159 Table 6.4 Velocity ratios and blood flow of various vessels during physiological and anaemic states, and uncomplicated canine babesiosis 162 Table B.1 Arterial numerical data 213 Table B.2 Venous numerical data 214 Table B.3 Arterial descriptive data 215 Table B.4 Venous descriptive data 216 vii
ABSTRACT This study compared uncomplicated canine babesiosis (CB) with various grades of experimentally induced normovolaemic anaemia (EA) and the physiological state (controls) in the dog using Doppler variables of the abdominal aorta and splanchnic vessels. There were 14 cases of uncomplicated CB, and each EA and control group had 11 Beagles. There were significant increases in the abdominal aorta, cranial mesenteric artery, coeliac artery and main portal vein blood flow velocities, and in portal blood flow during EA when compared with the physiological state. There were significant reductions in resistance indices of the same vessels, and those of the hilar splenic artery. Changes were most notable during severe EA and less consistent during lower grades of anaemia. Significant changes in renal haemodynamics were found only during severe acute EA. In contrast to other abdominal vessels, left renal artery pulsatility and resistive indices increased significantly during EA while those of the interlobar artery remained unchanged. There was a significant increase in peak systolic velocity and significant decrease in end diastolic velocity. Renal artery time-averaged mean velocity (TAV mean ) (P 0.008) and end diastolic velocity (P 0.041) were significantly lower than the corresponding variables of the aorta, cranial mesenteric and coeliac arteries during the EA but not the physiological state. The TAV mean ratio was significantly (P = 0.014) lower during EA when compared to the physiological state, and significantly (P 0.004) lower than the corresponding variables of cranial mesenteric or coeliac artery during the EA but not the physiological state. viii
There was a striking similarity between CB and EA regarding haemodynamic change patterns of Doppler variables in all vessels. In spite of this, renal resistive indices during CB were significantly higher than during EA and the physiological state. The similarity between CB and EA haemodynamic patterns is attributed to anaemia while significant differences between them may be attributable to pathophysiological factors peculiar to CB. This observation supports the view that CB impairs renal circulation through certain mechanisms such as capillary blockage with sequestered red blood cells. Doppler ultrasonography is a useful technique for clinical investigation of haemodynamics in CB and related diseases. Key terms: anaemia, canine babesiosis, abdominal splanchnic haemodynamics, Doppler characteristics ix
ABSTRAK Die doelwitte van hierdie studie was om die Doppler veranderlikes van die abdominale aorta en splankniese bloedvate te vergelyk tussen eksperimentele normovolemiese anemie (EA), ongekompliseerde babesiose in honde (CB) en ook teenoor die normale fisiologiese status in kontrole honde. Doppler veranderlikes van die abdominale bloedvate gedurende die normale fisiologiese status en verskillende grade van eksperimentele anemie is gemeet in 11 klinies normale Beagles, en in 14 honde met ongekompliseerde babesiose. Daar was betekenisvolle verhogings in die bloedvloeispoed van die abdominale aorta, kraniale mesenteriese slagaar, koiliak slagaar en die hoof portale aar en in die portale bloedvloei gedurende EA in vergelyking met die kontrole groep. Daar was betekenisvolle verlagings in die weerstands indekse van dieselfde bloedvate en van die milt hilus slagaar. Veranderinge was mees merkbaar gedurende erge EA en minder gevorderd gedurende ligter grade van anemie. Betekenisvolle renale hemodinamiese veranderinge is alleenlik gedurende erge akute anemie gevind. In kontras met ander abdominale bloedvate het die pulseer en weerstandsindekse van die linker renale slagaar betekenisvol verhoog gedurende EA terwyl die van die interlobêre slagaar onveranderd gebly het. Daar was betekenisvolle verhogings in die piek sistoliese bloedvloeisnelheid en betekenisvolle verlagings in die eind diastoliese vloeisnelheid. x
Renale slagaar tyd-gemiddelde mediane vloeisnelheid (TGMB) (P 0.008) en eind diastoliese vloeisnelheid (P 0.041) was betekenisvol laer as die ooreenkomende veranderlikes van die aorta, kraniale mesenteriese en koiliak slagare gedurende anemie, maar nie in die kontrole honde nie. Die TGMB verhouding was betekenisvol laer (P 0.014) gedurende anemie in vergelyking met die kontroles, en betekenisvol laer (P 0.004) in vergelyking met die ooreenstemende veranderlikes van die kraniale mesenteriese en koiliak slagare gedurended anemie, maar nie in die kontrole honde nie. Daar was n merkbare ooreenkoms tussen CB and EA hemodinamiese neigings met betrekking tot alle Doppler veranderklikes vir alle bloedvate. Ondanks hierdie enersheid het CB betekenisvolle verhogings gehad vir die renale weerstandsindeks teenoor EA en die kontrole groepe. Die algemene hemodinamiese neigings gedurende CB en EA mag toegeskryf word aan die anemie terwyl die verskille toegeskryf kan word aan spesifieke CB patofisiologiese faktore. Hierdie waarnemings ondersteun die opinie dat CB renale bloedvloei belemmer word deur verstopping van kapilêre bloedvate deur gesekwestreerde rooibloedselle. Doppler ultrasonografie is n handige tegniek vir kliniese ondersoeke van die hemodinamika van CB en soortgelyke siektes. Sleutel woorde: anemie, honde babesiose, abdominale splankniese hemodinamika, Doppler eienskappe. xi