may account for the removal of homologous References transfused cells that may contain subtle foreign 1.Love, J. l. and Wiygul, G.: Free Amino Acids In Plasma, Red antigens (altered cells) undetectable by existing Cells and Anaplasmata of Parasitized Calves. Comp. Biochem. Phy-ioL, 30, (1969): 923-929. - serologic tchniques. 2. Darre, D. L, Wallace. W.R.and Dimopoullos, G. T.: Evidence of Lactate Dehydrogenase in The apparent reduced susceptibility of HbF cells Anaplasma marginale. J. Blacteriol., 93, (1967): 806-810. - 3. to A. marginale infection opens a field of F. R. and Dimopoullos, G. T.: Demonstration of an Autoantibody Cox. interesting speculation regarding strain resistances Associated with Anaplasmosis. Am. J.Vet. Res., 33, (1972): 73-76. - 4. Schroeder, W. hinging on cellular components such a hemoglobin F. and Ristic, M.: Blood Serum [-actor Associated with Erythrophagocytoss in Calves with Anuplusmosis. types, enzymatic factors, ion makeup, etc. Am. J. Vet. Res., 29, (1968): 1991-1995. - 5. listic, St. Lykins, The continuing reports of new data in the area D. and Morris, 11.R.: Anaplasmosis Opsonins and llernaglutinirn J. Etiology of Anemia. Exptl. Parasit., 31, (1972): 2-12. in of immunopathology is encouraging to the research - 6. Anderson, I. L., et al.: Anaplasnla marginale: Hemoglobin Patterns community and with each comes a more complete in Experimentally Infected Young Calves. Exptl. Parasit., 32, understanding of the pathogenesis of the disease (1972): 265-271. - 7. Williams, Transfusions During Patent llovine E. 1. and Jones, E. W.: Blood through reevaluation of previously obtained data. 29, (1968): 703-710. Anaplasmosis. Am. J. Vet. RCL, Observations During Concurrent Anaplasmosis and Babesiosis in Experimentally Infected Calves D. E. Corner, D. V.M., M.S., and L. G. Adams, D. V.M., Ph.D. DepartmentofPathology and the Institute of Tropical Veterinary Medicine College of Veterinary Medicine Texas A&M University College Station, Texas 77843 Introduction Other investigatord, studying concurrent infection Thte common distributinn of anaplasmosis and in experimentally infected splenectomized calves, babesiosis and the high incidence of concurrent reported that only one of the hemoparasites infection of cattle with Anaplasma and Babesia established the normal expected parasitemia (16). species has been noted by numerous investi- The invasion of erythrocytes by the second gators (5,6,14,15,17,24,26). In many tropical hemoparasite, though initially substantial, decreas and subtropical regions, the high incidence of ed and occasionally ceased prematurely. It was concurrent infection has resulted in the standard suggested that a non-antibody inhibiting factor procedure of premunizing cattle against both of may have been produced which allowed the the diseases (14,15,26,29). Descriptions of the hemoparasite with the highest established para clinical course and pathological manifestations of sitemia to prevail while further infection of concurrent infection have been few. Simultaneous erythrocytes by the second organism was inhibited. premunization against both ,naplasmosis and Splenectomized calves infected with B. bigemina babesiosis was reported to produce an intense during the convalescent stage of anaplasmosis were anemia (6). The severity of the anemia was reported to have abnormally low Babesia para attributed to the additive effect of the individual sitemias and a prepatent period which was from 16 anemias caused by each of the hemoparasites. to 21 days longer than that normally observed for Supported by linancial assistance from the Agency for International Development and The Rockefeller Foundation. The work was done babesiosis (27). at the Laboratorio de Investigaciones The common distribution of anaplasmosis and Colombia, with the Medicas Veterlnarias I Bogota, support and coopcrition of The Instituto babesiosis and the high incidence of concurrent Colombiano Agropecuario. disease has indicated that a clearer understanding 60 of the relationship of the two disease agents during technique using cellulose acetate membranes (4). concurrent infection is desirable. The purpose of Serum glutamic oxalacetic transaminase (SGOT) this investigation was to describe the clinical activity was measured by a kit procedure* course, serological response and pathological modified from the original method (19). Serum manifestations of concurrent infection in intact soibitol dehydrogenase (SD) activity was measured calves experimentally infected with A. marginate by a modified kit procedure** adapted from an and B. bigcmina and to study the relationship of original method (7). Serum biirubin concentra the two organisms during the concurrent infection. tions were determined by a modification of the hi.tcniak and hicihods Van den Bergh procedure (8). Twenty-two, male, non-splenectomnized, Serum samples were screened for the presence of Holsteii .-Friesian calves seven months of age and complement fixing (CF) antibodies for A. free of previous or current Anaptusna and Babesia marginale by the standardized CF test for feon preousedcuor erenAntal andmal. T anaplasmosis (2). The CF test employed to detect infection were used as experimental animals. The calves were randomly divided into four groups. antibodies against B. bigemina was a previously decidmofcaon(5ofnorgaletd Groups I and 11 each contained three calves and described modification (25) of an original method Groupsed and ach cont hrcalves and ainedroup (12). All serum samples found to be positive by the served as control groups for anaplasmosis and screening procedures were titrated by a micropro babesiosis, respectively. Groups III and IV each cedure technique (9). Antigen used in the CF test contained eight calves. The calves of Group III for anaplasmosis was obtained from the United were infected on day 0 with A. marginate. States Department of Agriculture. Antigen used in Following recovery from acute anaplasmosis, the the CF test for babesiosis was obtained by a calves were infected with efect f B. bigemina cocurent stud th asecndar and served to previously reported technique using a distilled study the effect of a secondary concurrent water extract of the parasite suspension (13). infection with B. bigemina in calves recovering Rib bone marrow specimens were collected by from anaplasmosis. The calves of Group IV were biopsy from two calves from each of the four infected on day 0 with B. bigemina. Following groups of calves on days 0, 50, 90 and 120 of the recovery from infetedwit acute babesiosis, the calves were argnaiA.andb~lvedto sudythe vestigation. Myeloid:erythroid (M:E) ratios were infected with A. marginaeand, rved to study the determined. effect of a secondary concurrent infection with A. in clve rombabsiois.Two reoveing Trmind.concurrently infected calves from each of marginate iGroups III and IV and a non-infected control calf Stabilates prepared from purified Colombian were euthanatized by electrocution and submitted isolates of A. marginate and B. bigemina were used to gross and histopathological examinations. in the investigation. Each calf was infected by the subcutaneous inoculation of stabilate which was Results thawed in a water bath at 380 C for one minute. The clinical manifestations of infection were The Anaplasma inoculum contained approximately most severe in the concurrently infected calves, less 9.5 x 108 marginal bodies and the Babesia severe in the Anaplasma controls and least severe in inoculum 10.5 x 108 organisms. the Babesia controls. The clinical signs of infection consisted of increases in rectal temperature, The body weight of each calf was determined on inactivity, dull haircoats and poor body condition. day 0 and at the termination of the investigation Mean total weight gains and average daily gains and the mean total weight gains and average daily were moderately lower in the concurrently gains for each group of calves was -letermined. infected calves than in the Anaplasma controls and Blood and serum samples were collected and rectal markedly lower than in the Babesia controls (Table temperatures determined twice weekly from each 1). calf for two weeks prior to infection and for 17 Decreases in the mean PCV were more marked weeks following infection, in the concurrently infected calves than in the Packed cell volumes (PCV), reticulocyte counts control calves (Figure 1). Mean low PCVs of 13% and total and differential leukocyte counts were and 20% were observed in the calves concurently determined by tandard hlboratory procedures infected with B. bi.g,,ia and A. marginate, (23). The perc(ntage of parasitized crythrocytcs r(.pectively, as compared to mean low values of 'vns determined by the microscopic examination of 27% and 22% in the Babcsia and Anaplasma Gicmsa stained thin blood smears. Total serum control groups. protein (TSP) concentrations were ascertained using a hand held refractometer (3). Serum protein *Sigma Chemical Co., St. Louis. MissourL dectrophoretic patterns were determined by a "Sina Chemical Co.. Si. Lous, Misouri. 61 Table 1 initial and final wdghts with total weight Pins and averap daily ' . pins of the four groups of calves bigemin. Anaplame margiale and/or Babesi experimentally Infected with Group meant and o"'*. ["uJ''l:" standard deviations from the mean are presented.j (' " cow" ~ 8.i.i .0 . C 1- s P , w . .161.1 V. 10 0 !( b .) b• 1.o Y itiI . 10l~ 0 1 . ) IV l).t~ .g Ci. 1.e1 C 4 6 . . 4.2 ) .1 Itol ". O., e fl j ipMSI % ,q I ~llf t , I Il~~..* 1 2. • ,, i~e • i 4iSe -i II I hutM 6.2)t hill$ 322 8 O.21h0.l 164,2W all2 h 14n1 " .lJsO. ,i J i 22622 1112116 24ei, ~iP-P. ft- .6 4222 .264,.22 Ie t.tl -U*" IHO So. 441 ".44.o. Wi 62 22 eOW R°greZ Te ercntde ofpans/rted rybrcyzs fite ou goups of calves cx pea$lmenfgailyl(I inece wihAnpamamrgnl and/orBabes/a bigemina. Group means are presented and vertical ?' * lnes represent range. Encircledletters Indicate lime ofsubcutaneous ________________ nocutlation withAnaplasmna marginaale or wit/h Babeuia bigenaina J ' calves. A moderate monocytosis occurred in each ? of the four groups of calves. i "The " ,, changes which occurred in the SGOT, serum SD and serum bilirubin concentrations were not , significantly different between the concurrently J infected and the control calves. ? ? The M:E ratio steadily decreased in each of the Z [,1 , four groups of calves and was substantially lower, J-- ,,,,, , ,at the termination of the investigation, in the T- concurrently infected calves than in the control ,9 1calves. The number of reticulocytes was observed .. .... . ..... .... ... to increase moderately higher in the concurrently '*' infected than in the control calves. Flgwe) . Fluctuation, in thac pocked ce/i volumes of tiae fow' 570 ups Total serum protein concentrations increased Of calves experimentally infected with Alnaplasma marginnle and/or sutailyhgerntecournlynftd ttabes/a bigem i a ,Group teans are presented mld vertical lines su ta ial h g er n th co ur n ly nf t d represent ranag. .n7circtcd tetten iadicate time of sabcutanaeoaas and in the Antaplasmna control calves th~an ;n the inoculation! wit/a 1Aaaptazaau ,,wrgitaak or wit/a /Jabwiia lic'ahta. Babe, i° controls. 'lhl avernge serum albumin concentration and thre A:G ratio decreased in each Significant increases in the mean number of of the four group)s of calves with little difference infected erythrocytes were observed in the occurring between the concurrently infected and concurrently infected calves (Figure 2). Mean the control calves. maximum parasiternias of 1.0% and 2.2% were Serum globulin concentrations increased in each observed in the calve~s concurrently infected with of the four groups of calves and were substantially B. bigetnina and A. mnargitraIt, respctively, while higher in the concurrently infected and in the the mean maximum J)arasitemias observed in) the Anaplasmna controls than in the Ilabesia controls Jiabe, ia and Anuluhsnia controls were 0.06%, and (Figure 3). 1.4%, respectively. Significant differences in the mean maximum No differences occurred in the total number of CF antibody titers between the concurrently leukocytes n)or in the differential leukocyte counts infected and the control calves were not observed between the concurrently infected und control (Figure 4). Mean maximum CF titers of 1:100 and 62 calves concurrently infected with Babesia were • -:150 and 1:170. re. pectively. Gross lesions observed in the concurrently 1:* '. 4 infected calves which were euthanatized for dissection included: an excessive amount -)f cler ... yellow fluid in the peritoneal and pleural cavities; moderate splenomegaly with prominent malpighian follicles; moderate hepatomegaly and lymph node enlargement; and the occasional serous atrophy of depot fat. I "'--,- Tissue sections from the concurrently infected calves were grouped together by organ and ... examined microscopically: Liver. Slight to moderate centrolobular degen eration of the hepatocytcs was obsr.-rved. A slight to moderate infiltration of lymphocytes and reticulondoth'liial ccllm wm observcd in the peripor1d areas. The hepatic sinusoids contained . .an excessive number of mononuchnr inflammatory cells and immature nucleated erythrocytes. iR J. 77,,onc,,,a,,,,, of alpho. hla and pi,,a s,'o,, c Kupffer cell hypertrophy, erythrophagocytosis and Wiabul/s of the lor grnoti, of co'h-cx orplerhntistaly litcled 1 lh Alnaplaiaa ,narglnak ahml/or Iah'.ia hlgncuoia. ;roup nrm tiare phagocytized granules of hemosiderin were occa p a hfrieiuld 'd 'rlehal !hia'n'prcinil rmuge. E'clrdeld let'er Indlcatc linie of subaitai'us hionslollost wills Am~plame sionally observed. Irdkai or witho siia h igent lola. Kidney. An cosinophilic proteinaceous material was observed in Bowman's capsule and in the , lumens of the renal tubules. A slight infiltration of lymphocytes and plasma cells was occasionally ": l ,observed in the interstitial tissues. Phagocytized hemosiderin granules were occasionally seen in macrophages in the glomerular tufts and in the "" b,-- Iinterstitium. IN. .. ,.. Spleen. A moderate to marked lymphoid hyperplasia of the malpighian corpuscles was commonly observed. Hyperplasia of reticu loendothelial cells in the red pulp was observed in some sections. Granules of phagocytized hemosiderin were observed in the sinuses of all sections. Lymph Nodes. A histological examination was conducted on tissue sections prepared from the I\ suprapharyngeal, prescapular, prefemoral, sternal, .j]''' . bronchial, renal and mesenteric lymph nodes. The microscopic abnormalities observed were similar irregardhess of which of the lymph nodes was . 0: .0 M.................examined. Moderate hyperihksia of the lymphoid Ftiprc 4. Coraplen,jtirinx .muiho-', filers of the jiurgroups of follicles was o)served in all sections, with marked ralhes ,xpenmnctally imJfefeld with Anaplasita mrginale and/ar hY )perplasia hvilag observed in several sections. a. Babehsm higri,' (;tup nicapitare t1'raeited and iertical lines llyperplasia of reicinloendothclial cells was occa f¢lrcsat-a rana'. nrdekd leters indicate tsi',e of saibrulaicoiss Innrilaii', with Analdeto marginale or with Ilabeia bhicrmina. sionally obs.erved. Graniuls of phagocytized heinosiderin wcre present ir, several sections. 1:140 were ob.served in the Anaphstat controls Sections of tissue.; from the lung, cerebrum, nnd calves concurrently infected with Anaplastn, cera'hllum, adrenal and thyroid glands were also respectively. The mean maximum CF antibody examined. 'hllemicrorcopic alnormahities observed titers ob.served in tl, Babesia controls and the were tlight and inconsistent and were not 63 considered to have resulted from Infection with A. serum globulins which occurred in the concurrent. margnaleor with . bigemina. ly infected calves was due to an additive effect of Vcussloa both infections with the Anaplasma infection being The increased severity of the efinical signs and predominately responsible. the more pronounced reductions in to''.d weight The decrease in A:G ratio which occurred in gains and average daily gains observed in the each of the four groups was attributed to the concurrently infected calves were apparently due increase in the gamma globulin concentration to the combined effects of the Anaplasma And associated with antibody production and to the Babesia infections. The mild clinical signs and F.mall decrease in serum albumin concentration. reductions in weight gains which occurred in the The concurrently infected calves developed CF Babesia control group suggested the severity of the antibody ters against A. marginale and against B. clinical disease observed in the concurrently bigemina which were considered to be independent infected calves was predominately due to infection of the concurrently infecting organism. with A. marginale. The calves The severity of the anemic condition which infectedgross lesions the same as thoseconcurrently were observed in the described as ocurgdrignactaapsmss(,12) occurred in the concurrently infected calves was occurring during nonacute anaplasmosis (11,21,22) considered to have resulted from the combined or during nonacute babesiosis (11,20). The effects of the Anaplasma and Babesia infection presence of transudates in the major body cavities with the Anaplasma organism being predominately was considered to have been associated with a responsible. y decrease in the osmotic pressure of the blood due The significant increase in the number of to decrease in loss albumin concentration and Thethe moderate serumof albumin via the kidneys. infected erythrocytes in the concurrently infected the presence of proteinaceous material in Bow. calves was an unexpected observation. Several the psen ofd ternal tubul in the authors reported that exacerbations of anaplas- man's casule and in the renal tubules indicated the mosis may result from intercurrent infections probable loss of albumin via the renal pathway. placing additional stress on the reticuloendothelial Splenomegaly, lymph node enlargement and the system of the host (11,18). The ability of the moderate to marked lymphoid hyperplasia ob reticuloendothelial system to remove infecting served in the malpighian corpuscles of the spleen organisms may have been moderately reduced in and lymphoid follicles of the lymph nodes were con the concurrently infected calves allowing the sidered to be indicative of a responding reticuloen. secondary infecting organism to reach substantially dothelial system. higher levels in the peripheral blood. The moderate degenerative changes observed in The moderate monocytosis observed in each of the hepatocytes in the centrolobular areas of the the four groups of calves was considered to have liver were attributed to hypoxia associated with been associated with the removal of damaged the anemic condition of the calves. The degenera. erythrocytes, erythrocytic debris and infecting tion of hepatocytes during anaplasmosis was organisms. previously reported to be the result of a hypoxic The presence of reticulocytes in the peripheral condition resulting from anemia (1,10,22). blood and of nucleated erythrocytes in the hepatic The presence of hemosiderin granules within sinusoids along with non-significant changes in the macrophage in the spleen, plomerular tufts, lymph total and differential leukocyte counts indicated nodes and in the Kupffcr cells ofete liver was the decrease observed in the M:E ratio was due to atrotes an the ssee tc tion of an increase in the number of cells of the erythroid eqthrocytes and tie subsequent accumulation of series. The more prolonged and severe anemic erythrocytic debris. condition of the concurrently infected calves Cwduiunu probably acted as a more intense stimulus resulting The clinical and pathological manifestations of in the M:E ratio being substantially lower in the disease were considered to have been more severe concurrently infected than in the control calves. in the concurrently infected culves than those The elhvation in '11l' observed in each of the observed in the singularly infectid controls. four groups of calves was attributed predominately Infection with A. marginaleapparently contributed to an increa.,se in the concentration of the serum more to the severity of the cow'urrent infection gumlnu glolbulin fraction. IncreaLses in 'TSI' and than did infection with Bi. bigcia. Neither an serum globulin concentrations were higher in the inhibitory nor a synergistic effect between the Anuplasmia controls than ini the Babesla colitruls Infecting organisms wis evident during the suggestiiig te substantial Increase in 'ISI1 and Investigation and the relationship of the organisms 64 during the concurrent infection was one of Santa Gcrtnidis Cattlc Against Piroplasma spp. and AAplama independency. The increased severity of the rm'isale. Pliipping J. Anim. Ind., 23-1/4, (1962): 1-20. - 7. Gerlach, U.: Zur Klinischen Bedcutung der Aktiviislmessung von concurrent infection was attributed to the Sobiltdehydrogcnase In Menschlichcn lutserum. Kin. Wschr., 37, concurrent infections being additive. (1959): 93-98. Adapted by Sigma Chemical Co. as Tech. Bulletin No. 50-U.V., St. Louis, Mo., 1965. - 8. Gibson, R. I. and Summary Goodrich, G. E.: Dcterminat;on of Plasma Itilirubin; A Modified Van den Bergth Procedure. Proc. Soc. l.xp. Biol. Mcd., 31, (1934): The clinical, serological and pathological 413415. - 9. IliJalgo, R. J. and Dimopoullo% G. T.: Complement manifestations of disease in intact calves concur- vi,ation Microprocr.durcs for Anaplasmosis. Am. J.Vet. Res., 28, rently infected with Anaplasma marginale and (1967): 245-251. - 10. Jones, 1. W. and Brock, W. E.: Bovine Anaplasmosis. Its Diagnosis, Treatment and Control. J.A.V.M.A., Babesia bigemina were investigated. Clinical signs 149, (1966): 1624-1633. - 11. Jubb, K.V. F. and Kennedy. P.C.: were more severe in the concurrently infected Pathology of Domestic Animals. Vol. 1, 2nd cd. Academic Press, calves than in singularly infected controls. New York, N.Y., 1970. - 12. Mahoney, D. F.: Bovine Babcsiosis: Diagnosis of Infection by a Complement Fixation Test. Austral. Decreases in packed cell volume, albumin:globulin Vet. J., 38, (1962): 4-52. - 13. Mahoncy. D. F.: Bovine ratio, myeloid:erythroid ratio and increases in the Babesiosis: Preparation and Assessment of Complement Fixing number of reticulocytcs, total serum proteins and Antigens. Exp. Parasite', 20. (1967): 232-241. - 14. Malson. It. A.: Cont11rul of Anilnsmosis, Iltabesiosis nd "hcilcrisis in Rhdcsia. erum gainina globulins were more proniounced ii hill. Off. Il. .l:i,., 64, (1965): 465A76. 1 IS. Mkus, C. I'., tWe concturrt'lntly infected cailv. The cotncurrn t Garcia, F. M. mid )nri, It. A.: Control ol I'l~inla~muis in Infections had no al,parcnt effect on the Viictuicla. Accliuatl/ailon, Nutrition. aoid IPrcuunition of Im11port ed Cattle. Dull. Off. ht. EIplz., 64, (1965): 493-517. - 16. Orcllana, production of complement fixing antibodies. Gross V. M. and Brock, W. I-.: invcsligaciones Sobre Anaplasmosis y lesions observed in the concurrently infected calves Piroptasmosi. Rev. Fac. Vet. Med. y ZooS., 2, No. 4, Universidad de included: pleural and peritoneal transudates; San Carlos, Guatemala, (1969): 69-75. - 17. Otte, L. and Kiltz, II. I!.: Tick Borne Diseases in Imported Cattle. 1. Vaccination Against splenomegaly; hepatomegaly; and moderate lymph Anaplasmosis with A. centralc. i. Infection with B. argentina and node enlargement. Histological lesions included: E. wernyonL Mem. Coll. Agric. Natn. Taiwan University, 9, No. 2, moderate hepatocellular degeneration; lymphoid (1968): 2440. - 18. Patnaik, M. M.: A Note on Bovine Anaplasmosis. Indian Vet. J., 40, (1963): 655-657. - 19. Reitman, hyperplasia in the spleen and lymph nodes; at. s. and Frankel, S.: A Colonmetric Method for the Determination or hemosiderosis of the spleen, lymph nodes, liver and Serum Glutamic Oxalacetic and Glutamic Pyiuvic Transaminases. kidneys. The relationship of A. marginale and B. Am. J. Cin. Path., 28, (1957): 56-63. - 20. Rick, R.F.: iBabesiosis. In Infectious Blood Diseases of Aan and Aninals. Vol. II. Ist d. bigemina during the concurrent infections appear- Edilcd by D. Weiman and M. Rislic. Academic Press,. New York. ed to be one of independency. The increased N.Y., (1969): 219-268. - 21. Ristic, M.: Anaplauno-is. In sveryofclinical and pathological signs of the Infectious Blood Diseases of Alan and Animals. Vol. II, 1st ed. severity odited by D.Weiman and M. Ristic. Academic Prcss, New York. disease in the concurrently infected calves was N. Y., (1969): 443-542. - 22. Riqtic, M.and Sippel. W.L.: IEffcct attributed to the concurrent infections being of Cortisone on the Mechanism of Anaplasma Immunity in additive. Experimentally Infected Calve%. II. Study of Patlholugical Changes. Am. J. VcL Res., 19, (1958): 44-50. -- 23. Schalm. 0. W.: Veterinary Hematology. 2nd cd. Lea and Febiger. Philadelphia, Pa. References 1965. - 24. Seddon, II. R.: Disease of Domestic Animals in I. Allbritton, A. R. and Seger, C. L: The Transport and Australia. Part 4, 2nd ed. Service Pub. No. 8, Dept. of 111th. Ecrction of Bile Pipments in Anaplasmosis. Am. J. Vet. Rex., 23, Commonwealth of Australia. (1966): 3-31. - 25. Todorovic, R. A., (1962): 1011-1018.- 2. Anonymous: A Manual for Conducting the Vizcaino, 0. G. and Adams. L G.: The Detection of Babcsia Complement Fixation Test for Anaplasmosis. United Slates Antibodies by the Complement Fixation Technique. Revista, ICA, Department of Agriculture, Washington, D.C., 1958. - 3. Barry, K. Vol. VI, No. 3, (Sept. 1971): 213-233. - 26. Topaclo, T.: G., McLaurin, A. W. and Pamell, B. L: A Practical Temperature- Immunization Against Anapla.smosis and Pirnplasmosis. Philippine J. Compensated Hand Refractometer (the TS mete): Its Clinical Use Anim. Ind., 3, (1936): 169-179. - 27. Vindas, S. A.: Resi%tcncia a and Application in istimalion ofTotal Serum Proteins. J. Lab. Clin. la Piroplasmosis 'xpcrimcntal de las lritrocitos Jovcnes de Temeros Med., 55, (1960): 803-808. - 4. Bricre, R. 0. and Mull, J. D.: Esplenectomizados Rccientementc Recuprados de Anaplasmosh. Electrophoresis of Serum Proteins With Celluloes Acetate. A Rev. Fac. Mcd. Vet. y Zoot., 2, No. 4, Univcnidad de San Carlos, Method or Quantitation. Am. J. Clin. Path., 42, (191,4): 547-551. - Guatemala, (1969): 86-91. - 28. Williams, E. I. and Jones, F. W.: S. Christensen, J. F.: Bovine labesiosis. In Disease' of Cattle. 2nd Blood Transfusions During Patent Bovine Anaptasmosis. Am. J. VeL ed. Edited by W. J. Gibbons, American Veterinary Publications, Res., 29, (1968): 703-710. - 29. Williams, If. E. and Gonzalez, F. Inc., Santa Dazbaru, Calif., (1963): 665-672. - 6. Dumag, P. U., 0.: Two Tick-Borne Dieases Affecting Exotic Cattle Introduced Reyes, B. V. and Castllo, A. h.: Observation on the Premunitlon of into Trinidad, W. I. Can. VOL J., 10, (1969): 61-70.
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