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AVIAN DISEASES 47:1–20, 2003

Origins of Coccidiosis Research in the Fowl—The FirstFifty Years

H. David Chapman

Department of Poultry Science, University of Arkansas, Fayetteville, AR 72701

Received 18 June 2002

SUMMARY. In 1910, H. B. Fantham described the life cycle of a coccidian parasite inbirds. Fantham was a parasitologist at Cambridge University in the United Kingdom workingfor an enquiry into diseases affecting the red grouse. Despite the growing importance of thepoultry industry and the realization that coccidiosis was an important disease of the fowl,little further work was carried out in the United Kingdom until coccidiosis research wasinitiated at the Veterinary Laboratory, Weybridge almost 30 yr later. Further progress de-pended upon research carried out at academic and agricultural institutions in the UnitedStates. E. E. Tyzzer at Harvard University provided the solid foundation upon which ourpresent knowledge of coccidiosis, and the species of Eimeria involved in the disease, is based.Agricultural experiment stations (AESs) throughout the nation played an important role incommunicating advances to the agricultural community. W. T. Johnson at Western Wash-ington and, subsequently, Oregon AES made significant contributions to our understandingof the disease, as did C. A. Herrick and coworkers at Wisconsin AES, J. P. Delaplane andcoworkers at Rhode Island AES, and P. P. Levine at Cornell University.

Key words: Eimeria, coccidiosis, poultry, history, avian disease, agricultural experimentstation

Abbreviation: AES 5 agricultural experiment station

Coccidiosis research in the fowl originated inthe United States and United Kingdom duringthe first half of the 20th century. This reviewis concerned with the vital role that institutionsin both countries (predominantly in the UnitedStates), and researchers trained in parasitology,pathology, and veterinary science, played in thisresearch. The review covers a period of 50 yr,from 1899, when the earliest textbook con-cerned with poultry diseases, which included asection on coccidiosis, was published (146), to1949, when the first coccidiosis conference wasorganized by the New York Academy of Sci-ences (12).

Much early work was undertaken by agri-cultural experiment stations (AESs) in the Unit-ed States and has not previously been cited inthe scientific literature. Although it is now con-sidered important to publish original researchin peer reviewed journals, in the past fewer spe-

Published with permission of the Director, Arkan-sas Agricultural Experiment Station, University of Ar-kansas, Fayetteville, AR 72701.

cialist journals were available, and it was con-sidered important to communicate to the agri-cultural community by means of bulletins, an-nual reports, circulars, and the proceedings ofprofessional societies. This creates a problemfor those interested in literature of the periodbecause these articles are often difficult to ob-tain and usually are not indexed either by sub-ject or by author.

Coccidiosis has long been known as impor-tant in poultry, and even today, control requiressignificant financial expenditure. It is difficultto imagine the problem farmers must havefaced with a disease that was seemingly presentin every flock and impossible to eradicate. Dur-ing the latter half of the 19th century, the U.S.government came under considerable pressureto solve problems of the agricultural commu-nity. This led to the creation of AESs through-out the nation, with a role to conduct researchinto diseases of livestock and to disseminatefindings rapidly to the public. In contrast to theUnited States, apart from some early work car-ried out at Cambridge University, there was

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very little coccidiosis research in the UnitedKingdom during the period. An editorial in1933 from the Veterinary Record, quoted byPayne, states, ‘‘It is safe to say that many mem-bers of our profession have not yet realized themagnitude of the poultry industry in this coun-try, or the remarkable and steady expansion ithas made in the past decade’’ (134).

Hawkins divides the history of coccidiosis re-search into three phases (74). The first phaseprecedes 1929, before the ‘‘monumental workof Tyzzer,’’ and the second from 1929 to 1936when Herrick and Holmes reported the activityof sulphur against Eimeria tenella. This usheredin the third stage when most research was con-cerned with chemotherapy. Previous historicalreviews are principally concerned with the‘‘blackhead story’’ as it relates to coccidiosis(116) and control of the disease (141). Becker(24,25) and Morgan and Hawkins (130) re-viewed some of the early literature. Annotatedbibliographies by Merck and Co. have beenconsulted for references from the 1930s and area valuable source of information regarding che-motherapy (13,14).

EARLY RESEARCH

The grouse enquiry in the United King-dom. The first detailed investigation of the lifecycle of a coccidian parasite in birds was carriedout by Harold Benjamin Fantham (1876–1937), a distinguished zoologist and parasitol-ogist who during his career studied many dif-ferent microbial organisms including trypano-somes, herpetomonads, amoebae, microspori-dia, and myxosporidia (references in 169).Fantham was at one time an assistant to theQuick Professor of Biology at Cambridge Uni-versity and was employed as a protozoologist tothe Grouse Disease Enquiry that was estab-lished in the United Kingdom to investigateheavy mortality occurring in grouse chicksreared on Scottish moors. He believed only onespecies of coccidia occurs in birds and gave thisthe name Eimeria avium after the recommen-dation of Doflein (45). By administering oo-cysts from feces of diseased grouse to chickensand pigeons, Fantham thought he could pro-duce coccidiosis in these hosts (55).

Fantham was aware of pioneering studies ofprotozoan parasites carried out in Italy, France,and Germany during the last decades of the

19th century. In Italy, Rivolta and Silvestriniwere the first to recognize a coccidian in thefowl and provide an account of sporulation ofthe oocyst (144). Rivolta described Gregarinaavium intestinalis (143), a parasite that Tyzzerwas subsequently able to identify as the causeof acute cecal coccidiosis in chickens (159).The French workers Raillet and Lucet measuredoocysts from ceca of chickens and described anew species, Coccidium tenellum, a name laterchanged by Railliet to E. tenella (139,140). InGermany, details of the life cycle were graduallyelucidated. Pfeiffer had proposed a cycle in-volving alternation of parasite generations witha multiplicative phase in cells of the gut epi-thelium and a reproductive phase leading toformation of oocysts (135). Subsequently,Schaudinn described the complete life cycle ofEimeria schubergi from the centipede (147).Fantham notes that in this ‘‘celebrated memoir’’three essential phases of the life cycle, involvingmultiplication, reproduction, and spore forma-tion, are reported with a ‘‘wealth of morpho-logical and cytological detail.’’

Fantham described, in intricate detail, theentire life cycle of an eimerian parasite from anavian host (55). He recorded sporozoite liber-ation from sporocysts (with the aid of pancre-atic juices), cell penetration by sporozoites, for-mation of nuclei within schizonts, merozoiteformation, several generations of schizogony,formation of macrogametes with wall formingbodies, and microgametes with flagella, fertil-ization, oocyst wall formation, and sporogony.The life cycle of E. avium as drawn by Fanthamis reproduced in Fig. 1.

Information was also obtained on the path-ologic effects of infection upon the host. Le-sions caused by the parasite were thought toadmit bacteria to the circulation, thus providinga possible explanation for various theories fromAmerican sources of causes of ‘‘white diarrhea’’in chickens. Oocysts had been reported in eggs(137), but Fantham was unable to observe oo-cysts in ‘‘genitalia of adult grouse’’ and thoughtthat their presence could be explained by con-tamination of eggs as they pass through the clo-aca.

The development of E. avium was restrictedto the intestinal tract; ‘‘examination of kidneys,spleen, liver, and gall bladder of infected grousehas yielded negative results’’ (56). Unfortunate-ly, in later articles Fantham did not restrict

3Origins of coccidiosis research

Fig. 1. The life cycle of E. avium as drawn by H.B. Fantham (55). Reproduced with permission of theZoological Society of London.

comments to his own findings but repeated re-current themes that E. avium occurs in manyavian hosts and is responsible for blackhead dis-ease in turkeys (57,58).

The Bureau of Animal Industry. Whereasin the United Kingdom coccidiosis researchoriginated in an academic setting, and wassponsored by sporting interests, in the UnitedStates research involved those in animal agri-culture. In 1884, Congress established a Bureauof Animal Industry with a remit to investigatethe condition of domestic animals, causes ofdisease among them, and means for preventionand cure and to collect information that couldbe valuable to agricultural and commercial in-terests of the country.

A veterinarian, D. E. Salmon, was appointedchief of the Bureau and served in this capacityfor the first 20 yr. Although Salmon was prin-cipally concerned with devastating plagues af-fecting cattle (Texas fever and pleuropneumo-nia), he also wrote the earliest textbook con-cerned with poultry diseases, which included asection on coccidiosis (146). He mentioned two

species, C. tenellum, a parasite of ceca causingwhitish patches, denuded surfaces, and ulcers(resulting in inflammation, diarrhea, whitishexcrement, loss of appetite, weakness, anddeath), and Eimeria dubia (perhaps appropri-ately named), thought to cause lesions resem-bling those of tuberculosis. Eimeria dubia alsodeveloped in the intestine but could spread tothe liver and lungs. Despite lack of basic knowl-edge, Salmon gave advice on prevention andtreatment. Sanitation was emphasized (disinfec-tion of feeding troughs and drinkers, changingground followed by ploughing, and restockingwith incubator reared chicks from healthyflocks). Treatments recommended included hy-posulfite of soda, quinine, subnitrate of bis-muth, and a mixture of fennel, anis, coriander,gentian, ginger, and aloes in the feed.

Salmon recruited a graduate of Cornell Uni-versity, pathologist Theobald Smith, and sethim to work on the problem of Texas fever. In1893, Smith and his colleague Kilborne pro-duced the classic monograph on the causativeagent, Babesia bigemina, and the mode of trans-mission via the cattle tick (153). Research atthe Bureau was primarily concerned with cattleand swine, but in 1893, Smith received organsof an adult turkey from Rhode Island AES andfound that the ceca and liver were ‘‘extensivelydestroyed’’ by a ‘‘peculiar’’ disease. The nextyear, Smith spent 3 wk at the station and ex-amined livers and ceca of 50 turkeys, of which18 were affected by a protozoan parasite thathe named Amoeba meleagridis. This research ledto a detailed description of infectious entero-hepatitis or blackhead (151). Parasites in thececa of two turkeys were identical with C. te-nellum, but Smith thought it improbable theywere related to the true parasites causing thedisease.

In a bureau circular, G. B. Morse reportedthat C. tenellum occurs in various domestic andwild birds, but commented, with some fore-sight, that use of the name C. tenellum was ten-tative and without prejudice to any other ‘‘va-riety’’ that might be recognized (131). Confu-sion over the cause of various pathologic con-ditions in poultry was evident because theparasite, in addition to causing ‘‘white diar-rhea,’’ was found in cases of ‘‘limberneck,’’ ‘‘legweakness,’’ and ‘‘going light.’’ In 1910, the Bu-reau acquired a farm near Beltsville, MD (laterknown as Beltsville Research Center), and lim-

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ited poultry work began in 1914. Early workwas greatly handicapped by the reappearance ofcoccidiosis. ‘‘This has rendered it impossible torear satisfactory young stock, those escapingdeath being stunted and entirely unfit to savefor breeding purposes’’ (128).

AESs. In 1887, Congress passed the HatchAct that created a system of state AESs with aremit to conduct original research on subjectsbearing directly upon the agricultural industry.The stations were placed on campuses of landgrant institutions, thus creating a strong linkbetween agriculture and the research and edu-cation mission of the latter organizations. Oneof the earliest bulletins concerned with parasiticdiseases, from North Carolina AES, refers tothe ‘‘cholera germ—Gregarina avium intestin-alis,’’ a parasite of the bowels, liver, and lungs(127). In a bulletin from Delaware AES, Fred-erick Chester wrote, ‘‘there are no free popularpublications at hand to inform the farmer orthe farmer’s wife how these troubles (diseases offowls) are to be controlled or treated’’ (35). Henoted that the best books on the subject werewritten in German or French and that Salmon’sbook had not generally been circulated.

Chester was aware of Theobald Smith’s workregarding blackhead but thought he could pro-duce typical enterohepatitis by feeding liver tis-sue containing coccidia to fowls, ‘‘thereforethere can be no doubt as to their causative re-lation to the disease’’ (35). Thirteen years afterSmith’s work, Cole and Hadley stated thatblackhead is a form of coccidiosis and thatSmith’s organism is a stage in the coccidian lifecycle (36). This must have been galling forSmith because Cole and Hadley’s work was car-ried out at Rhode Island AES where he hadconducted his earlier studies. In a subsequentbulletin, ‘‘cysts’’ of coccidia were reported frommany birds such as guinea fowl, ducks, pheas-ants, quail, grouse, pigeons, sparrows, and tur-keys (37). Everett Lund (116) noted thatSmith, by then Professor of Comparative Pa-thology at Harvard University, wrote a scathingdenunciation of Cole and Hadley for confusingthe two diseases (152). Undeterred, Hadleycontinued his investigations and some years lat-er identified two types of parasite in cases ofblackhead, E. avium and an unidentified fla-gellate protozoan (70). During the 1920s, cir-culars continued to report that the liver is oc-casionally involved in cases of coccidiosis

(32,67). Final resolution of the blackhead con-troversy awaited work of another professor fromHarvard, E. E. Tyzzer.

Although G. B. Morse believed that ‘‘whitediarrhea’’ was caused by C. tenellum, L. F. Rett-ger at Yale University, in collaboration with F.H. Stoneburn at the Storrs AES, Connecticut,demonstrated that a bacterium, designated Bac-terium pullorum, was responsible for this con-dition (142). A circular from California AESnoted that the term ‘‘white diarrhea’’ causesconfusion ‘‘since any disorder of very youngchicks is liable to be manifested by a distur-bance of the digestive system and consequentdiarrhea’’ (17). Bacillary white diarrhea causedby B. pullorum was distinguished from enteritiscaused by C. tenellum, although lesions due tothe latter were thought to occasionally occur inthe liver, lung, and other organs, as well as inthe intestine. B. F. Kaupp, a distinguished pa-thologist from the North Carolina AES, sub-sequently reported three separate causes of di-arrhea in chicks, B. pullorum, C. tenellum, anda flagellate named Trichomonas pullorum(100,101).

Coccidiosis was recognized by most AESs asa common and widespread disease of poultry.Roy L. Mayhew at the Louisiana AES estimatedthat in natural outbreaks losses could exceed50%, with survivors in ‘‘a poor and unthriftycondition for months afterward,’’ and that theloss in profit could amount to 10%–40% dueto slower rate of growth (122). The MichiganAES reported that E. avium was present in atleast 90% of all poultry yards (33), and datafrom Massachusetts AES indicated that coccid-iosis was the most frequent disease diagnosedin flocks reared under intensive management(106). In California, coccidiosis was so wide-spread that ‘‘practically all established poultryfarms are infected’’ (19). In Nebraska, however,coccidiosis was ‘‘only rarely encountered in ma-terial examined but may have been overlooked’’(53). The disease was considered not commonenough to deserve a great deal of attention. AtNew Jersey AES, coccidiosis was the most im-portant disease reported in chickens, and atNew Hampshire AES, coccidiosis was the sec-ond most frequently diagnosed condition andwas considered the most important disease con-fronting poultry raisers (22,64). An extensivesurvey of the incidence of poultry diseases wasundertaken at New Jersey from July 1923 to

5Origins of coccidiosis research

June 1930 (23). A total of 9952 specimensfrom 3719 farms were examined and coccidi-osis was diagnosed in 14%, a number exceededonly by cases of pullorum. Mortality did notgive an accurate picture of disease frequency be-cause some conditions were so common thatspecimens were not sent in for diagnosis.

A concern of poultry growers was a condi-tion known as fowl or range paralysis, and acircular from the California Extension Serviceshowed a picture of a recumbent bird, with legssplayed out horizontally, with a legend ‘‘fourmonth old pullet with chronic coccidiosis’’(21). Eighty percent of birds with paralysis atFlorida AES showed ‘‘inflammation of the du-odenum and the duodenal type of coccidia inthe intestinal tract’’ (149). At Michigan, H. J.Stafseth thought that ‘‘so-called cases of rangeparalysis are nothing more or less than duode-nal coccidiosis’’ and that other symptoms seenincluded inflammation of the iris, blindness, in-coordination of movement, drooping wings,and emaciation (154). Rickets was also consid-ered a secondary manifestation of coccidiosisand a consequence of interference with diges-tion of nutrients (155). A circular from the Wy-oming Extension Service reported that chroniccoccidiosis was the most common cause of fowlparalysis (105), and a survey conducted byStorrs AES (Connecticut), revealed that eightof 49 stations (California, Colorado, Illinois,Massachusetts, Michigan, New Hampshire,South Dakota, and Texas) believed that coccid-iosis was associated with or the cause of fowlparalysis (133). Histologic observations of birdswith paralysis, however, failed to reveal a cor-relation with coccidiosis (133), and W. T. John-son noted that fowl experimentally infectedwith coccidia showed no paralysis even whenkept for several months (92).

Researchers continued to look for chemicalremedies. A report from the Pennsylvania StateSanitary Board optimistically concluded thatcalomel and methylene blue might have valuein controlling coccidiosis (129). An arsenicalcompound, neoarsphenamine, had been suc-cessful in treating protozoan diseases in hu-mans, but at Missouri AES, this drug wasfound to be ineffective against coccidiosis (51).Ward and Gallagher (166) considered that cat-echu (recommended by Fantham) was more ef-fective than other preparations, but Beach andCorl tested various chemicals, including cate-

chu, and found none effective (18). A circularfrom Utah AES advised that administration ofdrugs is of questionable value, ‘‘poultrymenshould beware of various patented powders andliquids sold on the market as cures for coccid-iosis’’ (117). Colorful language was often em-ployed to promote these remedies. For example,coccidiosis was considered ‘‘a tramp that followsthe spring rains and warm sunshine and leavesa trail of dismantled poultry farms due to deadchicks’’ (52).

Walter T. Johnson (1892–1937). W. T.Johnson was a graduate of Washington StateCollege and worked for 6 yr at Western Wash-ington AES. In 1925, he moved to Oregon totake up a position as poultry pathologist andspent the next 13 yr at the State College AES,attaining the rank of Professor of VeterinaryMedicine. During this period, he made manyimportant contributions to our understandingof coccidiosis. He demonstrated that coccidiafrom sparrows are morphologically differentfrom those of chickens and not infective forpoultry. He was unable to infect turkeys withcoccidia from chickens, thus indicating the hostspecificity of Eimeria (88). He examined tur-keys showing typical lesions of blackhead andfound no coccidial parasites in the ceca, but hedid find many motile flagellates and concludedthat it is unlikely the coccidium has a directrelationship to blackhead disease. His findingsconcerning morphologic variability were signif-icant. ‘‘Distinctly noticeable variations are seenas to size, shape, and structure of similar stagesof apparently the same species of coccidium.The differences are often so marked as to sug-gest very strongly the probability of more thanone species of coccidia being found in thechicken’’ (89). Initially, he was uncertain ifthere was more than one species, ‘‘. . . presentinformation indicates that the same coccidiummay be so variable that one can be readily mis-led to the belief that more than one species isbeing observed even when this is not true. . . .only one species—E. avium—is here recog-nized’’ (89). The publications committee of theAmerican Association of Instructors and Inves-tigators in Poultry Husbandry requested thatJohnson prepare a series of photomicrographsfor readers of Poultry Science to ‘‘provide a clearpicture of what happens when a chicken be-comes infected with coccidiosis.’’ Some of themicrographs are reproduced in Fig. 2, and, on

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Fig. 2. Illustration of oocysts of Eimeria (8753 magnification) by W. T. Johnson (89). Oocysts wereobtained from smears of intestinal scrapings from the duodenum (fig. 1), and cecum (figs. 2, 3, 6, 7). Originof the oocyst depicted in fig. 4 was not given. Reproduced with permission of Poultry Science.

the basis of the size of the oocysts it seems thatat least three species were illustrated (89). TheseEimeria species were subsequently identified byTyzzer (159) as E. acervulina (89: Fig. 1), E.

tenella (89: Figs. 2, 6, 7), and E. maxima (89:Fig. 4).

In an AES bulletin published in December1928, Johnson stated that four kinds of coccid-

7Origins of coccidiosis research

ia were present in Oregon and illustrated thiswith photomicrographs of small and large oo-cysts from the small intestine and midsized oo-cysts from ceca (92). In March that year, John-son had corresponded with Tyzzer, who toldhim he had isolated four similar species of Ei-meria. Two years earlier, at the December(1926) meeting of the American Society of Par-asitologists, Tyzzer had reported that E. tenellawas different from species that develop in thesmall intestine (158). Tyzzer had also confirmedJohnson’s suggestion that a species of Eimeriafrom turkeys was different from E. avium andnamed this Eimeria meleagridis. In the biennialreport of the Oregon AES for 1928–30, John-son recognized six species of Eimeria in thechicken and provided a brief description of twonew species, Eimeria praecox and Eimeria neca-trix (8). The description included average di-mensions of 50 E. praecox oocysts (20.6 3 23.8mm), but the size of E. necatrix oocysts was notgiven. Nine schizonts of E. necatrix were mea-sured, ‘‘the largest of any species’’ (average of49.2 3 23.8 mm). Oocysts of E. praecox appearon the fourth day after inoculation, a few hoursearlier than for E. acervulina. Eimeria praecox‘‘attacks the small intestine beginning near thegizzard.’’ Eimeria necatrix also attacks the smallintestine and, in severe infections, producesmarked hemorrhage. It was not possible todemonstrate cross-immunization between E.praecox and species that had been described byTyzzer (E. acervulina, E. maxima, and E. mitis).

Johnson was the first to relate the number ofsporulated oocysts ingested to severity of infec-tion (91). He showed that the life cycle is self-limiting, ‘‘infected fowls rid themselves of coc-cidial forms in a comparatively short time’’(91). He used potassium dichromate to prevent‘‘putrefaction’’ in cultures of sporulating oo-cysts, an idea that suggested itself following in-formation provided by Hadley, formerly fromRhode Island AES (91).

Johnson carried out pioneering studies con-cerned with immunity. He noted that immu-nity could be produced by experimental inoc-ulation, that there are many observations thatolder fowls are less affected by coccidiosis thanyounger birds, but age is not necessarily the de-termining factor (90). He found that chickensgiven oocysts obtained from the small intestinedo not develop resistance to subsequent chal-lenge with oocysts obtained from ceca. He was

interested in producing immunity by controlledinoculation (92,94) and showed it is possible toimmunize chickens by including low doses ofoocysts of five species each day in the feed (93).Chandler was skeptical, ‘‘the possibility of im-munizing a flock of chicks against severe infec-tions by feeding chicks a few oocysts seems tobe remote’’ (33), but Jungherr was of the opin-ion that ‘‘the search should be continued for auniversally applicable method of early immu-nization against all types of coccidia’’ (98).

After Johnson’s death in 1937, Oregon AESclaimed, ‘‘more information on the parasiticdisease coccidiosis has been discovered at theOregon station than at almost any other place.The Oregon station is probably the only insti-tution in the world where six known species ofcoccidia of the chicken are available in pure cul-ture’’ (10). Losses in Oregon due to coccidiosiswere estimated as $250,000 annually for an in-dustry valued at $8,000,000. Mrs. Johnsonwrote an article, ‘‘from rough manuscript notesand tables prepared by her husband over a pe-riod of research that occupied the later years ofhis life’’ (95). M. C. Hall of the Bureau of An-imal Industry was acknowledged for suggestingthe names E. necatrix and E. praecox, the formersignifying murderess because of extreme path-ogenicity, and the latter signifying precocity be-cause of early oocyst development. In additionto detailed information on pathogenicity andlife cycles, photomicrographs were presented il-lustrating three types of oocysts and intestinallesions.

Johnson’s views on control were ahead of histime. ‘‘With the chicken susceptible to at leastsix species of coccidia . . . infection occurringat irregular times . . . it seems inconceivablethat a treatment can be considered an impor-tant means of control unless it is highly effec-tive, practical, and economical to apply for in-definite periods’’ (95). ‘‘. . . actual inoculationof young stock on poultry farms, as a controlmeasure, is becoming more valid as the factsregarding coccidiosis are ascertained. The rec-ommendation to purposely infect by actuallyfeeding oocysts involves a rather complicatedprocedure . . . must first be approached exper-imentally. The multiplicity of coccidial speciescertainly complicates the solution’’ (95).

Edward E. Tyzzer (1875–1965). EleryBecker wrote, in the preface of the first bookdevoted to coccidiosis, ‘‘take away the monu-

8 H. D. Chapman

Fig. 3. Life cycle stages of E. acervulina as drawn by E. E. Tyzzer (159). Key: mi 5 microgametocyte; oo5 oocyst; tr 5 trophozoite. Reproduced with permission of Oxford University Press.

mental researches of Tyzzer and of Perard andhow different would our conception of host–parasite relationships in the coccidia be today’’(24). Tyzzer, Doctor of Medicine at the De-partment of Comparative Pathology in themedical school at Harvard University, like Fan-tham and Smith, had studied many differentparasitic protozoa (references in 169). His earlyachievements include a description of Crypto-sporidium parvum from mice and resolution ofearlier blackhead controversies by naming His-tomonas as the flagellate responsible for this dis-ease.

Tyzzer’s papers in the American Journal ofHygiene are recognized as the most significantcontributions to our knowledge of coccidiosisin poultry (159,163). The work published in1929 (159) ‘‘was undertaken primarily for thepurpose of reconciling apparently contradictoryobservations relative to the pathogenicity of Ei-meria avium for chickens.’’ In addition to pro-viding a detailed description of E. tenella, hedescribed three new Eimeria species from thechicken (E. mitis, E. maxima, and E. acervulina)and new species from the pheasant, quail, andturkey (E. dispersa, E. meleagrimitis, and E. me-leagridis). He presented exquisitely detaileddrawings of life cycle stages of Eimeria in sec-

tions of intestine; examples of the drawings ofE. acervulina, E. mitis, E. maxima, and E. te-nella are reproduced in Figs. 3–6. Tyzzer de-scribed nuclear division in schizogony and gavenew information on host and site specificityand immunity. Concerning site specificity, ‘‘thecharacteristic habitat of each species is not de-termined by the part reached by the infectiveform, but rather by the suitability of the tissuefor the further development of the parasite.’’Because he had developed methods for workingwith single rather than mixed species, he wasable to describe characteristic lesions of species,such as obvious hemorrhage in the ceca causedby E. tenella, superficial grayish spots in the up-per small intestine caused by E. acervulina, anda pinkish tinged exudate in the middle intestinecaused by E. maxima. In combination with oo-cyst dimensions, he prepared the first meaning-ful chart for differential species diagnosis. Henoted that more pronounced pathologic chang-es are associated with stages that penetratedeeply into the mucosa and attain large size.Thus, with E. tenella, ‘‘the most serious damageis wrought by the large schizonts, while with E.maxima nearly all the injury results fromgrowth of the sexually differentiated forms.’’

9Origins of coccidiosis research

Fig. 4. Life cycle stages of E. mitis as drawn by E. E. Tyzzer (159). Key: ma 5 macrogametocyte; me 5merozoite; oo 5 oocyst; sch 5 schizont; tr 5 trophozoite. Reproduced with permission of Oxford UniversityPress.

In the 1932 paper, Tyzzer provided detaileddescriptions of E. necatrix and E. praecox andgenerously credited these species to Johnson,‘‘notwithstanding the brevity of his descrip-tions, it appears reasonably certain that the twospecies which we have independently discov-ered are E. praecox and E. necatrix of Johnson’’(163). Tyzzer addressed many topics such asprotective immunity, sources of infection, anduse of chemicals, ‘‘up to the present time noneof the chemicals advocated serve either to pre-vent coccidial infection in the chicken or erad-icate it after it is established.’’ His views on con-trol were similar to those of Johnson, ‘‘attemptsto rear chickens in the absence of all coccidialinfection are in general ill advised and the grad-ual building up of immunity through repeatedlight infections appears to furnish more prom-ise.’’

At the 35th meeting of the United StatesLivestock Sanitary Association (160) and in anarticle for Science (161), Tyzzer described thecriteria and methods used in his investigations.He pointed out that coccidian infections are

ubiquitous, ‘‘failure to take account of adven-titious infection has led to much confusion ofspecies’’ and that the host response ‘‘has no ba-sis in humoral reactions but in a cellular one.’’Histologic studies establish that ‘‘the organismsare destroyed in the sporozoite stage. Largenumbers of the sporozoites penetrate the cellsin the immune bird but the cells, instead ofenlarging and taking on a development that isfavorable to the growth of the organisms, reactunfavorably. The nucleus shrivels up, the celldies and the organism is thus unable to devel-op.’’ W. L. Chandler had proposed a contraryexplanation for host resistance to reinfection.‘‘While it is quite probable that coccidial infec-tions may result in the production of specificantibodies or in phagocytosis, immunity prob-ably results principally because of slight changesin the physiology of the organ invaded’’ (34).

At the 2nd International Congress for Mi-crobiology held in London, it was evident thatTyzzer was concerned with regulation of infec-tion (162). He recognized self-limiting infec-tions that run a brief course and are not ter-

10 H. D. Chapman

Fig. 5. Life cycle stages of E. maxima as drawn by E. E. Tyzzer (159). Key: ma 5 macrogametocyte; mi5 microgametocyte; oo 5 oocyst. Reproduced with permission of Oxford University Press.

minated by any protective reaction and chronicinfections in which organisms persist in thehost indefinitely. He believed that the differencewas related to the population of asexual formsin successive generations and ‘‘a very delicatebalance in regard to reproduction.’’

In March 1949, the New York Academy ofSciences organized a conference exclusively de-voted to coccidiosis, and Tyzzer, then 74 yr old,was invited to be honorary chairman (12). Al-though not present in person, his introductorycomments indicated a continued interest inchronic infections: ‘‘I became much interested,at one time, in the occurrence in certain indi-viduals of infections in which the course wasindefinitely prolonged. . . . Such observationssuggest that there may occur a condition dia-metrically opposed to immunity for which, atpresent, we only have the rather inadequateterm lowered resistance.’’

RESEARCH AFTER TYZZER

AESs. AESs played an important role intransmitting new information to the poultry in-

dustry. For example, publications from Arizona(136), Connecticut (97), Illinois (66), Missouri(47), Nebraska (54), New Jersey (86), andOregon (43) AESs provided descriptions of thenewly identified species. Old ideas, such as sup-posed lack of host specificity, and links withblackhead, paralysis, and other unrelated con-ditions, were abandoned. Remedies availablewere generally recognized of questionable value,and the Bureau of Animal Industry advised thatmore attention should be given to improvingsanitation and hygiene (31). A circular from theExtension Service of the University of Arkansasreported excellent results in treating coccidiosisby including formalin in the drinking water(27), one of the few publications concernedwith poultry diseases from a state that wouldbecome one of the principal broiler producersin the United States (62,63). Georgia wouldalso become a major broiler producer, but apartfrom a brief mention in a bulletin from theUniversity of Georgia AES (61), and somework on sulphonamides (16), little coccidiosisresearch was carried out during the period re-viewed.

11Origins of coccidiosis research

Fig. 6. Life cycle stages of E. tenella as drawn by E. E. Tyzzer (159). Key: me2 5 generation 2 merozoite;ret sch 5 retained schizont; sch2 5 generation 2 schizont; tr 5 trophozoite. Reproduced with permission ofOxford University Press.

Studies on the pathogenicity of E. tenella werecarried out at Louisiana AES, and in addition toeffects on weight gain and mortality, infectionin hens was shown to result in fewer eggs anddelayed egg production (123,124,125). TheMichigan AES found that coccidiosis causes re-duced egg production (41). Other investigatorswere interested in whether modifications of dietcould affect the severity of coccidiosis. Duringthe 1920s, there had been widespread use ofmilk products because it was thought that fer-mentation of milk produces an acid environ-ment in the digestive tract that is unfavorableto parasite development (20). Tyzzer had beenunable to show any protection against coccidi-osis by including skimmed milk in the diet andconcluded that the chief virtue of milk was itsnutritional quality (159). Mayhew was unableto demonstrate any advantage of using butter-milk (126), and Becker and Waters found thatdried skimmed milk increased severity of infec-tion (26). Despite these observations, milktreatment continued to be advocated for the

control of coccidiosis. A press bulletin fromFlorida indicated that ‘‘beneficial results shouldbe noted almost immediately’’ (50), and in Mis-souri, milk products were ‘‘recommended un-hesitatingly for the control of the disease—untilsome other more successful treatment has beendevised’’ (48). An interesting theory by W. L.Chandler for the purported benefits was thatlactose in milk favored multiplication of Lac-tobacillus acidophilus and Bacillus megatheriumand that these suppressed various organisms re-sponsible for secondary bacterial infections thataccompany coccidiosis (34). At the Bureau ofAnimal Industry, diets high in protein wereshown to be of value (1), but Tyzzer’s coworker,Elizabeth E. Jones, could not confirm this (96).Vitamin A provided some protection against Ei-meria infection (1), and vitamin K was able toreduce severity of hemorrhage caused by E. te-nella (15).

Chester A. Herrick and others carried outextensive studies at the University of WisconsinAES. Specificity of E. tenella was investigated

12 H. D. Chapman

by surgically reconnecting the cecum with othersections of the intestinal tract (76). Changes inblood sugar of infected birds were measured(138,167), and glycogen (later shown to be am-ylopectin) was demonstrated in macrogameto-cytes (49). Respiration of oocysts was measuredwith a Warburg apparatus (150). Researchers atWisconsin also carried out pathologic and im-munologic experiments. Colon bacilli were iso-lated from the liver and spleen of chickens afterinfection with E. tenella, indicating that bacte-rial invasion occurs after damage to the cecum(132). Lactobacilli and enterococci in the cecaof chickens decreased in number during infec-tion with E. tenella but anaerobic organisms re-sembling Clostridium perfringens increased (87).Attempts were made to immunize chickens byadministration of oocysts treated by X-rays(168). Evidence was obtained that susceptibilityof chickens to cecal coccidiosis is inherited(145). After one generation of selection, a dif-ference in resistance of progeny was evident be-tween two lines of chickens. Perhaps the mostsignificant finding from Wisconsin was that sul-phur prevented cecal coccidiosis (77). Thisfinding was later supported by reports fromOregon and Louisiana AESs (44,65).

Considerable attention was given to destruc-tion of oocysts and chemical means of disinfec-tion. Sporulation was retarded if oocysts weresuspended in broth cultures of Escherichia colicontaining fecal material, and the ever-contro-versial W. L. Chandler believed that bacterialdecomposition of organic matter resulted inproducts that were toxic to oocysts (34). Oo-cysts were killed if suspended in solutions ofsome disinfectants (60), but none was effectivein the presence of organic material (130). Aneffective disinfectant must penetrate the oocystwall, and at Michigan AES, colloidal iodine wasshown to possess this characteristic (6). Colloi-dal iodine was sold for decontamination ofhatching eggs prior to placement in incubators(Iodine Suspensoid Merck) because oocysts onthe eggshell were believed to be a source of in-fection for chicks. Experiments at Texas AESshowed that E. tenella infection could be pre-vented by fumigation of soil with methyl bro-mide (28).

An interesting observation from WyomingAES concerned an outbreak of coccidiosis insage grouse on ranches where chickens were notconfined (78). Oocysts from the grouse were

not infective if given to chickens, a result ofinterest in view of Fantham’s earlier observa-tions (55).

P. Philip Levine (1907–79). P. P. Levinemade several important contributions to knowl-edge of coccidiosis. Levine worked in the De-partment of Pathology and Bacteriology, NewYork State Veterinary College, Cornell Univer-sity. He described two new Eimeria species, E.hagani and E. brunetti, on the basis of oocystsize and cross immunity studies (107, 114).The description of E. hagani was brief and in-sufficient to justify consideration as a new spe-cies, but E. brunetti has stood the test of timeand, unlike E. hagani, has been isolated inde-pendently by others. Eimeria brunetti wasnamed after Dr. E. L. Brunett, who had pro-duced several extension bulletins concernedwith coccidiosis (29,30).

Levine was able to infect chickens by inoc-ulating merozoites into the intestine and usedthis method to separate E. tenella from E. ne-catrix (109). He showed that ligation of pan-creatic ducts prevents establishment of thesespecies, indicating the importance of pancreaticsecretions for excystation, and that trypsin isnecessary for liberation of sporozoites (113).Levine found six species (E. acervulina, E. mitis,E. praecox, E. maxima, E. tenella, and E. neca-trix) in poultry flocks near Ithaca, NY, thus in-dicating the ubiquitous nature of coccidian in-fections (110).

Most significant, from a practical point ofview, was the study of sulphanilamide (108).Lund described this as a ‘‘landmark contribu-tion’’ that determined ‘‘the direction of researchefforts for decades to come’’ (116). At a meet-ing of the American Veterinary Medical Asso-ciation in Chicago, Levine explained that sul-phanilamide and sulphur are toxic and cannotbe included permanently in feed (115). He be-lieved that use of drugs should be an adjunctto management, ‘‘medication can never take theplace of proper husbandry.’’ In the panel dis-cussion, his views on chemotherapy were clear:‘‘if domestic animals, including poultry, have tobe medicated continually in order to keep themhealthy or alive, there is something fundamen-tally wrong.’’

Beltsville Research Center. From 1900 to1950, poultry keeping in the United Statesgrew from a small scale in which many farmersmaintained small flocks of less than 100 chick-

13Origins of coccidiosis research

ens to large holdings of several thousands ofbirds in farms where rearing of poultry was thepredominant occupation. Growth of the indus-try necessitated development of organizations,such as the Research Center at Beltsville, withresources and facilities necessary to conduct dis-ease research. Nutritional studies (already men-tioned) were carried out in the 1930s by EnaAllen, and brief reports were provided on thepathogenicity of E. mitis, the value of vinegarfor treatment of E. tenella infection, and a caseof prolonged cecal coccidiosis (2,3,4). Duringthe next decade, research was concerned withchemotherapy, and a series of papers were pro-duced on the action of sulphonamides (see be-low).

Research in the United Kingdom. Verylittle coccidiosis research was conducted in theUnited Kingdom after Fantham’s pioneeringstudies. D. C. Matheson, Professor of Pathol-ogy at the Royal (Dick) Veterinary College, Ed-inburgh, presented a report on coccidiosis atthe 4th World’s Poultry Congress (119). He be-lieved that a reduction in incidence might beachieved by strict attention to sanitation andhygiene and by establishing a register of coccid-iosis-free flocks. Some years later, Mathesonproduced guide notes for the veterinary profes-sion for the diagnosis of coccidiosis (120). At ameeting in Belfast, Northern Ireland, researchdevelopments in the United States provided thebasis for a stimulating discussion of practicalissues relating to coccidiosis control (104). Theeminent helminthologist E. L. Taylor advisedthe Lancashire Utility Poultry Society thatchicks ‘‘be exposed to slight infection to preventserious trouble later’’ (157).

A station ‘‘for practical experiments in thebreeding of poultry for the table’’ at the south-eastern Agricultural College, Wye, in Kent, re-ported that type of ration had a major influenceon mortality due to coccidiosis (9). The com-position of diets, however, was not indicated.The premier institution concerned with poultryhusbandry in the United Kingdom was HarperAdams Agricultural College at Newport, Shrop-shire, and experiments were carried out on thevalue of disinfectants and possible inclusion ofiodine in milk as a remedy for coccidiosis(102). An experiment at the Biological ResearchLaboratory in the Wirral, Lancashire, indicatedthat cecal coccidiosis was more severe in chicksgiven diets with a high fiber content (118). It

was suggested that this was due to bacterial pro-liferation, but no evidence to support this con-tention was provided. In the United States, ithad been suggested that an acid environmentin the digestive tract is unfavorable to parasitedevelopment and that administration of acidsmight be beneficial (20). Research at the min-istry of agriculture for Northern Ireland, how-ever, indicated that treatment with hydrochloricacid had no effect upon intestinal or cecal pH(103).

In a letter to the editor of the Veterinary Re-cord, G. Mayall raised the issue of host speci-ficity and referred to experiments in which coc-cidia from rabbits were transmitted to chicks(121). The chicks showed no illness and passedonly a few oocysts, but if these were recovered,sporulated, and fed to new chicks, the newchicks apparently fell ill with typical coccidiosis.J. S. Steward, veterinarian at Imperial ChemicalIndustries laboratory in Cheshire, investigatedhost specificity of the turkey species E. melea-gridis. Tyzzer (159) had been unable to infectchickens, quail, or pheasants with this species,but Steward inoculated chickens with largenumbers of E. meleagridis and obtained limiteddevelopment in the foreign host (156).

Discussions concerning need for a poultry re-search institute in the United Kingdom hadbeen ongoing since 1908, and in 1917, theBoard of Agriculture and Fisheries established aveterinary laboratory at Weybridge, Surrey, toconduct research into poultry diseases (39,40).A poultry section was created in 1920, but coc-cidiosis work did not commence until the1940s (134). Research was concerned withmethods for disinfecting poultry houses. Tyzzerhad dismissed use of the fire-gun, but the blow-lamp was tested and found impractical as ameans to destroy oocysts (83). Gaseous am-monia was an effective fumigant, but it wasnecessary to cover buildings to prevent leakageof gas (85). In 1948, the Veterinary EducationalTrust (a private body later known as the AnimalHealth Trust) established a research station forstudy of poultry diseases at Houghton, Hun-tingdonshire. Horton-Smith transferred toHoughton and, as at Beltsville and Weybridge,a research program principally concerned withsulphonamides was initiated (81).

ADVENT OF CHEMOTHERAPY

The report that sulphur could prevent cecalcoccidiosis was the first indication that control

14 H. D. Chapman

might be achieved by medication (77). The useof sulphur was encouraged during the 1940s asa contribution to the national war effort, en-abling the poultryman to produce more andbetter poultry (7). Sulphur was effective againstE. tenella and E. necatrix but ineffective againstother species (111). Furthermore, sulphur hadserious side effects including rickets, dermatitis,and poor feathering. Sulphanilamide was firstsynthesized in 1908, but its therapeutic valueagainst bacterial infections was not demonstrat-ed until 1935 (46). The contributions of PhilipLevine have already been noted. Sulphanil-amide was effective against intestinal speciesthat develop ‘‘superficially’’ in epithelial cells ofvilli but ineffective against E. tenella and E. ne-catrix that develop more deeply in the ‘‘glan-dular epithelium’’ (108). Levine also investigat-ed sulphaguanidine, a less toxic drug than sul-phanilamide, which at high concentrations iseffective against E. tenella and E. necatrix in ad-dition to intestinal species of Eimeria (112).Sulphaguanidine was used quite extensively forprevention but was ineffective for treatment ofestablished infections. Many laboratories inves-tigated the new drugs and some of these studiesare mentioned here. Researchers at Weybridgeand Beltsville confirmed Levine’s findings(5,59,79). Studies at Weybridge showed thatsulphamezathine and sulphadiazine could beused to treat established infections, but thesedrugs were toxic and could not be given formore than 3–5 days (84). Reports from Mich-igan AES confirmed the efficacy of sulphamez-athine but concluded the drug was too toxic forcontinuous use in poultry (73,75). The effectsof sulphonamides could be neutralized by para-aminobenzoic acid, thus providing a clue to themode of action of these drugs (82,164). Studiesat Rhode Island AES showed that sulphaqui-noxaline was effective against E. tenella and didnot interfere with immunity development (42).Sulphaquinoxaline was lethal to sporozoites andschizonts, but development of these stages wasnot completely inhibited (38), thus explainingthe lack of interference with immunity. Sulpha-quinoxaline was also effective against E. necatrixwhen given in an interrupted schedule of med-ication (68). The latter study was funded by agrant from Merck and Co., a forerunner of therole pharmaceutical companies would play infunding research in the academic sector.

Sulphonamide treatment was often followedby recurring outbreaks of coccidiosis and, there-fore, an intermittent schedule of medication in-volving treatment every fifth day, beginningwith the appearance of clinical signs, was widelyadopted. Intermittent treatment combined withintentional exposure to infection by placingbirds on known infected ground was proposedas a method of immunizing birds against coc-cidiosis (148). At the meeting of the 8thWorld’s Poultry Congress in Copenhagen, Hor-ton-Smith expressed the opinion that the aimof chemotherapy should be to permit the ac-quisition of immunity (80). He thought thatintentional exposure to infection had great pos-sibilities providing ‘‘we do not promote sul-phonamide fast strains.’’ Interestingly, at thismeeting, a speaker from Belgium stated that‘‘the mixing of small quantities of sulphon-amide with the meal had produced strains ofcoccidiosis resistant to sulphonamides,’’ but nodata were presented (11).

A major advance was the demonstration byJ. P. Delaplane and colleagues that sulphaqui-noxaline could be administered at low concen-trations continuously in the feed, thus dem-onstrating the feasibility of prophylaxis (42,69).Field trials at Storrs AES indicated that contin-uous medication with sulphaquinoxaline inmash rations ‘‘provides an effective, efficient,and economical control for cecal and intestinalcoccidiosis’’ (99). Medication on a continuousbasis gave better control than strict sanitation(71). At the annual meeting of the AmericanVeterinary Medical Association in July 1949,Philip Hawkins said, ‘‘In sulfaquinoxaline, wenow have the most satisfactory sulfonamide forthe prevention of coccidiosis in poultry.Whether we like the idea of medicated feed ornot, we have no choice in the matter; it is hereto stay. Although we may object to the adul-teration of feedstuffs with medicine, we mustremember that our unnatural methods of live-stock and poultry production have forced us tothis extreme’’ (74).

The 1949 conference organized by the NewYork Academy of Sciences brought togetherleading researchers from government, universi-ties, and industry. In addition to papers con-cerned with chemotherapy, information waspresented on economic losses due to coccidio-sis, regional differences in the incidence of somespecies of Eimeria, and factors involved in eti-

15Origins of coccidiosis research

ology of the disease (reviewed by Reid [141]).Attention was also given to coccidiosis in gamebirds, turkeys, and rabbits. The significance ofchemotherapy is evident because 11 of the 22poultry presentations were concerned withdrugs. New compounds effective against E. te-nella (nitrophenide and nitrofurazone) were dis-cussed (72,165). Several of the contributionswere from pharmaceutical companies, indicat-ing an important role the commercial sectorwould play in drug discovery (a process requir-ing considerable resources and intellectual ef-fort) and control of the disease.

CONCLUSION

The foundation of our knowledge of host–parasite relationships in Eimeria of the fowl wasestablished by pioneering studies undertakenduring the first half of the 20th century. In ret-rospect, it is remarkable how much knowledgeregarding coccidiosis was obtained. During thisperiod, animal facilities at most institutionswere limited, and although the chicken is in-expensive and relatively easy to maintain, theprevalence of Eimeria and the difficulty of rais-ing birds in the absence of infection has proveda major constraint on research. Many AESs andlaboratories that contributed to our early un-derstanding of coccidiosis no longer conduct re-search in this field. During the latter half of the20th century, coccidiosis research was under-taken at those institutions (government, uni-versity, and private) with resources and special-ized facilities necessary for producing andmaintaining coccidia-free birds. Examples inthe public sector include the Parasite ResearchLaboratory at Beltsville in the United States,the Central Veterinary Laboratory at Wey-bridge, and Houghton Poultry Research Stationin the United Kingdom. The ability to raisechickens in the absence of infection has alsobeen important for mass screening of chemicalsfor anticoccidial activity, and many pharmaceu-tical companies have been involved in this pro-cess. Control of coccidiosis has been achievedby the joint efforts of the academic community,government organizations, and private industry.

Success in controlling coccidiosis was builtupon solid foundations established by Johnson,Tyzzer, and others during the first half of the20th century. It is fitting to end this reviewwith Tyzzer’s final words to those attending the

meeting at the New York Academy of Sciences.‘‘When I started my investigations on avian in-fections somewhat over thirty years ago, therewas little reliable information in regard to avianpathology, the literature being pretty wellpacked with misinformation. One can not butbe impressed by the progress that has beenmade during the ensuing years and at presentone expects as critical work in this field as inany other’’ (12).

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ACKNOWLEDGMENTS

I thank L. R. McDougald for providing access tothe Malcolm Reid reprint collection and M. E. Rosefor reviewing the manuscript.

ADDENDUM

In addition to research at Wisconsin AES (145),studies at Hawaii AES, initiated in 1845, indicatedthat susceptibility to cecal coccidiosis in chickens isinherited. (Palafox, A., J. E. Alicara, and L. Kartman.Breeding chickens for resistance to cecal coccidiosis.World’s Poult. Sci. J. 5:84–87. 1949.)