Avian Pathology

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Biliverdin production in chickens infected with the

malarial parasite Plasmodium Gallinaceum

R.B. Williams

To cite this article: R.B. Williams (1985) Biliverdin production in chickens infected with
the malarial parasite Plasmodium�Gallinaceum , Avian Pathology, 14:3, 409-419, DOI:
10.1080/03079458508436242

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Avian Pathology, 14: 409-419, 1985

BILIVERDIN PRODUCTION IN CHICKENS

INFECTED WITH THE MALARIAL PARASITE
PLASMODIUM GALLINACEUM

R.B. WILLIAMS

Veterinary Research Department, Wellcome Research Laboratories1,

Berkhamsted, Herts. HP4 2QE, England
SUMMARY
Chickens infected with the malarial parasite Plasmodium gallinceum
produced green droppings: the predominant pigment was biliverdin.
Droppings of identical appearance were produced by chicks injected
with phenylhydrazine, a haemolytic agent: it is concluded that the
catabolism of haemoglobin resulting at least in part from malarial
haemolysis produces excess bile pigments which appear in the drop-
pings. Other chicken diseases in which green droppings are "a charac-
teristic objective symptom are fowl typhoid, Newcastle disease (Doyle's
form), spirochaetosis and fowl cholera. The correlation of this symp-
tom with haemolytic or other secondary anaemia is discussed and its
value in field outbreaks of avian malaria as an indicator of the need
for immediate therapy is emphasised.

INTRODUCTION
During a series of experiments on Plasmodium gallinaceum Brumpt, 1935 (Apicom-
plexa : Haemosporina) it was consistently observed that the droppings of infected
chickens became coloured with a bright green pigment, any survivors continuing
to pass green droppings throughout the patent period of the disease. The potential
value of this characteristic sign of infection in the field as an indication of the
need for prompt initiation of therapeutic medication of a poultry flock was immed-
iately recognised. Investigations were therefore carried out on the identity of the
pigment (which proved to be biliverdin), its source and the reason for its produc-
tion with reference to the malarial syndrome.

MATERIALS AND METHODS

The chickens used in all experiments were Ross Brown cockerels, 14 to 27 days
of age, which were housed in wire-floored cages at 24°C with 23 hours lighting.
They had free access to unmedicated drinking water and an unmedicated experi-
mental chick diet (LD5) deficient in vitamin K.

Received 11 January 1985

Accepted 2 May 1985
1
Now Coopers Animal Health.
410 R.B. Williams

Malarial infections were produced by injection into the jugular vein of 106 infected
erythrocytes from donor birds infected with the Wellcome line of Plasmodium
gallinaceum (strain 8A). Standard methods were used for routine assessments
of haematocrits, erythrocyte counts and parasitaemias (Giemsa-stained blood
smears). Haemolysis in chickens was induced by daily injections into the pectoral
muscle of 10 mg phenylhydrazine hydrochloride (equivalent to 7.5 mg phenyl-
hydrazine base) in 0.25 ml sterile distilled water.
Extracts were made from droppings of normal chickens, chickens injected with
phenylhydrazine or malarious chickens by vigorously shaking samples in a mixture
of chloroform and methanol (2:1 v/v) with a Whirlimixer followed by centri-
fugation. The minimum amount of solvent mixture was used and the supernatant
was chromatographed immediately. Preliminary trials showed that the following
system of thin layer chromatógraphy (TLC) gave the best results. Samples (5 to
15 /d) were spotted on to TLC aluminium sheets coated with 0.2 mm silica gel
60 F 25 4 (Merck), previously dried at 150°C for 2 hours. These were run at 23°C
in one direction using a solvent mixture of equal parts of methanol and ethyl
acetate. The samples separated into green or yellow spots, and colourless spots
which were visualised by viewing in ultraviolet light or by developing in an iodine
vapour tank. Standards of biliverdin hydrochloride (80% purity) and bilirubin
(Sigma Chemical Co.) were freshly prepared in the same solvents and chromato-
graphed simultaneously with the faecal extracts. All solvents used were of Chroma-
tographie quality (BDH Chemicals Ltd).

RESULTS
Post mortem examination of malarious chickens
Examination of the digestive tract of chickens which had died of P. gallinaceum
infection showed the intestine to be almost empty but the small amounts of con-
tents were tinged with green whether they occurred at the distal or proximal end
of the intestine (Fig. la). Sometimes the mucosal surface of the intestine was
stained various shades of green. Manipulation of the gall bladder and its associated
ducts in these birds forced bile into the jejunum, intensifying the colouration
described above. This finding suggests that bile is the source of the green coloura-
tion of the mucosa and of the intestinal contents.
Temporal relationships of infection, production of green droppings and deaths
of malarious chickens
The results obtained from seven separate experiments involving 122 infected
chickens showed that green droppings appeared almost invariably on either the
5th or 6th day after infection. In the same groups of birds, when deaths occurred,
the first were on the day before green droppings were observed on 2 out of 25
occasions; on the same day that they were observed on 10 occasions; 1 day after
on 12 occasions; and 2 days after just once. In all cases, the parasitaemia had been
rising and the haematocrit had been falling for between 1 and 4 days before green
droppings were produced.
Description of green droppings produced by malarious chickens
At the time of the first appearance of the green pigment, the droppings were
normally formed and the pigment was confined to the faecal part. "At this stage
(designated phase I), the colour was not very intense and was difficult to see but
it could be demonstrated by shaking droppings in a mixture of methanol and
 Biliveidin and avian malaria 411

Fig. la. Contents of opened jejunum of Fig. lb. Diarrhoea produced by chicken
chicken infected with P. gallinaceum. during phase II of infection with P. gallina-
ceum.

Fig. 1c. Extracts of chicken droppings: from Fig. Id. Normal chicken droppings,
left to right; control, injected with phenyl-
hydrazine, infected with P. gallinaceum.

Fig. le. Droppings from chickens in phase III Fig. If. Droppings from chickens injected
of infection with P. gallinaceum. with phenylhydrazine.
 Biliverdin and avian malaria '. 4 1 3

chloroform (2:1 v/v) when it appeared in the supernatant. This stage of phase I
lasted only a few hours, then followed an even shorter period when the colour
intensity increased and the uric acid portion of the dropping was also seen to be
coloured by the pigment, apparently by diffusion from the faecal part. During
phase II, a thin, mucoid, brilliant green diarrhoea was produced, whilst the birds
were anorexic. Sometimes the urine was passed separately as a sulphur-yellow
fluid at this time. The second phase lasted about 2 days and was the critical period
during which, if it were going to succumb, a bird usually died. More rarely, death
occurred slightly before (see above), or 1 or 2 days after this. Phase III, which of
course occurred only in survivors, was one in which the droppings were again
normally formed but with a green colour intermediate in intensity between those
seen in the first and second phases. The pigment disappeared from the droppings
when the parasitaemia became negative and the haematocrit simultaneously return-
ed to normal, or within a day or so either way.
Physical and chemical properties of the pigment(s) in the droppings
The typical colour of the pigment at its maximum intensity (phase II) during the
production of diarrhoea is shown in Fig. lb. The pigment as shown was stable
for at least 2 weeks when left to dry in air at about 23° C. It was insoluble in
hexane but could be extracted with ethyl acetate, methanol, ethanol, glacial acetic
acid or chloroform. The colours of extracts of droppings from uninfected control
birds and droppings from malarious birds in phase III of the disease are shown in
Fig. lc and the fresh droppings are shown in Figs Id and le respectively.
Chromatographie analysis (four runs) of the extracts shown in Fig. lc produced
a variety of spots, some yellow or green, and other colourless spots requiring
visualisation by ultraviolet light or by treatment with iodine vapour. No ninhy-
drin positive spots were separated. Only the details of coloured spots are given
here (see Text-fig. 1), although all extracts separated into colourless spots in addi-
tion. The control extracts exhibited only a yellow spot with a mean Rf of 0.855
(range 0.85 to 0.86). This coincided with a yellow spot in the extracts from malar-
ious birds with an Rf of 0.848 (0.83 to 0.86); the same extracts also exhibited a
green spot of Rf 0.330 (all four replicates identical) which did not appear in control
extracts. The control sample of 80% biliverdin hydrochloride gave two green
spots of Rf 0315 (0.30 to 0.33) and 0.655 (0.64 to 0.67) and a yellow one of
Rf 0.730 (0.72 to 0.74). The control sample of pure bilirubin gave only a yellow
spot with an Rf of 0.735 (0.73 to 0.74). Hence, the yellow spot produced by both
the control extracts and those of malarious birds did not coincide with bilirubin,
but bilirubin appeared as a contaminant of the control biliverdin sample. There
appeared also to be two isomers of biliverdin in the control sample, the slower
moving one coinciding with the green spot separated from the extracts from malar-
ious birds.
Application of a drop of concentrated nitric acid to each of the green spots pro-
duced by chromatography of samples from malarious birds and the control sample
of biliverdin hydrochloride immediately gave an intense purple colour, i.e. a posi-
tive Gmelin reaction diagnostic of bile pigments (see Pearse, 1972). A few drops
of nitric acid added to 1 ml of the methanol/chloroform extracts of droppings
from malarious birds gave the same colour but there was no reaction from extracts
of control droppings. The action of concentrated nitric acid on the yellow spots
produced by the pure bilirubin sample and the impure biliverdin sample was to give
414 R.B. Williams

a green colouration first, then a purple colour; the same effect was shown with the
stock samples in methanol/chloroform. This effect was not produced on the yellow
spots separated from any of the extracts of droppings.
The sulphur-yellow urine passed during phase II of the disease (see above) gave a
negative Gmelin reaction.

Text-fig. 1. Diagrammatic representation of chromatogram of extracts of chicken

droppings and control bile pigment samples, showing only yellow (y)
and green (g) spots. Colourless spots requiring subsequent visualisation
are omitted.
c = control extract; ph = phenylhydrazine extract; Pg = Plasmodium
gallinaceum extract; bv = biiiverdin sample; br = bilirubin sample.
 Biliverdin and avian malaria 415
Induction of haemolysis in uninfected chickens
Two experiments were carried out. In the first, 10 birds were each given a single
injection of phenylhydrazine hydrochloride (calculated dose 26 to 32.5 mg/kg
of phenylhydrazine). Within 24 hours, all birds were producing green droppings
identical to those produced during phase I of a malarial infection. Table 1 shows
the haematocrits and erythrocyte counts of the birds immediately before the
injection and 27 hours after the injection, when the experiment was terminated.
Table 1. Haematocrits and erythrocyte counts of 24-day-old chickens injected
with phenylhydrazine
Chicken Phenylhydrazine Haematocrit Eiythrocyte
no. dose (mg/kg) (3'o) count
(xlO" 6 per mm 3 )
a b a b
Al 26 27 21 2.14 1.48
A2 28 29 22 2.40 1.72
A3 28.5 28 21 2.29 1.70
A4 29 28 21 1.95 1.31
A5 28.5 27 21 2.10 1.63
A6 28.5 28 21 1.86 1.56
A7 32.5 30 21 2.08 1.75
A8 32.5 31 23 1.83 1.61
A9 29 28 21 1.85 1.60
A10 31.5 27 . d 2.12 d
a = immediately before tajection
b = 27 hours after injection
d = chicken dead
In the second experiment, 4 birds each received an injection of 31 to 47 mg/kg
phenylhydrazine, followed 24 hours later by another injection of 15.5 to 22.5
mg/kg. Within 24 hours of the first injection, the droppings resembled those from
birds in phase I of malaria infection and 24 hours after the second injection,
droppings resembled those of phase III (see Fig. If). Green colouration of drop-
pings was seen up to the 3rd day after the first injection, after which the droppings
appeared to be normal. Haematocrits are shown in Table 2.
Table 2. Haematocrits of 27-day-old chickens injected -with phenylhydrazine
Chicken Phenylhydrazine Haematocrit
no. dose (mg/kg) (%)
DayO Day 1 DayO Dayl Day 2 Day 3 Day 4
B5 37.5 18.5 28 g25 g20 g27 32
B6 47 22.5 30 g22 gl7 g28 31
B7 31 . 15.5 28 g20 gl9 g23 28
B8 31 15.5 31 g24 g22 g28 32
g = bird producing green droppings

In both these experiments, the birds were not anorexic and no diarrhoea was
observed. Extracts of the green droppings in methanol and chloroform gave a green
supernatant very similar to those from malarious birds (see Fig. 1 c) which gave a
positive Gmelin reaction. When the extracts were chromatographed, they gave
results identical to those of malarious birds (see Text-fig. 1) and the green spot
416 R.B. Williams

again gave a positive Gmelin reaction. The mean Rf of the green spot was 0.330
(all four replicates) and of the yellow spot was 0.853 (0.83 to 0.86). The yellow
spot gave a negative Gmelin reaction.

DISCUSSION
Although green diarrhoea as a symptom of outbreaks of P. gallinaceum malaria in
chickens in the field has been recorded previously (e.g.,Crawford, 1945; Omar and
Ismail, 1962), its potential use as an early warning of malaria does not seem to have
been recognised, nor has the question of its fundamental cause been addressed.
An important clinical aspect of this current work is the recognition of the potential
value in the field of this characteristic sign of infection with/*, gallinaceum. The
inclusion of malaria in the list of diseases already well known to give rise to green
droppings in chickens (see below) should suggest to the clinician the importance
of examining a Giemsa-stained blood smear as an aid to differential diagnosis in
geographical areas where chicken malaria is endemic. A positive result would
indicate the need for prompt initiation of therapeutic medication of the poultry
flock. Under the experimental conditions described herein, some chicks died more
or less just as green droppings were observed, but in the field, where infections
are transmitted by mosquitoes and would not be synchronous in a poultry flock,
deaths have been noted three or four days after the onset of the green diarrhoea
(Omar and Ismail, 1962). Hence, therapy begun at that time might save a consider-
able proportion of the birds from death. Abnormal droppings serve the same
purpose for the clinician in the cases of coccidioses in chickens caused by Eimeria
tenella or E. necatrix (bloody droppings), and histomoniasis in turkeys (sulphur-
yellow droppings).
The results of dissecting out the intestines of malarious chickens first provided
strongly suggestive evidence that bile is the source of the green faecal colouration.
Furthermore, the results of the chromatography which showed that a green spot
with an Rf of 0330 could be isolated and identified as a bile pigment by a positive
Gmelin reaction showed that the actual pigment was biliverdin. The yellow spot
(Rf 0.83 to 0.86) which occurred in extracts from malarious birds and also control
birds was not a bile pigment. This is perhaps surprising in view of the fact that
Iind et al. (1967) found biliverdin and bilirubin to be present in chicken bile in
the ratio of about 1:1.5. However, M.J. Clarkson (in Clarkson and Richards, 1971,
p. 1095) found the ratio of bilirubin to biliverdin in chicken gallbladder bile to be
about 1:17.9; If this latter ratio, or something like it, pertained in the chickens
used in the present work, it would explain the failure to detect bilirubin by chro-
matography, since the TLC plates were loaded with the lowest concentrations
of faecal extracts possible to avoid 'tailing' of the separated biliverdin spots and
therefore any bilirubin present may well have been below the threshold of visual
detection.
Since bile pigments are present in the normally formed droppings of birds recover-
ing from' malaria or those injected with phenylhydrazine (see below), it is apparent
that their presence is not simply the result of anorexia. The problem of how to
account for the apparent hyperproduction of bile (or maybe it is the increased
proportion of biliverdin in the bile) was approached by relating the occurrence
of the green droppings to changes in the parasitaemia and haematocrit. The facts
that the first appearance of green droppings (phase I) is preceded by a rising para-
 Biliverdin and avian malaria 417

sitaemia and a falling haematocrit and that the droppings return to normal (end of
phase III) when the parasitaemia becomes negative and the haematocrit returns to
normal strongly suggest an association between these blood parameters and bile
pigment production.
P. gallinaceum induces an anaemia by intravascular haemolysis and phagocytosis
(Seed and Manwell, 1977) and also by its effect of increasing the fragility of unpar-
asitised erythrocytes (Seed and Kreier, 1972). Furthermore, the catabolic deriva-
tion of bile pigments from haemoglobin is well established in birds (Clarkson and
Richards, 1971). According to Nichol (1970), chicken macrophages phagocytose
erythrocytes to produce biliverdin IXa. Hence, anaemia arising from malarial
infection is partly haemolytic and partly mediated by the reticulo-endothelial
system, i.e., it is a secondary, not a primary, anaemia. The hypothesis that the
biliverdin which appears in the droppings results mainly from the haemolytic
anaemia caused by malaria was tested by the experimental induction of haemolysis
with phenylhydrazine. The effect of this was the production of green droppings
identical to those produced by malarious birds in phase III, the Chromatographie
and chemical tests on the pigment also giving identical results, thus confirming the
hypothesis. Diarrhoea did not occur following phenylhydrazine treatment pre-
sumably because birds did not stop eating. The diarrhoea per se seen during phase II
of malarial infection probably resulted from anorexia but the great intensification
at this time of the green colour already present because of haemolysis probably
occurred because starvation of chickens reduces the rate of secretion of bile which
becomes more concentrated in the gall bladder (Schmidt and Ivy, 1937).
A literature survey of chicken diseases revealed that fowl typhoid, Newcastle
disease (Doyle's form), spirochaetosis and fowl cholera share the occurrence of
green diarrhoea as a characteristic objective symptom (Buxton and Fraser, 1977;
Albiston and Gorrie, 1942; Gross, 1978; Heddleston and Rhoades, 1978). Part
of the disease syndrome of fowl typhoid is a haemolytic anaemia (Assoku et al.,
1970). The occurrence of anaemia in fowl cholera is less certain but it has been
noted at least once in the past (Anon., 1951), although whether haemolytic or
otherwise was not stated. Hanson (1978) states that Newcastle disease virus can
lyse erythrocytes in vitro. Whether this also happens in vivo is presently open to
question. Gross (1978) and Long (1982) note anaemia as a sign of spirochaetosis,
and Long (1982) states that the faeces are bile-stained. Hence, it is hypothesised
that there is a correlation between secondary anaemia and the occurrence of
green droppings or diarrhoea in poultry diseases caused by bacteria, viruses or
protozoans. It therefore seems likely that chicken malaria due to P. juxtanucleare
might also give rise to green droppings. Recently, Bandopadhyay and Vegad (1984)
have suggested that the occurrence of green diarrhoea in avian spirochaetosis
results from inflammation and haemosiderosis. It is difficult to accept this con-
clusion, bearing in mind that haemosiderin is a yellow or brown, insoluble, intra-
cellular pigment (Pearse, 1972). Bandopadhyay and Vegad (1984) did not consider
the involvement of bile pigments in spirochaetosis.
It is emphasised that the correlation suggested above is specifically that between
secondary anaemia and the appearance of bile pigments in the excreta. The effect
of anorexia on the form of the droppings is a quite separate complicating factor.
Allan et al. (1982) stated that green diarrhoea in Newcastle disease is caused by ano-
rexia but, more specifically, it is suggested here that anorexia causes the diarrhoea
418 R.B. Williams

whilst the green colouration owes its occurrence mainly to secondary anaemia.

A cknowledgem en ts
I thank Mrs J. Brackpool for technical assistance and Mr G. White for helpful
discussions on bacterial and viral poultry diseases.

REFERENCES
Albiston, H.E. and Grrie, C.J.R. (1942). Newcastle disease in Victoria. Australian Veterinary
Journal, 18: 75-79.
Allan, W.H., Alexander, D.J., Biggs, P.M., Gordon, R.F., Jordan, F.T.W. and McFerran, J.B.
(1982). Viral diseases. In: Poultry Diseases, 2nd Edition, pp. 76-159. Edited by Gordon,
R.F. and Jordan, F.T.W., London: Balliére Tindall.
Anon. (1951). Handbook on Poultry Diseases, 3rd Edition, pp. 62-65. National Veterinary
Medical Association of Great Britain and Ireland.
Assoku, R.K., Penhaie, W.J. and Buxton, A. (1970). Haematological changes in acute experi-
mental Salmonella gallinarum infection in chickens. Journal of Comparative Pathology,
80: 473-485.
Bandopadhyay, A.C. and Vegad, J.L. (1984). Enteritis and green diarrhoea in experimental
avian spirochaetosis.Research in Veterinary Science, 37: 381-382.
Brumpt, E. (1935). Paludisme aviaire: Plasmodium gallinaceum n. sp. de la poule domestique.
Compte Rendu Hebdomadaire des Séances de l'Académie des Sciences, Paris, 200:
783-785.
Buxton, A. and Fraser, G. (1977). Animal Microbiology, 1. pp. 111-113, Oxford and London:
Blackwell Scientific Publications.
Clarkson, MJ. and Richards, T.G. (1971). The liver with special reference to bile formation.
In: Physiology and Biochemistry of the Domestic Fowl, 2, pp. 1085-1114. Edited by
Bell, D.J. and Freeman, B.M., London and New York: Academic Press.
Crawford, M. (1945). Plasmodium gallinaceum, a malarial parasite of the domestic fowl. Veteri-
nary Record, 57: 395-396.
Gross, W.B. (1978). Spirochetosis. In: Diseases of Poultry, 7th Edition, pp. 330-334. Edited
by Hofstad, M.S., Calnek, B.W., Helmboldt, C.F., Reid, W.M. and Yoder, H.W., Ames:
Iowa State University Press.
Hanson, R.P. (1978). Newcastle disease.In: Diseases of Poultry, 7th Edition, pp. 513-535.
Edited by Hofstad, M.S., Calnek, B.W., Helmboldt, C.F., Reid, W.M. and Yoder, H.W.,
Ames: Iowa State University Press.
Heddleston, K.L. and Rhoades, K.R. (1978). Avian pasteurellosis. In: Diseases of Poultry,
7th Edition, pp. 181-207. Edited by Hofstad, M.S., Calnek, B.W., Helmboldt, C.F.,
Reid, W.M. and Yoder, H.W., Ames: Iowa State University Press.
Lind, G.W., Gronwall, R.R. and Cornelius, C.E. (1967). Bile pigments in the chicken. Research
in Veterinary Science, 8: 280-282.
Long, P.L. (1982). Parasitic diseases. In: Poultry Diseases, 2nd Edition, pp. 166-197. Edited
by Gordon, R.F. and Jordan, F.T.W., London: Balliére Tindall.
Nichol, A.W. (1970). The degradation of haemoglobin and formation of biliverdin in tissue
cultures of chicken macrophages. Proceedings of the Australian Biochemical Society,
3: 92.
Omar, AM., and Ismail, Y. (1962). Plasmodium gallinaceum infection among chickens in
Malaya. Journal of the Malayan Veterinary Medical Association, 3: 75-80.
Pearse, A.G.E. (1972). Histochemistry: Theoretical and Applied, 2, 3rd Edition, pp. 1050-
1100. Edinburgh and London: Churchill Livingstone.
Schmidt, C.R. and Ivy, A.C. (1937). The general function of the gall bladder. Journal of Cellu-
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311-357. Edited by Kreier, J.P. London: Academic Press Inc. Ltd.
 Biliverdin and avian malaria 419

RESUME
Production de biliverdine chez le poulet infecté par le
parasite de la malaria Plasmodium gallinaceum
Les poulets infectés par le parasite de la malaria Plasmodium gallinaceum ont des
excréments verdâtres dont le pigment prédominant est la biliverdine. Ces fécès
sont d'apparence identique à ceux observés lors de l'injection d'un agent hémoly-
tique, la phenylhydrazine, ce qui permet de conclure que le catabolisme de l'hémo-
globine, résultant au moins partiellement de l'hémolyse due à la malaria produit un
excès de pigments biliaires qui apparaissent dans les fientes. Les autres maladies
du poulet dans lesquelles une coloration verte des fientes constitue un symptôme
caractéristique sont la typhose, la maladie de Newcastle (forme de Doyle), la
spirochétose et le choléra aviaire. La corrélation de ce symptôme avec une anémie
secondaire hémolytique ou autre est discutée et il est insisté sur sa valeur dans
les cas de malaria avaire sur le terrain comme indicateur de mise en oeuvre d'un
traitement immédiat.

ZUSAMMENFASSUNG
Die Biliverdinproduktion bei Hühnern die mit dem
Malariaparasiten Plasmodium gallinaceum infiziert sind
Hühner, die mit dem Malariaparasiten Plasmodium gallinaceum infiziert waren,
produzierten grüne Faeces: das vorherrschende Pigment war Biliverdin. Faeces von
identischem Aussehen wurden von Küken produziert, denen Phenylhydrazin, ein
haemolytischer Stoff, infiziert worden war. Daraus folgt, daß der Haemoglobinkata-
bolismus, der mindestens zum teil die Folge einer Malariahaemolyse ist, zu einer
Überproduktion von Gallepigmenten führt, die in den Faeces erscheinen. Andere
Hühnerkrankheiten bei denen grüne Faeces zu den charakteristischen sachlichen
Symptomen gehören, sind Hühnertyphus, Newcastlekrankheit (Doyle'sform),
Spirochaetose und Hühnercholera. Die Korrelation dieses Symptoms mit haemoly-
tischen oder anderen sekundären Anaemien wird diskutiert und ebenso seine
Bedeutung als Indikator für die Notwendigkeit einer sofortigen Therapic bei aviaren
Malariafeldausbrüchen.

RESUMEN
La produccion de biliverdina en pollos infectados con el
parásito de la malaria Plasmodium Gallinaceum
Se observó en pollos infectados con el parásito de la malaria Plasmodium gallina-
ceum excremento de color verde, encontrándose que el pigmento predominante
era la biliverdina. Heces fecales con idéntica apariencia fueron reproducidas en
pollos inyectados con fenilhidrazina, la cual es un agente hemolítico, por lo que se
concluye que el catabolismo de la hemoglobina resulta al menos parcialmente en el
caso de la hemolisis por malaria en un exceso de pigmentos biliares, los cuales
aparecen el excremento. Otras enfermedades aviares en las que el excremento verde
es un síntoma característico son la tifoidea aviar, la enfermedad de Newcastle (Tipo
Doyle), la espiroquetosis y el cólera aviar.
Se discute la correlación de este síntoma con la anemia hemolítica u otra anemia
secundaria y su importancia con brotes de campo de malaria aviar como indicador
de la necesidad de una terapia inmediata.