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Korean J Parasitol > Volume 49(3):2011 > Article
Hashemnia, Khodakaram-Tafti, Razavi, and Nazifi: Changing Patterns of Acute Phase Proteins and Inflammatory Mediators in Experimental Caprine Coccidiosis

Abstract

This experiment was conducted to assess the changing patterns and relative values of acute phase proteins and inflammatory cytokines in experimental caprine coccidiosis. Eighteen newborn kids were allocated to 3 equal groups. Two groups, A and B, were inoculated with a single dose of 1×103 and1×105 sporulated oocysts of Eimeria arloingi, respectively. The third group, C, received distilled water as the control. Blood samples were collected from the jugular vein of each kid in both groups before inoculation and at days 7, 14, 21, 28, 35, and 42 post-inoculation (PI), and the levels of haptoglobin (Hp), serum amyloid A (SAA), TNF-α, and IFN-γ were measured. For histopathological examinations, 2 kids were selected from each group, euthanized, and necropsied on day 42 PI. Mean Hp concentrations in groups A and B (0.34 and 0.68 g/L) at day 7 PI were 3.2 and 6.3 times higher than the levels before inoculation. The mean SAA concentrations in groups A and B (25.6 and 83.5 µg/ml) at day 7 PI were 4.2 and 13.7 times higher than the levels before inoculation. The magnitude and duration of the Hp and SAA responses correlated well with the inoculation doses and the severity of the clinical signs and diarrhea in kids. These results were consistent with the histopathological features, which showed advanced widespread lesions in group B. In both groups, significant correlations were observed for TNF-α and IFN-γ with SAA and Hp, respectively. In conclusion, Hp and SAA can be useful non-specific diagnostic indicators in caprine coccidiosis.

INTRODUCTION

Acute phase proteins (APPs) are a group of blood proteins that show concentration increases (positive APP) or decreases (negative APP) after inflammation, infection, trauma, some neoplastic growth, or immunological disorders. Early reaction of the host to infection or tissue damage leads to a release of pro-inflammatory cytokines [1]. The main cytokines released by infected cells are primarily inteferons, especially IFN-γ, from mononuclear inflammatory cells, although TNF-α and IL-1β may also be involved. The positive APPs are mainly C-reactive protein (CRP), Hp, and SAA which are released by the hepatocytes after cytokine stimulation [2]. When severe cellular destruction is present, a full acute phase response (APR) can be observed [2,3]. The APR is considered to be a non-specific immune mechanism involving systemic and metabolic changes against insult before specific immunity is achieved [4, 5]. During the acute phase response, the serum concentration of the APPs changes dramatically. The circulating concentrations of the APPs are related to the severity of the disorder and the extent of tissue damage in the affected animals. APP levels are not suitable for establishing a specific diagnosis, but quantification of their concentration can provide objective information about the extent of ongoing lesions in individual animals [6, 7]. Ruminant coccidiosis is a contagious protozoal disease that occurs especially in lambs and kids, with a worldwide distribution [8].
Clinical coccidiosis occurs mainly in 4-6-month old kids and lambs and stress factors, such as inclement weather, weaning, dietary changes, traveling, and regrouping have important roles in caprine coccidiosis [9]. In goats, 16 species have been described, of which Eimeria christenseni, Eimeria arloingi, Eimeria caprina, and Eimeria ninakohlyakimovae are of major concern [10-12]. E. arloingi, a common coccidian species of goats worldwide, causes high mortality in kids and leads to economic loss from both subclinical and clinical infections, including low growth performance, decrease in productivity, and treatment cost [13, 14].
The diagnosis of coccidiosis depends on the clinical findings (diarrhea, dehydration, and progressive emaciation), the presence of large numbers of oocysts in the feces, and appropriate signalment and intestinal lesions at necropsy [8]. Acute phase proteins may provide alternative means of monitoring animal health. An increased focus on the application of APPs for this purpose has been developed [15]. APPs may be useful for providing information about the stage of clinical and subclinical infections and also for prognosis of their severity.
To our knowledge, there is no document describing the changes in serum concentrations of APPs and inflammatory mediators in caprine coccidiosis. The purpose of this study was to evaluate the dependent changes in the serum concentrations of Hp, SAA, TNF-α, and IFN-γ in kids experimentally infected by E. arloingi.

MATERIALS AND METHODS

Experiment, animals, and sampling

A pure strain of E. arloingi was obtained from the Parasitology Department of Shiraz University, Shiraz, Iran. The oocysts were stored at 4℃ in 2.5% potassium dichromate (K2Cr2O7) solution for about 2 weeks before their use in the experiment. Before inoculation, the suspension containing oocysts was freed of the potassium dichromate by series washing and centrifugation at 750 g for 5 min. The sediment was mixed with 100 ml distilled water and the number of oocysts was calculated for each ml of suspension. Eighteen Iranian crossbred kids were separated from their dams immediately after birth, fed with a milk replacer and reared under coccidia-free conditions in closed rooms with restricted access. At 15 days of age, the kids were divided into 2 groups. The kids of groups A (n=6) and B (n=6) were infected orally with 1×103 (low dose) and 1×105 (high dose) sporulated oocysts of E. arloingi per animal, respectively. The third group, C, received distilled water as the control.
Fresh fecal samples, approximately 3-5 g, were obtained directly from the rectum by stimulation of the anus and were examined for the presence of oocysts every day. Fecal consistency was assessed on the basis of a scoring system (1, normal; 2, semi liquid to liquid; 3, watery; 4, hemorrhagic and/or with tissue). Blood samples for determination of serum Hp, SAA, IFN-γ, and TNF-α were collected from the jugular vein of each kid in both groups before inoculation and at days 7, 14, 21, 28, 35, and 42 PI. Simultaneously, blood samples were collected from 6 non-infected kids as controls. The sera were separated following centrifugation for 10 min at 750 g and were stored at -20℃ until analyzed.

Measurements

Haptoglobin (Hp) was measured based on prevention of the peroxidase activity of hemoglobin, which is directly proportional to the amount of Hp. The analytical sensitivity of this test in serum has been determined as 0.0156 mg/ml for Hp by the manufacturer (Tridelta Development Plc, Wicklow, Ireland).
Serum amyloid A (SAA) was measured by a solid phase sandwich-ELISA. The analytical sensitivity of this test in serum has been determined as 0.3 µg/ml for SAA by the manufacturer (Tridelta Development Plc). IFN-γ and TNF-α were measured by a solid phase sandwich-ELISA (AbC 606 and AbC 607, respectively; Votre Fournisseur AbCys S.A., Paris, France).

Histopathological examinations

For histopathological examinations, 2 kids were selected from each group, euthanized, and necropsied at day 42 PI. After systematic postmortem examination, the small and large intestines were opened and inspected carefully. Appropriate samples of the visceral organs including small and large intestines, liver, spleen, pancreas, and mesenteric lymph nodes from 4 affected kids were fixed in 10% neutral buffered formalin. Paraffin-embedded tissues were sectioned at 5 µm thickness, stained with hematoxylin-eosin, and examined with a light microscope.

Statistical analysis

Descriptive statistics, including the mean, standard deviation, median, minimum, and maximum were calculated for all variables. The ANOVA and Tukey tests were used for comparison of different parameters. Data were analyzed by SPSS software, version 16, and P<0.05 was accepted as a statistically significant difference.

RESULTS

All animals in both groups showed the symptoms of clinical coccidiosis. The oocyst shedding was observed after the prepatent period, which varied between 16 to 18 days in groups A and B. All inoculated kids produced comparable numbers of oocysts (Fig. 1). The clinical signs of the infected kids varied with the size of the inoculation dose. The signs in group B were more severe. In group A, diarrhea started from day 20 PI, a kid with semiliquid and the others with liquid diarrhea (score 2). Severe diarrhea with variable amounts of mucus (score 3) occurred in group B from day 18 PI. Other signs included dehydration, anorexia, depression, paleness of eye mucosa, and listlessness.
The median pre-inoculation concentration of Hp was 0.1 g/L, and a significant increase was detected at day 7 PI (Fig. 2A). The highest median concentration (0.47 and 0.7 g/L) was detected at days 14 and 21 PI in groups A and B, respectively. The levels of this protein remained increased until the end of the experiment.
The median SAA concentration prior to inoculation was 6.1 µg/ml, and concentrations of this protein were significantly increased at day 7 PI (Fig. 2B). The maximum median SAA concentration (27.8 and 90.4 µg/ml) was reached at days 35 and 21 after inoculation in groups A and B, respectively. The levels of this protein remained increased until the end of the experiment.
The mean TNF-α concentration before inoculation was 22.7 pg/dl, and a significant increase (about 2.4 times) was observed at day 7 PI (Fig. 2C). The highest median concentrations were 57.6 pg/dl in group A and 58.5 pg/dl in group B. The mean IFN-γ concentration before inoculation was 15.3 pg/dl, and a significant increase (about 3 times) was observed at day 7 PI (Fig. 2D). The highest median concentrations were 46.7 pg/dl and 45.8 pg/dl in groups A and B, respectively.
There were significant correlations between Hp and SAA (r=0.949, P<0. 01), Hp with TNF-α(r=0.742, P<0. 01), Hp with IFN-γ(r=0. 728, P<0. 01), SAA with TNF-α(r=0.635, P<0.01) and SAA with IFN-γ(r=0.627, P<0.01) in both groups. Significant correlation was observed for TNF-α and IFN-γ(r=0.961, P<0.01). As shown in Fig. 2A and 2B, Hp and SAA concentrations were significantly higher in group B compared with group A (P<0.05) in all weeks. However, there were no significant changes in concentrations of TNF-α and IFN-γ between group A and group B. During the experiment, in group C, the concentrations of Hp, SAA, TNF-α, and IFN-γ were within the reference interval.
There were differences between groups A and B with regards to gross and histopathological lesions. The most remarkable macroscopic lesion was white to grey, slightly to well-raised pin-point foci to relatively large nodules mostly on affected mucosa in the middle jejunum to the ileum (Fig. 3). The kids in group A had milder lesions, including a few scattered whitish non-pedunculated nodules in the mucosa of the jejunum and ileum. The kids in group B showed advanced widespread lesions characterized by thickened mucosa due to mucosal hyperplasia and adenomatous-like changes in the mucosa and a cerebriform or gyrate pattern of projections visible from the serosa.
The main histopathological lesion in both groups was proliferative enteritis associated with the presence of the developmental stages of parasite including mature schizonts, microgametocytes, macrogametocytes, and immature oocysts in the epithelial cells of villi and crypts of the jejunum, ileum, cecum, and proximal colon (Fig. 4). Also, mild lymphoid hyperplasia of the Peyer's patches, remarkable congestion, and edema were observed in some cases. Generally, the kids in group B showed more prominent microscopic lesions than those in group A.

DISCUSSION

Caprine coccidiosis is an important disease resulting from complex interactions between parasites and host, with many factors influencing the severity of the disease. Age, stress, genetic susceptibility, physical condition, and the degree of immunity are important in pathogenesis [10, 16, 17]. The development of clinical coccidiosis in goats is considerably dependent on the species involved [18]. Coccidiosis causes high morbidity and mortality in livestock, and diagnosis is limited to clinical findings, the presence of large numbers of oocysts in the feces, and histopathological findings [8].
There are relatively few reports of APP induction by parasite infections, although infections with Plasmodium falciparum, Babesia canis, Leishmania infantum, and Trypanosoma brucei might be accompanied by increased levels of APPs [19-23]. Haptoglobin and SAA are major acute phase proteins in most species studied [24]. In our experiment, we have shown that the APP response is induced in kids following infection with E. arloingi. The exact mechanism whereby E. arloingi causes APR in kids remains unclear. However, the induction of APPs supports the hypothesis that pro-inflammatory cytokines play an important role [25].
The acute phase response is regulated by a complex network of interactions [5,25]. The main pathway leading to APP production involves the initial release of pro-inflammatory cytokines by macrophages and other inflammatory cells at the site of inflammation or infection. The most important inducers of APPs are cytokines of the IL-1, TNF, and IL-6 families. TNF-α, IL-1β, and IFN-γ are essential for induction of other cytokines (IL-6 and IL-8) and agents, such as platelet activating factor, prostaglandins, leukotrienes, and nitric oxide. When these pro-inflammatory cytokines spill into the circulation, they induce the release of APPs by the liver into the circulation. IL-6 is the principal regulator of most APPs and induces the production of Hp, whereas IL-1 and TNF-α induce expression of SAA and α1-acid glycoprotein and Hp, depending on the mammalian species [1,25].
As was demonstrated in this study, serum Hp, SAA, TNF-α, and IFN-γ concentrations were significantly higher on day 7 after inoculation compared with their concentrations before inoculation, and the levels of these proteins remained increased until the end of the experiment. Hp is a major APP in ruminants, in which species it has a slight circulating level in normal animals, but increases over 100 folds on stimulation [26]. The mean Hp concentrations in groups A and B at day 7 PI were 3.2 and 6.3 times higher than the levels before inoculation. In both groups, significant correlations were observed for Hp with SAA, TNF-α, and IFN-γ. Petersen et al. [27] reported that clinical signs of lameness, diarrhea, respiratory disease, and ear necrosis were reflected in a high serum Hp concentration. Many studies have reported the serum Hp as a clinically useful parameter for measuring the occurrence and severity of inflammatory responses in cattle with enteritis, peritonitis, endometritis, mastitis, pneumonia, endocarditis, abscesses, and other natural or experimental infectious conditions [15,28-37].
The mean SAA concentrations in groups A and B at day 7 PI were 4.2 and 13.7 times higher than the levels before inoculation. In both groups, significant correlations were observed for SAA with Hp, TNF-α, and IFN-γ. SAA is a remarkably moderate acute phase protein in cattle increasing around 2-5 times during an acute phase response [38-40]. Because of the difficulty of measuring serum SAA levels, the application of SAA assays to veterinary diagnosis has not been as widespread as that of Hp assays. SAA has been suggested to be more useful in distinguishing acute and chronic inflammations than neutrophil counts and white blood cell counts [41]
In our study, the magnitude and the duration of the Hp and SAA responses correlated well with the inoculation doses and severity of the clinical signs and diarrhea in individual animals. Hp and SAA concentrations were significantly higher in group B compared with group A (P<0.05). These results were consistent with histopathological investigations, which showed advanced widespread lesions in group B. In some papers, no correlation between Hp and disease severity was observed [34,36].
Sickness behavior with decreased appetite or anorexia is mediated by the pro-inflammatory cytokines through induction of prostaglandins [1,42,43]. The elevation in APPs following E. arloingi infection very strongly indicated that pro-inflammatory cytokines were released into the peripheral circulation. Significant increases in TNF-α and IFN-γ concentrations (about 2.4 and 3.0 times, respectively) were observed at day 7 PI in both groups. Significant correlations were observed for TNF-α and IFN-γ with Hp and SAA in both groups. Although serum concentrations of TNF-α and IFN-γ increased after inoculation in both groups, significant correlations were not observed with the inoculation doses and severity of the clinical signs and diarrhea in individual animals. It is important to note that the APP-response-inducing cytokines are small molecules with a very short half-life. Therefore, cytokines are not very useful for most general diagnostic purposes, in contrast to the APPs, which are stable proteins and have relatively long half-lives [38,44]. In addition, assays for the individual pro-inflammatory cytokines, TNF-α, IL-1, and IL-6 are not commercially available for animals.
According to our study, it seems that SAA and Hp are 2 major APPs that significantly increase in caprine coccidiosis. Considering the timing of the response and the correlation between the magnitude of the response and the severity of the infection, it can be established that parasites causing focal lesions can induce acute phase responses, most probably indirectly via parasite-mediated tissue perturbations.
In conclusion, measuring Hp and SAA can be a suitable indicator of inflammatory reactions in caprine coccidiosis. In our experiment, increased concentrations of APPs were observed before the appearance of clinical signs. Therefore, APPs could be used as a non-specific marker for disease as well as for monitoring the response to treatment in coccidiosis. Measuring APPs along with clinical signs and oocysts per gram (OPG) can be useful for providing information about the stages of clinical and subclinical coccidiosis.

REFERENCES

1. van Miert AS. Pro-inflammatory cytokines in a ruminant model: Pathophysiological, pharmacological, and therapeutic aspects. Vet Q 1995;17: 41-50. PMID: 7571278.
crossref pmid
2. Heinrich PC, Castell JV, Andus T. Interleukin-6 and the acute phase response. Biochem J 1990;265: 621-636. PMID: 1689567.

3. Van Reeth K, Nauwynck H, Pensaert M. Bronchoalveolar interferon-alpha, tumor necrosis factor-alpha, interleukin-1, and inflammation during acute influenza in pigs: A possible model for humans? J Infect Dis 1998;177: 1076-1079. PMID: 9534986.
crossref pmid
4. Saini PK, Webert DW. Application of acute phase reactants during antemortem and postmortem meat inspection. J Am Vet Med Assoc 1991;198: 1898-1901. PMID: 1714890.
pmid
5. Suffredini AF, Fantuzzi G, Badolato R, Oppenheim JJ, O'Grady MP. New insights into the biology of the acute phase response. J Clin Immunol 1999;19: 203-214. PMID: 10471974.
crossref pmid
6. Clark GR, Fraser CG. Biological variation of acute phase proteins. Ann Clin Biochem 1993;30: 373-376. PMID: 7691039.
crossref
7. Eckersall PD. Recent advances and future prospects for the use of acute phase proteins as markers of disease in animals. Rev Med Vet (Toulouse) 2000;151: 577-584.

8. Georgi JR, Georgi ME. In Georgi JR ed, Protozoans. Parasitology for Veterinarians. 1990, 5th ed. Philadelphia, USA. Saunders. pp 84-91.

9. Cox FE. Control of coccidiosis: Lessons from other sporozoa. Int J Parasitol 1998;28: 165-179. PMID: 9504343.
crossref pmid
10. Levine ND. Veterinary Protozoology. 1985, Ames, USA. Iowa State University Press.

11. Norton CC. Coccidia of the domestic goat Capra hircus, with notes on Eimeria ovinoidalis and E. bakuensis (syn. E. ovina) from the sheep Ovis aries. Parasitology 1986;92: 279-289. PMID: 3714300.
crossref
12. Razavi SM, Hassanvand A. A survey on prevalence of different Eimeria species in goats in Shiraz suburbs. J Fac Vet Med Univ Tehran 2007;61: 373-376.

13. Radostits OM, Blood DC, Gay CC. Veterinary Medicine. 1994, 6th ed. London, UK. Bailliere Tindall. pp 879-886.

14. Jalila A, Dorny P, Sani R, Salim NB, Vercruysse J. Coccidiosis infections of goats in Selangor, peninsular Malaysia. Vet Parasitol 1998;74: 165-172. PMID: 9561704.

15. Skinner JG, Brown RA, Roberts L. Bovine haptoglobin response in clinically defined field conditions. Vet Rec 1991;128: 147-149. PMID: 1903006.
crossref pmid
16. Daugschies A, Najdrowski M. Eimeriosis in cattle: Current understanding. J Vet Med B Infect Dis Vet Public Health 2005;52: 417-427. PMID: 16364016.
crossref pmid
17. Jolley WR, Bardsley KD. Ruminant coccidiosis. Vet Clin North Am Food Anim Pract 2006;22: 613-621. PMID: 17071356.
crossref pmid
18. Smith MC, Sherman DM. Goat Medicine. 1994, Philadelphia, USA. Lea and Febiger.

19. Graninger W, Thalhammer F, Hollenstein U, Zotter GM, Krems-ner PG. Serum protein concentrations in Plasmodium falciparum malaria. Acta Trop 1992;52: 121-128. PMID: 1283805.
crossref pmid
20. Shapiro SZ, Black SJ. Identification of an acute-phase reactant in murine infections with Trypanosoma brucei. Infect Immun 1992;60: 3921-3924. PMID: 1500201.
pmid pmc
21. Lobetti RG, Möhr AJ, Dippenaar T, Myburgh E. A preliminary study on the serum protein response in canine babesiosis. J S Afr Vet Assoc 2000;71: 38-42. PMID: 10949516.
pmid
22. Eckersall PD, Gow JW, McComb C, Bradley B, Rodgers J, Murray M, Kennedy PG. Cytokines and acute phase response in post-treatment reactive encephalopathy of Trypanosoma brucei brucei infected mice. Parasitol Int 2001;50: 15-26. PMID: 11267928.
crossref pmid
23. Martínez-Subiela S, Tecles F, Eckersall PD, Cerón JJ. Serum concentrations of acute phase proteins in dogs with leishmaniasis. Vet Rec 2002;150: 241-244. PMID: 11916025.
crossref pmid
24. Mackiewicz A, Kushner I, Baumann H eds, Acute Phase Proteins Molecular Biology, Biochemistry and Clinical Applications. 1993, Boca Raton, Florida, USA. CRC Press.

25. Baumann H, Gauldie J. The acute phase response. Immunol Today 1994;15: 74-80. PMID: 7512342.
crossref pmid
26. Murata H, Shimada N, Yoshioka M. Current research on acute phase proteins in veterinary diagnosis: An overview. Vet J 2004;168: 28-40. PMID: 15158206.
crossref pmid
27. Petersen HH, Dideriksen D, Christiansen BM, Nielsen JP. Serum haptoglobin concentration as a marker of clinical signs in finishing pigs. Vet Rec 2002;151: 85-89. PMID: 12164226.
crossref pmid
28. Höfner MC, Fosbery MW, Eckersall PD, Donaldson AI. Haptoglobin response of cattle infected with foot-and-mouth disease virus. Res Vet Sci 1994;57: 125-128. PMID: 7973086.
crossref pmid
29. Horadagoda A, Eckersall PD, Hodgson JC, Gibbs HA, Moon GM. Immediate responses in serum TNF alpha and acute phase protein concentrations to infections with Pasteurella haemolytica A1 in calves. Res Vet Sci 1994;57: 129-132. PMID: 7973087.
crossref pmid
30. Godson DL, Campos M, Attah-Poku SK, Redmond MJ, Cordeiro DM, Sethi MS, Harland RJ, Babiuk LA. Serum haptoglobin as an indicator of the acute phase response in bovine respiratory disease. Vet Immunol Immunopathol 1996;51: 277-292. PMID: 8792565.
crossref pmid
31. Hirvonen J, Pyörälä S, Jousimies-Somer H. Acute phase response in heifers with experimentally induced mastitis. J Dairy Res 1996;63: 351-360. PMID: 8864931.
crossref pmid
32. Wittum TE, Young CR, Stanker LH, Griffin DD, Perino LJ, Littledike ET. Haptoglobin response to clinical respiratory tract disease in feedlot cattle. Am J Vet Res 1996;57: 646-649. PMID: 8723875.
pmid
33. Hirvonen J, Pyörälä S. Acute-phase response in dairy cows with surgically-treated abdominal disorders. Vet J 1998;155: 53-61. PMID: 9455159.
crossref pmid
34. Hirvonen J, Eklund K, Teppo AM, Huszenicza G, Kulcsar M, Saloniemi H, Pyörälä S. Acute phase response in dairy cows with experimentally inducedEscherichia coli mastitis. Acta Vet Scand 1999;40: 35-46. PMID: 10418194.
pmid
35. Deignan T, Alwan A, Kelly J, McNair J, Warren T, O'Farrell C. Serum haptoglobin: An objective indicator of experimentally-induced Salmonella infection in calves. Res Vet Sci 2000;69: 153-158. PMID: 11020367.
crossref pmid
36. Eckersall PD, Young FJ, McComb C, Hogarth CJ, Safi S, Weber A, McDonald T, Nolan AM, Fitzpatrick JL. Acute phase proteins in serum and milk from dairy cows with clinical mastitis. Vet Rec 2001;148: 35-41. PMID: 11202551.
crossref pmid
37. Nazifi S, Ansari-Lari M, Asadi-Fardaqi J, Rezaei M. The use of receiver operating characteristic (ROC) analysis to assess the diagnostic value of serum amyloid A, haptoglobin and fibrinogen in traumatic reticuloperitonitis in cattle. Vet J 2009;182: 315-319. PMID: 18783967.
crossref pmid
38. Gruys E, Obwolo MJ, Toussaint MJM. Diagnostic significance of the major acute phase proteins in veterinary clinical chemistry: A review. Vet Bull 1994;64: 1009-1018.

39. Alsemgeest SP, Kalsbeek HC, Wensing T, Koeman JP, van Ederen AM, Gruys E. Concen trations of serum amyloid-A (SAA) and haptoglobin (HP) as parameters of inflammatory diseases in cattle. Vet Q 1994;16: 21-23. PMID: 8009814.
crossref pmid
40. Werling D, Sutter F, Arnold M, Kun G, Tooten PC, Gruys E, Kreuzer M, Langhans W. Characterisation of the acute phase response of heifers to a prolonged low dose infusion of lipopolysaccharide. Res Vet Sci 1996;61: 252-257. PMID: 8938857.
crossref pmid
41. Horadagoda NU, Knox KM, Gibbs HA, Reid SW, Horadagoda A, Edwards SE, Eckersall PD. Acute phase proteins in cattle: Discrimination between acute and chronic inflammation. Vet Rec 1999;144: 437-441. PMID: 10343375.
crossref pmid
42. Johnson RW. Inhibition of growth by pro-inflammatory cytokines: An integrated view. J Anim Sci 1997;75: 1244-1255. PMID: 9159271.
pmid
43. Johnson RW, von Borell E. Lipopolysaccharide-induced sickness behavior in pigs is inhibited by pretreatment with indomethacin. J Anim Sci 1994;72: 309-314. PMID: 8157515.
pmid
44. Blackburn WD Jr. Validity of acute phase proteins as markers of disease activity. J Rheumatol Suppl 1994;42: 9-13. PMID: 7529838.
pmid
Fig. 1
The daily oocyst outputs of groups A and B over the period of whole experiment
kjp-49-213-g001.jpg
Fig. 2
The kinetics of acute phase proteins and inflammatory mediators following experimental infection of goats (kids) with E. arloingi. (A) Haptoglobin (Hp), (B) Serum amyloid A (SAA), (C) TNF-α, and (D) IFN-γ. Results are shown as mean±SEM. 0=before inoculation (♦, Group A; ▪, Group B; ▴, Group C).
kjp-49-213-g002.jpg
Fig. 3
Jejunum of an infected kid (formalin-fixed). Thickening of the jejunal mucosa and the presence of scattered whitish pinhead size (1-2 mm in diameter) nodules (arrows) are seen.
kjp-49-213-g003.jpg
Fig. 4
Jejunum of an infected kid. The endogenous stages of parasites (mature schizonts, microgametocytes, macrogametocytes, and immature oocysts) are observed in the epithelial cells of affected villi. H-E stained. Bar=50 µm.
kjp-49-213-g004.jpg
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