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Research Note: Isolation of Two Filamentous Bacteria Associated with Enteritis in Turkey Poults
RESEARCH NOTES Research Note: Isolation of Two Filamentous Bacteria Associated with Enteritis in Turkey Poults TERESA Y. MORISMTA, 1 KENNETH M. LAM, 2 and RICHARD H. MCCAPES 1 ' 2 Veterinary Medical Teaching Hospital, and Department of Epidemiology and Preventive Medicine, School of Veterinary Medicine, University of California-Davis, Davis, California 95616 (Received for publication June 13, 1991)
1992 Poultry Science 71:203-207
INTRODUCTION Poult enteritis is a disease that causes concern in the turkey industry. It results in production losses via decreased feed efficiency, slower growth rate, and increased morbidity and mortality rates, and may predispose the poult to other diseases. Recent research has focused on the virological (Saif et ah, 1985; Reynolds et ah, 1987) and the aerobic bacteriological (Schmidt et ah, 1988) etiologies of poult enteritis. M a n y bacteria, i n c l u d i n g filamentous organisms (Fuller and Turvey, 1971; Goodwin et ah, 1989; Angel et ah, 1990), have been seen in the intestinal wall of the chicken in the crop, ileum, and cecum (Fuller and Turvey, 1971). These filamentous organisms have been observed to be attached to the enterocytes and have been associated with diarrhea in turkeys, chickens, and quail (Goodwin et ah, 1989). Angel et ah (1990) associated these long-segmented filamentous organisms with a stunting syndrome in turkeys.
Veterinary Medical Teaching Hospital. Department of Epidemiology and Preventive Medicine.
However, their exact role in the intestinal tract has not been fully elucidated, partly because of the inability to culture and propagate these organisms. The present study reports on the isolation and propagation of two filamentous organisms isolated from the intestinal tracts of poults exhibiting signs of diarrhea. In addition, the inoculation of poults with these two identified bacterial agents and their subsequent effect on rate of gain was studied.
MATERIALS AND METHODS Source of Birds Commercially reared Nicholas White broadbreasted turkey poults were obtained from several flocks of six ranches in the Central Valley of California. All study flocks had poults demonstrating clinical signs of diarrhea. Poults ranged in age from 1 to 35 days and were selected based on the demonstration of clinical signs of diarrhea, i.e., grossly having fecal material adhering to the vent region of affected birds. Agematched poults were selected based on the absence of clinical signs of diarrhea and served as a control group. Enteritis was
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ABSTRACT Two microaerophilic filamentous bacteria have been isolated from the intestines of turkey poults exhibiting signs of enteritis. These two filamentous bacteria, denoted as F-l and F-2, were reinoculated into 4-day-old poults and those poults have shown a reduction in rate of gain when compared with aged-matched controls. Weight reduction was 14% for F-l and 11% for F-2, respectively, at 21 days of age. (Key words: turkeys, poult enteritis, filamentous bacteria, microaerophilic bacteria, weight loss)
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confirmed histologically in those birds with diarrhea. Birds without diarrhea did not have enteritis when examined histologically. There were increased numbers of heterophils and lymphocytes in the lamina propria of the jejunum of birds with diarrhea when compared with the agematched poults that were not showing any clinical signs of enteritis. In all birds examined, no evidence of infectious agents were observed except that filamentous bacteria were seen attached to and embedded in the enterocytes of the villus tips in the jejunum of those birds with enteritis.
Jejuna from these commercially reared poults were cultured on Campylobacter CVA 3 plates. [Campylobacter Agar (CVA) contains proteose peptone (15.0 g), liver digest (2.5 g), yeast extract (2.5 g), sodium chloride (5.0 g), agar (12.0 g), sheep blood (50.0 mL), cefoperazone (20.0 mg), vancomycin (10.0 mg), and amphotericin B (2.0 mg) per liter of deionized, distilled water.] The cultures were incubated at 37 C in the presence of 10% carbon dioxide, 5% oxygen, and 85% nitrogen. The presence of bacterial colonies was evaluated at 24, 48, and 72 h after inoculation. Two colonial types of bacteria were consistently and repeatedly isolated from birds exhibiting diarrhea and confirmed with enteritis histologically. Each of the colonies was picked from the primary isolation plate and restreaked on a fresh Campylobacter CVA plate for further characterization. The colonies were arbitrarily identified as F-l and F-2, respectively. To test for the presence of other bacteria in the intestines, these jejuna were also cultured aerobically (5% sheep blood agar, 3 MacConkey media, 3 Hektoen agar, 4 and in selenite broth 4 ) and anaerobically (Brucella blood agar 3 ). No aerobic or anaerobic bacterial agent was identified as to possible cause of the observed enteritis. Filtered intestinal contents were inoculated into turkey embryo fibroblast tissue culture
Microbiologicals, Sacramento, CA 95827. Difco Laboratories, Detroit, MI 48283. ^elco, Ted Pella, Inc., Redding, CA 96049. ^ a r l Zeiss, Oberkochen, 7082, Germany. 4
Identification of Filamentous Bacteria Bacteria were characterized morphologically. A loopful of bacterial colonies were mixed with a drop of sterile saline on a glass slide, air dried, heat fixed, and Gram stained. Electron microscopy was performed to identify cellular characteristics further. Bacterial pellets were fixed in 2.5% glutaraldehyde in cacodylate buffer and processed. Ultrathin sections were then mounted on copper 300/75 mesh grids 5 and viewed under a Zeiss 10A transmission electron microscope. 6
Poult Inoculation Study The two bacteria, F-l and F-2, were propagated in brain-heart infusion (BHI) broth for 48 h. All poults used in the study were obtained from a commercial hatchery. Twenty-four 1-day-old Nicholas White broadbreasted poults were killed by cervical dislocation and were determined to be free of the organisms that were to be tested through the culturing of jejuna, ceca, and yolk sacs. Three groups, consisting of 10 4-day-old poults each, were given 1 mL of one of the following inocula: 1) F-l suspended in BHI (7 x 10 9 cfu/mL), 2) F-2 suspended in BHI (5 x 10 9 cfu/mL), and 3) BHI (control group). Poults were inoculated via an oral gavage. Each experimental group was done in duplicate. Each group of poults were housed in different isolation rooms of the Animal Resource Service, University of California-Davis. Poults were weighed at Days 0,10, and 21. At 21 days of age, birds were killed by cervical dislocation and necropsied. The jejuna were cultured to reisolate the organisms, F-l and F2. In addition, jejuna were cultured for
Downloaded from http://ps.oxfordjournals.org/ at UCSF Library on April 29, 2015
Isolation of Bacteria
cells to check for the presence of virus via cytopathic effects (CPE). N o CPE were observed in these cells. In addition, samples were submitted to the California Veterinary Laboratory System, Davis, California (CVDLS) for intestinal virus isolation. Results were negative. A direct smear of gut contents, observed under a light microscope for parasites, was negative.
RESEARCH NOTE
205
Downloaded from http://ps.oxfordjournals.org/ at UCSF Library on April 29, 2015 FIGURE 1. A) Filamentous organism, F-l, viewed under a light microscope with oil. B) Filamentous organism, F-2, viewed under a light microscope with oiL C) Filamentous organism, F-l, viewed through the electron microscope. D) Filamentous organism, F-2, viewed through the electron microscope. Calibration bar for A and B represents 10 p.. Calibration bars for C and D represents 1 u.
aerobic bacteria (5% sheep blood agar, MacConkey media, Hektoen agar, and selenite broth), for anaerobic bacteria (Brucella blood agar), and for microaerophilic bacteria (Campylobacter CVA agar), Filtered intestinal contents were tested for virus through the observation of CPE in
turkey embryo fibroblast tissue culture cells. Gut contents were observed directly under a light microscope for parasites. The statistical significance of differences in the rate of gain of inoculated birds and control birds were analyzed via a Student's t test as described by Daniel (1987).
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RESULTS Identification of Bacteria
Poult Inoculation Studies These filamentous organisms were propagated and reinoculated into turkeys. All groups had similar body weights at the start of the experiment (Table 1). These filamentous organisms did not appear to cause diarrhea to the same extent as seen in the field cases but gross necropsy of experimental birds revealed gaseous intestinal contents in poults inoculated with F-l or F-2 3 to 7 days after inoculation. Filamentous organisms F-l and F-2 were reisolated from 80 and 88%, respectively, of the inoculated poults at the end of the experiment. Both F-l and F-2 were not isolated from the control poults. With the exception of Escherichia coli, attempts to isolate other aerobic and anaerobic bacteria
DISCUSSION Previous studies have demonstrated bacteria associated with the intestinal wall of poultry (Fuller and Turvey, 1971; Goodwin et al., 1989; Angel et ah, 1990). Goodwin et al. (1989) have described longsegmented filamentous organisms from the intestines of poults exhibiting clinical signs of enteritis. Angel et al. (1990) associated long-segmented filamentous organisms with a stunting syndrome in turkey poults. Although observed in histopathology sections and electron micrographs, these long-segmented filamentous organisms have never been cultured. The present study reports the first isolation and propagation of two filamentous organisms from clinical cases of enteritis in poults. The successful isolation of these bacteria was probably due to a combination of microaerophilic conditions and by using a medium containing a variety of antibiotics (cefoperazone, vancomycin, and amphotericin B) that inhibit the faster growing enteric bacteria. In clinical cases of enteritis, it has been noticed that a higher number of these organisms are cultured when there is an increase of E. coli organisms cultured from the gut (Morishita, unpublished data). N o other infectious agents (viral, bacterial, or
TABLE 1. Body weights (x ± SD) of poults ioculated with either bacterium, F-l and F-2, at Day 4 (start of experiment). Day 10, and Day 21 Days of age 10 21 (g)_ Control 90.00 ± 7.63 131.21 ± 9.42 306.34 ± 20.34 Bacterium F-l 89.32 ± 9.87 126.08 ± 13.16 263.10 ± 65.87* Bacterium F-2 88.56 ± 6.40 145.41 ± 32.69 271.87 ± 27.95** 1 Each study group consists of 10 birds. There were two study groups per inoculum. *P<.025. **P<.005. Study group1
4
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Two previously undescribed filamentous organisms were isolated from the jejuna of commercially reared poults exhibiting signs of diarrhea. These jejuna were examined histopathologically and demonstrated an increased number of heterophils and lymphocytes in the lamina propria of the villus tips in the jejunum when compared with those of age-matched controls. Both organisms were catalase-negative, nonmotile, and gram-positive. Older culture, after 72 h, revealed Gram-variable staining characteristics. Both organisms had a tendency to form filaments. The F-2 bacteria had a medusa-head colonial margin, but the F-l organism had a smooth, circular colonial margin. Electron micrographs of the bacteria are shown in Figure 1.
from the jejunum were negative. N o CPE were observed in turkey embryo fibroblast tissue culture cells. Intestinal contents were also submitted to the CVDLS for intestinal virus isolation. Results were negative. Direct smear of gut contents did not reveal any internal parasites.
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protozoal) have been isolated from these clinical cases. Inoculation studies of these t w o filamentous organisms, F-l and F-2, have demonstrated a decreased rate of gain in 4-day-old poults. It appears that they have pathogenic potential, however, the exact role they play in the pathogenesis of poult enteritis is unknown. ACKNOWLEDGMENTS
Angel, C. R., J. L. Sell, J. A. Fagerland, D. L. Reynolds, and T. W. TrampeL 1990. Longsegmented filamentous organisms observed in poults experimentally infected with stunting syndrome agent. Avian Dis. 34594-1001. Daniel, W. W., 1987. Pages 188-234 in: Biostatistics: A Foundation for Analysis in the Health Sciences. John Wiley and Sons, Inc., New York, NY. Fuller, R., and A. Turvey, 1971. Bacteria associated with the intestinal wall of the fowl (Gallus domesticus). J. Appl. Bacterid. 34:617-622. Goodwin, M. A., G. Cooper, W. D. Waltman, J. Brown, M. A. Smeltzer, A. A. Bickford, D. A. Anderson, R. E. Bamhart, and T. G. Dickson, 1989. Diarrhea associated with long segmented filamentous organisms (LSFOs) in the small intestines of turkeys, chickens, and quails. Pages 103-109 in: Proceedings of the 38th Western Poultry Disease Conference, March 6-9, 1989, Tempe, AZ. Reynolds, D. L., Y. M. Saif, and K. W. Theil, 1987. A survey of enteric viruses of turkey poults. Avian Dis. 31:89-98. Saif, L. J., Y. M. Saif, and K. W. TheiL 1985. Enteric viruses in diarrheic turkey poults. Avian Dis. 29: 798-811. Schmidt, G. P., C. H. Domermuth, and L. M. Potter, 1988. Effect of oral Escherichia coli inoculation on performance of young turkeys. Avian Dis. 32: 103-107.
Downloaded from http://ps.oxfordjournals.org/ at UCSF Library on April 29, 2015
The authors would like to express their thanks to the California Turkey Industry Federation for their support of this project. Special thanks to the University of California-Davis, Veterinary Medical Teaching Hospital, Microbiology Section (D. Hirsch, S. Jang, B. Davis, D. Early, A. Melli, E. Samitz, and A. Wong) for their technical help and advice in bacteriology, to T. Harrington and J. Schmidt for technical assistance with the transmission electron microscope, and to L. Lowenstine (University of California-Davis, Department of Veterinary Pathology) for pathological assistance with the field cases.
REFERENCES
1992 Poultry Science 71:203-207
INTRODUCTION Poult enteritis is a disease that causes concern in the turkey industry. It results in production losses via decreased feed efficiency, slower growth rate, and increased morbidity and mortality rates, and may predispose the poult to other diseases. Recent research has focused on the virological (Saif et ah, 1985; Reynolds et ah, 1987) and the aerobic bacteriological (Schmidt et ah, 1988) etiologies of poult enteritis. M a n y bacteria, i n c l u d i n g filamentous organisms (Fuller and Turvey, 1971; Goodwin et ah, 1989; Angel et ah, 1990), have been seen in the intestinal wall of the chicken in the crop, ileum, and cecum (Fuller and Turvey, 1971). These filamentous organisms have been observed to be attached to the enterocytes and have been associated with diarrhea in turkeys, chickens, and quail (Goodwin et ah, 1989). Angel et ah (1990) associated these long-segmented filamentous organisms with a stunting syndrome in turkeys.
Veterinary Medical Teaching Hospital. Department of Epidemiology and Preventive Medicine.
However, their exact role in the intestinal tract has not been fully elucidated, partly because of the inability to culture and propagate these organisms. The present study reports on the isolation and propagation of two filamentous organisms isolated from the intestinal tracts of poults exhibiting signs of diarrhea. In addition, the inoculation of poults with these two identified bacterial agents and their subsequent effect on rate of gain was studied.
MATERIALS AND METHODS Source of Birds Commercially reared Nicholas White broadbreasted turkey poults were obtained from several flocks of six ranches in the Central Valley of California. All study flocks had poults demonstrating clinical signs of diarrhea. Poults ranged in age from 1 to 35 days and were selected based on the demonstration of clinical signs of diarrhea, i.e., grossly having fecal material adhering to the vent region of affected birds. Agematched poults were selected based on the absence of clinical signs of diarrhea and served as a control group. Enteritis was
203
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ABSTRACT Two microaerophilic filamentous bacteria have been isolated from the intestines of turkey poults exhibiting signs of enteritis. These two filamentous bacteria, denoted as F-l and F-2, were reinoculated into 4-day-old poults and those poults have shown a reduction in rate of gain when compared with aged-matched controls. Weight reduction was 14% for F-l and 11% for F-2, respectively, at 21 days of age. (Key words: turkeys, poult enteritis, filamentous bacteria, microaerophilic bacteria, weight loss)
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confirmed histologically in those birds with diarrhea. Birds without diarrhea did not have enteritis when examined histologically. There were increased numbers of heterophils and lymphocytes in the lamina propria of the jejunum of birds with diarrhea when compared with the agematched poults that were not showing any clinical signs of enteritis. In all birds examined, no evidence of infectious agents were observed except that filamentous bacteria were seen attached to and embedded in the enterocytes of the villus tips in the jejunum of those birds with enteritis.
Jejuna from these commercially reared poults were cultured on Campylobacter CVA 3 plates. [Campylobacter Agar (CVA) contains proteose peptone (15.0 g), liver digest (2.5 g), yeast extract (2.5 g), sodium chloride (5.0 g), agar (12.0 g), sheep blood (50.0 mL), cefoperazone (20.0 mg), vancomycin (10.0 mg), and amphotericin B (2.0 mg) per liter of deionized, distilled water.] The cultures were incubated at 37 C in the presence of 10% carbon dioxide, 5% oxygen, and 85% nitrogen. The presence of bacterial colonies was evaluated at 24, 48, and 72 h after inoculation. Two colonial types of bacteria were consistently and repeatedly isolated from birds exhibiting diarrhea and confirmed with enteritis histologically. Each of the colonies was picked from the primary isolation plate and restreaked on a fresh Campylobacter CVA plate for further characterization. The colonies were arbitrarily identified as F-l and F-2, respectively. To test for the presence of other bacteria in the intestines, these jejuna were also cultured aerobically (5% sheep blood agar, 3 MacConkey media, 3 Hektoen agar, 4 and in selenite broth 4 ) and anaerobically (Brucella blood agar 3 ). No aerobic or anaerobic bacterial agent was identified as to possible cause of the observed enteritis. Filtered intestinal contents were inoculated into turkey embryo fibroblast tissue culture
Microbiologicals, Sacramento, CA 95827. Difco Laboratories, Detroit, MI 48283. ^elco, Ted Pella, Inc., Redding, CA 96049. ^ a r l Zeiss, Oberkochen, 7082, Germany. 4
Identification of Filamentous Bacteria Bacteria were characterized morphologically. A loopful of bacterial colonies were mixed with a drop of sterile saline on a glass slide, air dried, heat fixed, and Gram stained. Electron microscopy was performed to identify cellular characteristics further. Bacterial pellets were fixed in 2.5% glutaraldehyde in cacodylate buffer and processed. Ultrathin sections were then mounted on copper 300/75 mesh grids 5 and viewed under a Zeiss 10A transmission electron microscope. 6
Poult Inoculation Study The two bacteria, F-l and F-2, were propagated in brain-heart infusion (BHI) broth for 48 h. All poults used in the study were obtained from a commercial hatchery. Twenty-four 1-day-old Nicholas White broadbreasted poults were killed by cervical dislocation and were determined to be free of the organisms that were to be tested through the culturing of jejuna, ceca, and yolk sacs. Three groups, consisting of 10 4-day-old poults each, were given 1 mL of one of the following inocula: 1) F-l suspended in BHI (7 x 10 9 cfu/mL), 2) F-2 suspended in BHI (5 x 10 9 cfu/mL), and 3) BHI (control group). Poults were inoculated via an oral gavage. Each experimental group was done in duplicate. Each group of poults were housed in different isolation rooms of the Animal Resource Service, University of California-Davis. Poults were weighed at Days 0,10, and 21. At 21 days of age, birds were killed by cervical dislocation and necropsied. The jejuna were cultured to reisolate the organisms, F-l and F2. In addition, jejuna were cultured for
Downloaded from http://ps.oxfordjournals.org/ at UCSF Library on April 29, 2015
Isolation of Bacteria
cells to check for the presence of virus via cytopathic effects (CPE). N o CPE were observed in these cells. In addition, samples were submitted to the California Veterinary Laboratory System, Davis, California (CVDLS) for intestinal virus isolation. Results were negative. A direct smear of gut contents, observed under a light microscope for parasites, was negative.
RESEARCH NOTE
205
Downloaded from http://ps.oxfordjournals.org/ at UCSF Library on April 29, 2015 FIGURE 1. A) Filamentous organism, F-l, viewed under a light microscope with oil. B) Filamentous organism, F-2, viewed under a light microscope with oiL C) Filamentous organism, F-l, viewed through the electron microscope. D) Filamentous organism, F-2, viewed through the electron microscope. Calibration bar for A and B represents 10 p.. Calibration bars for C and D represents 1 u.
aerobic bacteria (5% sheep blood agar, MacConkey media, Hektoen agar, and selenite broth), for anaerobic bacteria (Brucella blood agar), and for microaerophilic bacteria (Campylobacter CVA agar), Filtered intestinal contents were tested for virus through the observation of CPE in
turkey embryo fibroblast tissue culture cells. Gut contents were observed directly under a light microscope for parasites. The statistical significance of differences in the rate of gain of inoculated birds and control birds were analyzed via a Student's t test as described by Daniel (1987).
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RESULTS Identification of Bacteria
Poult Inoculation Studies These filamentous organisms were propagated and reinoculated into turkeys. All groups had similar body weights at the start of the experiment (Table 1). These filamentous organisms did not appear to cause diarrhea to the same extent as seen in the field cases but gross necropsy of experimental birds revealed gaseous intestinal contents in poults inoculated with F-l or F-2 3 to 7 days after inoculation. Filamentous organisms F-l and F-2 were reisolated from 80 and 88%, respectively, of the inoculated poults at the end of the experiment. Both F-l and F-2 were not isolated from the control poults. With the exception of Escherichia coli, attempts to isolate other aerobic and anaerobic bacteria
DISCUSSION Previous studies have demonstrated bacteria associated with the intestinal wall of poultry (Fuller and Turvey, 1971; Goodwin et al., 1989; Angel et ah, 1990). Goodwin et al. (1989) have described longsegmented filamentous organisms from the intestines of poults exhibiting clinical signs of enteritis. Angel et al. (1990) associated long-segmented filamentous organisms with a stunting syndrome in turkey poults. Although observed in histopathology sections and electron micrographs, these long-segmented filamentous organisms have never been cultured. The present study reports the first isolation and propagation of two filamentous organisms from clinical cases of enteritis in poults. The successful isolation of these bacteria was probably due to a combination of microaerophilic conditions and by using a medium containing a variety of antibiotics (cefoperazone, vancomycin, and amphotericin B) that inhibit the faster growing enteric bacteria. In clinical cases of enteritis, it has been noticed that a higher number of these organisms are cultured when there is an increase of E. coli organisms cultured from the gut (Morishita, unpublished data). N o other infectious agents (viral, bacterial, or
TABLE 1. Body weights (x ± SD) of poults ioculated with either bacterium, F-l and F-2, at Day 4 (start of experiment). Day 10, and Day 21 Days of age 10 21 (g)_ Control 90.00 ± 7.63 131.21 ± 9.42 306.34 ± 20.34 Bacterium F-l 89.32 ± 9.87 126.08 ± 13.16 263.10 ± 65.87* Bacterium F-2 88.56 ± 6.40 145.41 ± 32.69 271.87 ± 27.95** 1 Each study group consists of 10 birds. There were two study groups per inoculum. *P<.025. **P<.005. Study group1
4
Downloaded from http://ps.oxfordjournals.org/ at UCSF Library on April 29, 2015
Two previously undescribed filamentous organisms were isolated from the jejuna of commercially reared poults exhibiting signs of diarrhea. These jejuna were examined histopathologically and demonstrated an increased number of heterophils and lymphocytes in the lamina propria of the villus tips in the jejunum when compared with those of age-matched controls. Both organisms were catalase-negative, nonmotile, and gram-positive. Older culture, after 72 h, revealed Gram-variable staining characteristics. Both organisms had a tendency to form filaments. The F-2 bacteria had a medusa-head colonial margin, but the F-l organism had a smooth, circular colonial margin. Electron micrographs of the bacteria are shown in Figure 1.
from the jejunum were negative. N o CPE were observed in turkey embryo fibroblast tissue culture cells. Intestinal contents were also submitted to the CVDLS for intestinal virus isolation. Results were negative. Direct smear of gut contents did not reveal any internal parasites.
207
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protozoal) have been isolated from these clinical cases. Inoculation studies of these t w o filamentous organisms, F-l and F-2, have demonstrated a decreased rate of gain in 4-day-old poults. It appears that they have pathogenic potential, however, the exact role they play in the pathogenesis of poult enteritis is unknown. ACKNOWLEDGMENTS
Angel, C. R., J. L. Sell, J. A. Fagerland, D. L. Reynolds, and T. W. TrampeL 1990. Longsegmented filamentous organisms observed in poults experimentally infected with stunting syndrome agent. Avian Dis. 34594-1001. Daniel, W. W., 1987. Pages 188-234 in: Biostatistics: A Foundation for Analysis in the Health Sciences. John Wiley and Sons, Inc., New York, NY. Fuller, R., and A. Turvey, 1971. Bacteria associated with the intestinal wall of the fowl (Gallus domesticus). J. Appl. Bacterid. 34:617-622. Goodwin, M. A., G. Cooper, W. D. Waltman, J. Brown, M. A. Smeltzer, A. A. Bickford, D. A. Anderson, R. E. Bamhart, and T. G. Dickson, 1989. Diarrhea associated with long segmented filamentous organisms (LSFOs) in the small intestines of turkeys, chickens, and quails. Pages 103-109 in: Proceedings of the 38th Western Poultry Disease Conference, March 6-9, 1989, Tempe, AZ. Reynolds, D. L., Y. M. Saif, and K. W. Theil, 1987. A survey of enteric viruses of turkey poults. Avian Dis. 31:89-98. Saif, L. J., Y. M. Saif, and K. W. TheiL 1985. Enteric viruses in diarrheic turkey poults. Avian Dis. 29: 798-811. Schmidt, G. P., C. H. Domermuth, and L. M. Potter, 1988. Effect of oral Escherichia coli inoculation on performance of young turkeys. Avian Dis. 32: 103-107.
Downloaded from http://ps.oxfordjournals.org/ at UCSF Library on April 29, 2015
The authors would like to express their thanks to the California Turkey Industry Federation for their support of this project. Special thanks to the University of California-Davis, Veterinary Medical Teaching Hospital, Microbiology Section (D. Hirsch, S. Jang, B. Davis, D. Early, A. Melli, E. Samitz, and A. Wong) for their technical help and advice in bacteriology, to T. Harrington and J. Schmidt for technical assistance with the transmission electron microscope, and to L. Lowenstine (University of California-Davis, Department of Veterinary Pathology) for pathological assistance with the field cases.
REFERENCES