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Can Fusarium graminearum Survive Through the Digestive Tract of Cattle?

Published: January 19, 2009
By: Shannon L. Scott, Debra L. McLaren, T. Kelly Turkington, Yuxi Wang, and Tim McAllister - Presented at the 3rd Canadian Barley Symposium (Republished by the Government of Alberta Agriculture and Rural Development)
First recognised in a few fields in southern Manitoba in the early 1980’s, by the late 1990’s Fusarium Head Blight (FHB) had spread to cereal crops in south-eastern Saskatchewan. The Western Grains Research Foundation estimated that FHB has cost cereal producers and secondary processors over $1 billion due to losses in yield and end use quality (WGRF 2001). Fusarium head blight, caused by the fungus Fusarium graminearum, can occur on all small grain crops, particularly barley and wheat (McMullen and Stack 1999). Corn is also susceptible to infection by F. graminearum; the same fungus in its sexual stage, called Gibberella zeae, causes pink ear rot, or Gibberella ear rot, and stalk rot in corn (White 1999).

Until recently, losses due to FHB were experienced mainly by producers in Manitoba. Unfortunately, FHB is no longer only a concern for Manitoba producers. In 1993, this fungus was detected at very low levels in south-eastern Saskatchewan, and has been building up to the point where in 1998 it has become an important disease in this region affecting both wheat and barley. Surveys conducted by the Canadian Grain Commission (CGC) have shown a westward movement of this pathogen (Clear and Patrick 2000; 2003). Should it become well established in the province of Alberta, it could have a significant effect on the ability of that province to produce disease- and mycotoxin-free grain for the pivotal swine, malting and food sectors.

Not only does F. graminearum infection cause yield losses in grain and corn, it can also downgrade their nutritive, physical and chemical qualities, resulting in their being used for animal feed rather than for human consumption (Charmley et al. 1994). A contaminated crop can be salvaged by feeding it to livestock or poultry, but further losses may be incurred due to the negative effects of fungal metabolites, called mycotoxins, on animal performance. The most common mycotoxins produced by F. graminearum are deoxynivalenol (DON, also known as vomitoxin), 15-acetyldeoxynivalenol, and nivalenol. Belonging to a group of compounds known as trichothecenes, these mycotoxins are attributed with diminishing feed consumption in domestic livestock, especially swine (CAST 2003). Even though DON is one of the least toxic metabolites synthesised by Fusarium species (Abramson 1998), effects of feeding swine mycotoxin-contaminated grain on growth and feed consumption (Smith et al. 1997; Trenholm et al. 1994) and on the immune system (Overnes et al. 1997; Rotter et al. 1994) have been well documented. Less information is available on the effects of DON contamination in cattle.

Ruminants seem to be more tolerant of trichothecene contamination of grain, possibly due to detoxification by rumen micro-organisms. When DON (equivalent to a feed contamination level of 10 ppm) was incubated in vitro with rumen fluid over 24 hours, virtually all of it was transformed by the rumen microbes (King et al. 1984). Finishing cattle were fed diets with three levels of DON (0.2, 2.3, and 10.0 ppm) by substituting wheat screenings contaminated with DON for high-moisture corn. No effects on average daily gain (ADG), dry matter intake (DMI), or feed conversion (F:G) were observed (Wagner 1993). Feedlot steers fed diets containing FHB-infested barley during the growing and finishing periods (total ration DON levels of 0.9, 3.7, 6.4, and 9.2 ppm during the growing period and 1.1, 5.0, 8.8 and 12.6 ppm during the finishing period) did not show any effects of DON levels on ADG, DMI or F:G (Anderson et al. 1996).

Because of their apparent tolerance for higher levels of dietary DON than swine, Fusarium-infested grains are often fed to cattle or sheep as opportunity feeds. Over the last few years, there have been reports of significant quantities of F. graminearum infected feed grain moving westward into Alberta to be fed to feedlot cattle. Concerns continue to be expressed regarding the movement of F. graminearum-infected feed grain into Alberta, due to the possibility that feeding these opportunity feeds will increase the spread of FHB into Alberta. However, this would require that the fungal pathogen would have to survive through the digestive tract. Currently, little information is available regarding the ability of plant pathogens to survive as they move through the gastrointestinal tract of cattle. Some fungi have the ability to survive passage through the digestive tract of cattle, eventually sporulating on the infested dung (Kendrick 1985; Atlas & Bartha 1981; Hauser 1999). If the fungus F. graminearum can survive consumption and processing by livestock, especially feeder cattle, this may represent an important method of introducing FHB into areas where it has not previously been found or where its occurrence is rare. We have therefore undertaken studies to evaluate the potential for spread of F. graminearum via feed grain after passage through the digestive system of feedlot cattle.



Study 1: Isolation of Plant Pathogenic Fungi from Barley Grain Collected from Alberta and Manitoba Feed Bunks and Manure



Materials and methods


Feedbunk grain and manure samples were collected from feedlots in Alberta and Manitoba during three years (1999-2001), with samples processed at the AAFC Lacombe Research Centre, Lacombe, AB. From the bunk samples for each feedlot, 25 intact barley kernels were collected for further pathogen isolation. Manure samples from each feedlot were suspended in water and passed through screens to retain any cereal grain present in the manure. Twenty-five whole intact barley kernels were then collected from the screened material for each feedlot. Intact whole kernels from either the feed bunks or manure were incubated on an agar growth medium for up to 10 days, followed by identification of any plant pathogenic fungi that were present.


Results


Results were obtained for a number of pathogenic fungi, but only the results for F. graminearum are reported here. In 1999, samples from five feedlots were collected and evaluated. No F. graminearum was detected in the feed bunk barley grain or on the whole barley kernels screened from manure. In 2000, bunk and manure samples were collected from 6 feedlots in Alberta and 8 in Manitoba. No F. graminearum was detected from the Alberta feed bunk samples. In Manitoba, the mean incidence of F. graminearum in barley grain from feed bunks was 23.3%. No F. graminearum was detected in the barley grain screened from either Alberta or Manitoba feedlot manure samples. In 2001, feed bunk and manure samples were collected from 2 feedlots in Alberta and 6 in Manitoba. No F. graminearum was detected from the Alberta feed bunk grain samples. In Manitoba, the mean incidence of F. graminearum in barley grain from feed bunks was 6.7%. No F. graminearum was detected in the barley grain screened from either Alberta or Manitoba feedlot manure samples.



Study 2: Determination of Viability of Fusarium graminearum in Beef Manure



Materials and methods


The purpose of this study was to determine the survival of F. graminearum when it was added to fresh or sterilised beef manure. F. graminearum colonised barley was prepared in the laboratory by inoculating clean barley with the fungus. Kernels of Fusarium-colonised and clean barley were plated on an agar growth medium and the results were read one week later. Fresh beef manure was then obtained from the feedlot at the AAFC Brandon Research Centre. Half the manure was sterilised by autoclaving. One hundred kernels of clean or F. graminearum-infested barley, placed in mesh bags, were added to 250 ml samples of fresh or sterilised manure and samples were incubated at 39°C for 24 hours. The mesh bags were washed, kernels were removed and plated on an agar growth medium and the presence or absence of F. graminearum was read one week later.


Results


The results (Table 1), based on two tests of 50 kernels each, showed that the method of inoculating barley was successful and that no (test 1) or trace (test 2) levels of F. graminearum were found in the clean barley. In addition (Table 2), F. graminearum in infected kernels remained viable in sterilised (autoclaved) manure, but not when placed in fresh manure.


Table1. Number and percentage of Fusarium graminearum infected barley kernels.


 
Number kernels plated
Number F. graminearum infected
% F. graminearum infected
F. graminearum colonised barley
100
100
100
Clean barley
100
3
3



Table 2. The effect of fresh and sterilised beef manure on viability of Fusarium graminearum on barley kernels.

Manure
Barley
Rep
Number kernels plated
Number F. graminearum infected
% F. graminearum infected
Autoclaved
Clean
1
200
0
0
 
2
200
1
0.5
 
3
200
0
0
 
4
200
0
0
Autoclaved
F. graminearum colonised
1
200
63
31
 
2
200
25
12
 
3
200
59
30
 
4
200
78
39
Fresh
Clean
1
200
0
0
 
2
200
0
0
 
3
200
0
0
 
4
200
0
0
Fresh
F. graminearum colonised
1
200
1
0.5
 
 
2
200
1
0.5
 
 
3
200
0
0
 
 
4
200
0
0




Study 3: Preliminary Feeding Trial to Determine Survival of Fusarium graminearum through the Ruminant Digestive Tract



Materials and methods

Two steers that had been feed a hay only diet were fed 600 g of a mixture of equal parts of intact Fusarium graminearum-colonised barley and sterile steam rolled barley. The purpose of feeding two forms of barley was to be able to distinguish the F. graminearum-colonised barley in the manure collected from these steers. The Fusarium-colonised barley had 6.4 ppm (March trial) and 15.4 ppm (April trial) DON. The steers were fed this mixture of barley individually for three days. Faecal samples were collected from each steer approximately 24, 48, 72, and 96 hours after the first feeding of barley. Intact barley kernels were isolated from each manure sample as in Study 1, plated on an agar growth medium and examined one week later for the presence or absence of F. graminearum.


Results

Of the intact barley kernels that were screened from the manure samples, only one sample showed any evidence of survival through the digestive tract (Table 3).


Table 3. Survival of Fusarium graminearum through the digestive tract of two steers.

Steer #
Sample Date
Sample Time
Sample Volume (ml)
Number kernels plated
Number F. graminearum infected
% F. graminearum infected
M 791
11-Mar-03
2:00 p.m.
1800
85
0
0
 
12-Mar-03
1:00 p.m.
1000
116
0
0
 
13-Mar-03
12:45 p.m.
1200
86
0
0
 
14-Mar-03
12:15 p.m.
1500
15
0
0
M 795
11-Mar-03
2:00 p.m.
1800
104
0
0
 
12-Mar-03
1:00 p.m.
2300
148
0
0
 
13-Mar-03
1:45 p.m.
1100
21
0
0
 
14-Mar-03
12:30 p.m.
800
3
0
0
Steer #
Sample Date
Sample Time
Sample Volume (ml)
Number kernels plated
Number F. graminearum infected
% F. graminearum infected
M 791
22-April-03
11:00 am
800
46
1
2
 
23-April-03
1:00 p.m.
1100
58
0
0
 
24-April-03
1:00 p.m.
1000
57
0
0
 
25-April-03
1:00 p.m.
800
13
0
0
M 795
22-April-03
2:15 p.m.
1000
1
0
0
 
23-April-03
1:00 p.m.
900
19
0
0
 
24-April-03
1:00 p.m.
800
13
0
0
 
25-April-03
1:00 p.m.
800
5
0
0




Conclusions

Survey results from Alberta and Manitoba feedlots indicated that while many fungal species were readily detected from barley grain sampled from feed bunks, they were not detected from whole intact grain screened from manure from these same feedlots. Passage through the bovine digestive tract may help to eliminate a number of plant pathogenic fungi present in feed grain, but the survey study does not imply cause and effect. The survival of F. graminearum was reduced by placing infected barley kernels directly into manure, with almost complete elimination occurring with non-autoclaved manure. Preliminary feeding trials with infected barley indicated almost complete elimination of F. graminearum after passage through beef steers. Results from all three studies indicate that the risk of survival of F. graminearum in infected grain after passage through beef animals followed by incubation in manure is very limited. Further trials are planned, including the use of fistulated animals.


Acknowledgements


The support of the Alberta Agricultural Research Institute, the Alberta Crop Industry Development Fund, and the Agriculture and Agri-Food Canada Matching Investment Initiative Program is gratefully acknowledged.


Literature cited


Abramson, D. Mycotoxin formation and environmental factors. Pages 255-277 in Mycotoxins in Agriculture and Food Safety, K.K. Sinha and D. Bhatnagar, eds. Marcel Dekker, Inc., New York, NY.

Anderson, V.L., Boland, E.W., and Casper, H.H. 1996. Effects of vomitoxin (deoxynivalenol) from scab-infested barley on performance of feedlot and breeding beef cattle. J. Anim. Sci. 74(Suppl. 1): 208.

Atlas, R.M., and R. Bartha. 1981. Microbial ecology: fundamentals and applications. Addison-Wesley Publishing Company, Inc. 560 pp.

CAST (Council for Agricultural Science and Technology). 2003. Mycotoxins: Risks in Plant, Animal and Human Systems. CAST, Ames, Iowa, USA. 199 pp.

Charmley, L.L., Rosenberg, A., and Trenholm, H.L. 1994. Factors responsible for economic losses due to Fusarium mycotoxin contaminants of grains, foods, and feedstuffs. Pp.s 471-486 in J.D. Miller and H.L. Trenholm (eds.) Mycotoxins in Grains: Compounds Other Than Aflatoxins. Eagan Press, St. Paul, MN

Clear, R.M., and Patrick, S.K. 2000. Fusarium head blight pathogens isolated from fusarium-damaged kernels of wheat in western Canada, 1993 to 1998. Can. J. Plant Pathol. 22: 51-60.

Clear, R.M., and Patrick, S.K. 2003. Fusarium head blight in Canada. [Online] Available:
http://www.grainscanada.gc.ca/Pubs/fusarium/fusarium-e2.htm. [7 February 2003].

Hauser, J.T. 1999. Be it ever so humble, there’s no place like dung. Carolina Biological Supply Company (no longer available at this URL - www.gene.com/ae/RC/CT/no_place_like_dung.html)

Kendrick, B. 1985. The fifth kingdom. Mycologue Publications. 364 pp.

King, R.R., McQueen, R.E., Levesque, D., and Greenhalgh, R. 1984. Transformation of deoxynivalenol (vomitoxin) by rumen micro-organisms.

McMullen, M.P., and Stack, R.W. 1999. Fusarium Head Blight (Scab) of Small Grains. North Dakota State University Extension Service Publication no. PP-804. Available online at
http://www.ext.nodak.edu/extpubs/plantsci/smgrains/pp804w.htm.

Overnes G., Matre, T., Sivertsen, T., Larsen, H.J.S., Langseth, W., Reitan, L.J. and Jansen, J.H. 1997. Effects of diets with graded levels of naturally deoxynivalenol-contaminated oats on immune response in growing pigs. Zentralblatt Fur Veterinarmedizin - Reihe A. 44: 539-550.

Rotter, B.A., Thompson, B.K., Lessard, M., Trenholm, H.L. and Tryphonas, H. 1994. Influence of low-level exposure to Fusarium mycotoxins on selected immunological and hematological parameters in young swine. Fundam. Appl. Toxicol. 23:117-124.

Smith, T.K., McMillan, E.G. and Castillo, J.B. 1997. Effect of feeding blends of Fusarium mycotoxin-contaminated grains containing deoxynivalenol and fusaric acid on growth and feed consumption of immature swine. J. Anim. Sci. 75: 2184-2191.

Trenholm, H.L., Foster, B.C., Charmley, L.L., Thompson, B.K., Hartin, K.E., Coppock, R.W. and Albassam, M.A. 1994. Effects of feeding diets containing Fusarium (naturally) contaminated wheat or pure deoxynivalenol (DON) in growing pigs. Can. J. Animal Science 74: 361-369.

Wagner, J.J. 1993. Scab-infested wheat or barley for feedlot cattle or sheep. Extension Extra no. 2017, Co-operative Extension Service, South Dakota State University/USDA.

Western Grains Research Foundation. 2001. The "State of the Union" on Fusarium. WGRF Industry Report, February, 2001, p. 1.

White, D.G. 1999. Compendium of corn diseases. 3rd Ed. APS Press, St. Paul, MN, 78 pp.



Authors: Shannon L. Scott1, Debra L. McLaren1, T. Kelly Turkington2, Yuxi Wang3, and Tim McAllister3

Agriculture and Agri-Food Canada (AAFC)
1 AAFC, Brandon Research Centre
2 AAFC, Lacombe Research Centre
3 AAFC, Lethbridge Research Centre



Presented at the
3rd Canadian Barley Symposium (June 19-20, 2003)
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