Intercurrent coccidiosis and necrotic enteritis of chickens: rational, integrated disease management by maintenance of gut integrity

Figures & data

Figure 1. Some factors that contribute to wet litter in commercial poultry flocks.

Table 1. In vivo efficacy of antibiotic growth promoters and ionophores included alone in various diets against clinical NE in chickens

Compound	Concentration (parts/10^6)	Efficacy^a	Major cereals	Animal proteins	Reference^b
Avilamycin	10	Good	42% wheat/20% barley/10% oats	5% fish-meal/2% meat-meal	Elwinger et al. (1998)
Avoparcin	5.5	Marginal	Not stated	50% fish-meal	Prescott (1979)
Avoparcin	15	Good	42% wheat/20% barley/10% oats	5% fish-meal/2% meat-meal	Elwinger et al. (1998)
Avoparcin	19	Good	Not stated	50% fish-meal	Prescott (1979)
Bacitracin	25	Good	Not stated	50% fish-meal	Prescott (1979)
Lincomycin	1.8	Poor	Not stated	50% fish-meal	Truscott & Al-Sheikhly (1977)
Lincomycin	18	Moderate	Not stated	50% fish-meal	Truscott & Al-Sheikhly (1977)
Monensin	100	Moderate	42% wheat/20% barley/10% oats	5% fish-meal/2% meat-meal	Elwinger et al. (1998)
Narasin	70	Moderate	42% wheat/20% barley/10% oats	5% fish-meal/2% meat-meal	Elwinger et al. (1998)
Narasin	70	Moderate	Not stated (“broiler diets”)	Fish-meal	Brennan et al. (2001)
Virginiamycin	5, 10, 15, 20, 40	Moderate	Not stated	26% fish-meal	George et al. (1982)
Virginiamycin	20	Good	50% barley/11% wheat/10% oats	3% fish-meal	Elwinger & Teglöf (1991)
Virginiamycin	20	Moderate	24% wheat/41% barley	7% fish-meal/3% meat-meal and bone-meal	Jansson et al. (1990)
Virginiamycin	40	Moderate	24% wheat/41% barley	7% fish-meal/3% meat-meal and bone-meal	Jansson et al. (1990)
^aAssessments in this table are subjective, based on the author's judgement of published clinical results.
^bOther references are available, but often the experimental methods are not detailed enough for inclusion, or the concomitant use of an additional anticoccidial drug or AGP confounds the results for the compound being tested.

Table 2. In vitro sensitivities of C. perfringens isolated from chickens (C) or turkeys (T) to antibiotic growth promoters and ionophores

Compound	Number of strains	% of strains resistant^a	Date of isolation	Country	Reference^b
Amoxycillin	44 (C)	0	2002	Belgium	Martel et al. (2004)
Ampicillin	20 (C/T)	0	1997 to 2002	Denmark	Johansson et al. (2004)
Ampicillin	22 (C/T)	0	1986 to 2001	Norway	Johansson et al. (2004)
Ampicillin	58 (C/T)	0	2000 to 2001	Sweden	Johansson et al. (2004)
Avilamycin	31 (C)	0	1992	Belgium	Devriese et al. (1993)
Avilamycin	44 (C)	0	2002	Belgium	Martel et al. (2004)
Avilamycin	20 (C/T)	0	1997 to 2002	Denmark	Johansson et al. (2004)
Avilamycin	22 (C/T)	0	1986 to 2001	Norway	Johansson et al. (2004)
Avilamycin	58 (C/T)	0	2000 to 2001	Sweden	Johansson et al. (2004)
Avilamycin	26 (C)	0	Pre-1996	USA	Watkins et al. (1997)
Avilamycin	22 (T)	0	Pre-1996	USA	Watkins et al. (1997)
Avoparcin	31 (C)	0	1992	Belgium	Devriese et al. (1993)
Avoparcin	26 (C)	0	Pre-1996	USA	Watkins et al. (1997)
Avoparcin	22 (T)	0	Pre-1996	USA	Watkins et al. (1997)
Bacitracin	31 (C)	6	1992	Belgium	Devriese et al. (1993)
Bacitracin	20 (C/T)	15	1997 to 2002	Denmark	Johansson et al. (2004)
Bacitracin	22 (C/T)	0	1986 to 2001	Norway	Johansson et al. (2004)
Bacitracin	58 (C/T)	3	2000 to 2001	Sweden	Johansson et al. (2004)
Bacitracin	26 (C)	88	Pre-1996	USA	Watkins et al. (1997)
Bacitracin	22 (T)	9	Pre-1996	USA	Watkins et al. (1997)
Cationomycin	3 (C)	0	Pre-1988	Japan	Benno et al. (1988)
Chlortetracycline	46 (C)	67	2002	Belgium	Martel et al. (2004)
Erythromycin	20 (C/T)	0	1997 to 2002	Denmark	Johansson et al. (2004)
Erythromycin	22 (C/T)	0	1986 to 2001	Norway	Johansson et al. (2004)
Erythromycin	58 (C/T)	0	2000 to 2001	Sweden	Johansson et al. (2004)
Flavophospholipol	31 (C)	100	1992	Belgium	Devriese et al. (1993)
Flavophospholipol	44 (C)	100	2002	Belgium	Martel et al. (2004)
Lasalocid	44 (C)	0	2002	Belgium	Martel et al. (2004)
Lincomycin	44 (C)	64	2002	Belgium	Martel et al. (2004)
Lincomycin	26 (C)	58	Pre-1996	USA	Watkins et al. (1997)
Lincomycin	22 (T)	50	Pre-1996	USA	Watkins et al. (1997)
Lysocellin	3 (C)	0	Pre-1988	Japan	Benno et al. (1988)
Maduramycin	44 (C)	0	2002	Belgium	Martel et al. (2004)
Monensin	44 (C)	0	2002	Belgium	Martel et al. (2004)
Monensin	3 (C)	0	Pre-1988	Japan	Benno et al. (1988)
Monensin	26 (C)	0	Pre-1996	USA	Watkins et al. (1997)
Monensin	22 (T)	0	Pre-1996	USA	Watkins et al. (1997)
Narasin	44 (C)	0	2002	Belgium	Martel et al. (2004)
Narasin	20 (C/T)	0	1997 to 2002	Denmark	Johansson et al. (2004)
Narasin	22 (C/T)	0	1986 to 2001	Norway	Johansson et al. (2004)
Narasin	58 (C/T)	0	2000 to 2001	Sweden	Johansson et al. (2004)
Narasin	26 (C)	0	Pre-1996	USA	Watkins et al. (1997)
Narasin	22 (T)	0	Pre-1996	USA	Watkins et al. (1997)
Oxytetracycline	20 (C/T)	10	1997 to 2002	Denmark	Johansson et al. (2004)
Oxytetracycline	22 (C/T)	29	1986 to 2001	Norway	Johansson et al. (2004)
Oxytetracycline	58 (C/T)	76	2000 to 2001	Sweden	Johansson et al. (2004)
Penicillin	26 (C)	0	Pre-1996	USA	Watkins et al. (1997)
Penicillin	22 (T)	0	Pre-1996	USA	Watkins et al. (1997)
Portmicin	3 (C)	0	Pre-1988	Japan	Benno et al. (1988)
Salinomycin	31 (C)	0	1992	Belgium	Devriese et al. (1993)
Salinomycin	44 (C)	0	2002	Belgium	Martel et al. (2004)
Salinomycin	3 (C)	0	Pre-1988	Japan	Benno et al. (1988)
Tilmicosin	26 (C)	0	Pre-1996	USA	Watkins et al. (1997)
Tilmicosin	22 (T)	18	Pre-1996	USA	Watkins et al. (1997)
Tylosin	31 (C)	3	1992	Belgium	Devriese et al. (1993)
Tylosin	44 (C)	0	2002	Belgium	Martel et al. (2004)
Tylosin	26 (C)	0	Pre-1996	USA	Watkins et al. (1997)
Tylosin	22 (T)	18	Pre-1996	USA	Watkins et al. (1997)
Vancomycin	20 (C/T)	0	1997 to 2002	Denmark	Johansson et al. (2004)
Vancomycin	22 (C/T)	0	1986 to 2001	Norway	Johansson et al. (2004)
Vancomycin	58 (C/T)	0	2000 to 2001	Sweden	Johansson et al. (2004)
Virginiamycin	31 (C)	6	1992	Belgium	Devriese et al. (1993)
Virginiamycin	20 (C/T)	0	1997 to 2002	Denmark	Johansson et al. (2004)
Virginiamycin	22 (C/T)	14	1986 to 2001	Norway	Johansson et al. (2004)
Virginiamycin	58 (C/T)	0	2000 to 2001	Sweden	Johansson et al. (2004)
Virginiamycin	26 (C)	38	Pre-1996	USA	Watkins et al. (1997)
Virginiamycin	22 (T)	45	Pre-1996	USA	Watkins et al. (1997)
^aStrains were deemed to be resistant if so stated by the authors or if responses of a number of strains were bimodal.
^bWhile other references are available, data are not always presented in a form that facilitates inclusion in this table.

Table 3. The impact of some pathophysiological effects of coccidioses on the development of clostridial infections in the chicken's intestine

Eimeria species of chicken	Pathophysiological effect on chicken	Impact on clostridial development in chicken
All	Reduced feed and water intake	Immunodepression
All	Increased gut passage time	Increased proliferation
E. acervulina, E. tenella, E. praecox	Reduced digesta viscosity	Neutral?
All (except E. tenella?)	Reduced protein digestion	Increased proliferation
All	Intestinal leakage of plasma proteins	Increased proliferation
E. Acervulina, E. brunetti, E. maxima, E. necatrix	Reduced intestinal pH	Reduced proliferation and toxin production
All	Mucosal damage	Increased adhesion and toxin production

Figure 2. The intercurrent coccidiosis-NE syndrome: a network of potentially important pathophysiological, medicinal, nutritional and husbandry factors. Those with solid-line arrows and ellipses are beneficial in controlling disease, those with dashed-line arrows and ellipses impart high disease risk. Major high-risk relationships are shown by double-line arrows. AGP, antibiotic growth promoter; CIA, chick infectious anaemia; CEP, competitive exclusion product; Cp, Clostridium perfringens; IBD, infectious bursal disease; MD, Marek's disease; NE, necrotic enteritis.

Table 4. Occurrence in chickens (C) or turkeys (T) of spontaneous coccidial infections and NE cases in circumstances where susceptible birds were exposed to a contaminated environment, but no experimental challenges were administered

Husbandry type	AGP	Anticoccidial	NE	No coccidia	Coccidiasis	Coccidiosis	Reference
Field case in broilers (T)	Not stated	Not stated	Yes	No	No	No	Eleazer & Harrell (1976)
Field case (C)	None	None	Yes	No	No	Yes	Bennetts (1930)
Field case in broilers (C)	Not stated	Not stated	Yes	No	No	Yes	Gardiner (1967)
Field case in broilers (C)	Not stated	Not stated	Yes	No	No	Yes	Nairn & Bamford (1967)
Floor-pen (C)	None	Present but not identified	Yes	No	No	Yes	Maxey & Page (1977)
Field case in caged pullets (C)	None	None	Yes	No	No	Yes	Frame & Bickford (1986)
Field case in breeders (T)	None	None	Yes	No	No	Yes	Droual et al. (1994)
Field cases in broilers (C)	Not stated	Present but not identified	Yes	No	Yes	No	Nairn & Bamford (1967)
Field cases in broilers (C)	Not stated	Not stated	Yes	No	Yes	No	Helmboldt & Bryant (1971)
Field cases (C)	Not stated	Present but not identified	Yes	No	Yes	No	Bernier et al. (1974)
Field cases in broilers (C)	Not stated	Not stated	Yes	No	Yes	No	Long et al. (1974)
Field case in caged pullets (C)	None	None	Yes	No	Yes	No	Broussard et al. (1986)
Field cases in broilers (C)	Not stated	Not stated	Yes	No	Yes	No	Kaldhusdal et al. (1995)
Field cases in broilers (C)	Not stated	Not stated	Yes	Yes	No	No	Helmboldt & Bryant (1971)
Field cases in broilers (C)	Not stated	Not stated	Yes	Yes	No	No	Long et al. (1974)
Field case in caged pullets (C)	Not stated	Not stated	Yes	Yes	No	No	Char et al. (1986)
Floor-pen (C)	None	None	Yes	Yes	No	No	Kaldhusdal & Hofshagen (1992)
Field trial (C)	None	Monensin	Yes	Yes	No	No	Mitsch et al. (2004)
Field case in cockerels (C)	Not stated	Not stated	Yes	Not stated	Not stated	No	Parish (1961a)
Field case in broilers (C)	Not stated	Not stated	Yes	Not stated	Not stated	No	Bains (1968)
Floor-pen (C)	None	Clopidol	Yes	Not stated	Not stated	No	Wicker et al. (1977)
Floor-pen (C)	Lincomycin	Present but not identified	No	No	No	Yes	Maxey & Page (1977)
Floor-pen (C)	None	None	No	No	Yes	No	Waldenstedt (2003)
Field cases in broilers (C)	Not stated	Not stated	No	Yes	No	No	Long et al. (1974)
Field trial (C)	None	Monensin	No	Yes	No	No	Mitsch et al. (2004)
Floor-pen (C)	None	Clopidol	No	Not stated	Not stated	No	Cowen et al. (1987)

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