Risk Assessment
Campylobacter infection transmission from pigs to man
using erythromycin resistance as a marker

by
David G S Burch BVetmed MRCVS
Octagon Services Ltd, Old Windsor, Berks, United Kingdom
 
paper given at the
International Conference on Antimicrobial Agents in Veterinary Medicine
Helsinki, Finland, August, 2002

 

Abstract:

The transmission of Campylobacter infections from meat to man is considered one of the major routes of spread, along with water contamination, of this increasingly common form of infectious intestinal disease. To make a risk assessment of the likely transmission from pigs to man, a database was established from a variety of references, as there was much variation in the data and few were sufficiently complete to allow for a quantitative assessment to be made. It was noted that erythromycin resistance was very high in pigs for both C. jejuni and C. coli in comparison with man and chicken, thought to be one of the major sources of infection and that this would act as a possible marker to determine the transmission rate of campylobacter spp. from pigs to man. There was no evidence of transmission of C. jejuni from pigs to man, as the organism was rarely isolated in pigs (4%) in comparison with chicken (90%) and man (92%) and resistance rates were very low at 2% in man, chicken 4% and 35% in pigs. With regard to C. coli, isolation in pigs is very high (96%) but low in chicken (10%) and man (8%) and erythromycin resistance in man (15%) is similar to chickens (15%) but much lower than in pigs (57%). This confirms that pig meat and environmental contamination by slurry / waste from pigs via water can be considered either a no risk or very low risk in the transmission of campylobacter infections to man and therefore also a no risk or very low risk in the transmission of antimicrobially resistant strains to man.

Introduction:

Campylobacter spp have become the most frequently reported cause of gastrointestinal infections in man, even more than Salmonella spp. (House of Lords, 1998). In 1999, 61713 reports were recorded in the UK and it was estimated from earlier studies that only 50% of cases went to the doctor, about one eighth of cases were reported and that the best estimate of cases of Campylobacter infections in the country was 870/100,000 population (0.87%). In Denmark it was estimated to be only 82 cases /100,000 population (Danmap, 2001) but in the United States an estimated 2.4 million persons were affected each year (0.84%) by the Center for Disease Control and Prevention (2001). An estimated 124 cases were fatal each year (0.00004%) and life-threatening sepsis could occur in immuno-compromised patients. The condition is thought to be primarily transmitted by contact with contaminated food, particularly raw or undercooked poultry meat and possibly unpasteurised milk. Water also has a role and the incidence increases 3-4 times in the summer months, possibly associated with swimming and environmental contamination may be a factor. Campylobacter jejuni is the main cause of disease in man but C. coli is also found. It was the purpose of this work to review the current literature, to determine the incidence of the different Campylobacter spp. in each animal species, examine their antimicrobial resistance patterns and to assess the risk of transmission from pigs to man.

 

Campylobacter spp. incidence - determination for each animal species:

Papers, which had a comparative isolation data of C. jejuni and C. coli from different animal species, were used to obtain comparative isolation percentages for each species.

Table 1. Campylobacter spp. determination for each animal species

Reference

Man

Chicken

Pig

Cattle

 

CJ

CC

CJ

CC

CJ

CC

CJ

CC

Aarestrup et al, 1997

75

7

95

17

3

99

29

0

House of Lords, 1998

1113

150

-

-

-

-

-

-

Marano et al, 1999

535

28

-

-

-

-

-

-

Saenz et al, 2000

537

10

59

10

0

37

-

-

Kramer et al, 2000

133

16

-

-

-

-

-

-

Danmap 2000, 2001

49

0

438

40

11

154

50

1

SVARM 2001, 2002

-

-

42

7

7

91

67

0

Teale, 2002

-

-

-

-

27

712

-

-

Total

2442

211

634

74

48

1093

144

1

Isolation incidence (%)

 

92

 

8

90

 

10

4

 

96

99

 

1

Legend: CJ = C. jejuni; CC = C. coli.

C. jejuni predominate in man (92%), chicken (90%) and cattle (99%), but C. coli is the most frequently isolated species in the pig (96%).

 

Antimicrobial resistance patterns in campylobacter spp. from several species:

The antimicrobial resistance patterns of C. jejuni and C. coli from a variety of animal species were compared in a Danish national surveillance study (Aarestrup et al, 1997) using an minimum inhibitory concentration (MIC) method with established breakpoints and it was highly noticeable that erythromycin (macrolide) resistance was higher in pigs in comparison with other animal species isolates. Human use of antimicrobials may also have an impact.

 

Table 2. Antimicrobial resistance (%) by Campylobacter spp. and by animal species (Denmark)

 

Man

Chicken

Pig

Cattle

Antimicrobial/Breakpoint

CJ

CC

CJ

CC

CJ

CC

CJ

CC

Erythromycin 8µg

0

14

6

18

33

74

3

-

Tylosin 64µg

0

14

6

18

33

73

3

-

Enrofloxacin 2µg

3

29

4

0

33

13

3

-

Tetracycline 16µg

11

0

2

0

0

1

0

-

Ampicillin 32µg

16

0

6

0

0

17

3

-

Gentamicin 16µg

0

0

0

0

0

0

0

-

(Source: Aarestrup et al, 1997)

A similar but regional Spanish study was also of interest for comparison purposes.

 

Table 3. Antimicrobial resistance (%) by Campylobacter spp. and by animal species (Spain)

 

Man

Chicken

Pig

Antimicrobial/disc strength

CJ

CC

CJ

CC

CJ

CC

Erythromycin 15µg

3

35

0

0

-

81

Ciprofloxacin 5µg

75

71

99

100

-

100

Tetracycline 30µg

-

-

32

0

-

94

Ampicillin 10µg

38

29

47

90

-

66

Gentamicin 10µg

0

9

12

80

-

22

(Source: Saenz et al, 2000)

Resistance assessments were different between the two studies with the Spanish study using sensitivity discs but both were according to NCCLS guidelines. Fluoroquinolone resistance can be judged as high across all species tested in Spain and that erythromycin resistance is high for C. coli from pigs but not in poultry confirming it as a differentiating marker.

Establishing an international database to compare erythromycin resistance in Campylobacter spp. and animal species

There would appear to be a substantial variation in resistance between countries and not all countries have the full information required to be able to carry out a quantitative risk assessment of the likely transmission to man from animals of Campylobacter spp.  To give a more accurate overview of the situation and to better determine the relevance of the above observations, an international database was established to compare erythromycin resistance in Campylobacter spp. isolated from the different animal species and compare them with man to see if it could be used to assess the risk of infection transference.

Table 4. International database of Campylobacter spp. and erythromycin resistance (%)

Reference (Country)

Man

Chicken

Pig

Cattle

 

CJ

CC

CJ

CC

CJ

CC

CJ

CC

Weber et al, 1984 (G)

-

-

-

-

67

60

-

-

Bradbury & Monroe, 1985 (Can)

-

-

0

-

-

-

-

-

Aarestrup et al, 1997 (DK)

0

14

6

18

33

74

3

-

House of Lords, 1998 (UK)

2

10

-

-

-

-

-

-

Marano et al, 1999 (USA)

5

-

-

-

-

-

-

-

Mevius et al, 2000 (NL)

0

-

13

-

-

-

-

-

Saenz et al, 2000 (SP)

3

35

0

0

-

81

-

-

Kramer et al, 2000 (UK)

0

6

-

-

-

-

-

-

Danmap 2000, 2001 (DK)

2

-

5

40

-

38

0

-

Guevremont et al, 2001 (Can)

-

12

-

-

-

61

-

-

SVARM 2001, 2002 (SW)

-

-

0

0

0

1

0

-

Teale, 2002 (UK)

-

-

-

-

40