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 8g

0

14

6

18

33

74

3

-

Tylosin 64g

0

14

6

18

33

73

3

-

Enrofloxacin 2g

3

29

4

0

33

13

3

-

Tetracycline 16g

11

0

2

0

0

1

0

-

Ampicillin 32g

16

0

6

0

0

17

3

-

Gentamicin 16g

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 15g

3

35

0

0

-

81

Ciprofloxacin 5g

75

71

99

100

-

100

Tetracycline 30g

-

-

32

0

-

94

Ampicillin 10g

38

29

47

90

-

66

Gentamicin 10g

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

85

-

-

Average (%)

 

2

 

15

4

 

15

35

 

57

1

 

-

 

Assessing the risk of C. jejuni and C. coli transmission from pigs to man using erythromycin resistance as a marker:

C. jejuni:

Very few C. jejuni are isolated from the intestines of pigs, therefore the likely contamination of meat is likely to be low. Kramer et al (2000) reported on the presence of quite high levels of isolation from swine liver in a survey (34% C. jejuni and 42% C. coli) but these samples were taken from retail outlets, as both prepackaged and unwrapped items, where some cross contamination may have occurred. However as the erythromycin resistance of C. jejuni is very low in man, similar to chicken and cattle, if pig isolates were responsible the resistance to erythromycin would be much higher. Therefore the likely risk of transmission of C. jejuni from pigs to man either via meat or by environmental contamination is not evident.

C. coli:

The erythromycin resistance levels in C. coli isolated from man tend to be similar to those isolated from chicken, both 15% and in pigs at 57%. Therefore pigs are considered unlikely to have a major role if any, in the transmission of C. coli to man.

 

Discussion:

The routes of transmission of Campylobacter spp. to man have not been fully determined. Besides food transmission there is obviously a link to water and contamination of that water possibly by human waste, animal waste from farms or animal waste applied near or in water, e.g. cattle grazing fields next to water, or wild birds excreting the organism. Fallacara et al (2001) showed that a variety of wildfowl in metropolitan parks in the US were excretors of C. jejuni, Canada geese (52%), Mallard ducks (40%) and hybrids (60%). All these would increase the risk of transmission either by swimming in contaminated water or picnicking next to water. Dingle et al (2002) demonstrated that C. jejuni found in beach sand was genetically identical to isolates found in man. Barbecuing, particularly of chicken products may also be a major contributor of summer infections.

Transmission of Campylobacter spp from pigs appears to be non-evident for C. jejuni and of very low risk for C. coli and this is confirmed by Kramer et al (2001) and also by Smerdon et al (2001), where only two out of 4604 incidents of infectious intestinal disease, investigated and reported to the Public Health Laboratory Service, over an eight year period, were linked to pig meat and one of these was due to cross contamination. The species of Campylobacter involved were not recorded. Many pig meat products are further processed to ham, bacon and pate thus reducing the likely survival of Campylobacter. Genetic detailing has shown that pig and human isolates of C. jejuni are different (Newell, 2002, personal communication) but similar work on C. coli has not been completed. If the transmission of Campylobacter spp. from pigs to man either directly via pig meat or via environmental contamination is very low, so also would be the risk of transmitting antimicrobially resistant strains to man.

References:

Aarestrup, F.M., Nielsen, E.M., Madsen, M. and Engberg, J. (1997) Antimicrobial Agents and Chemotherapy, 41, 10, 2244-2250.

Bradbury, W.C. and Monroe, D.L.G. (1985) Journal of Clinical Microbiology, 22, 3, 339-346.

Centers for Disease Control and Prevention (2001) Campylobacter Infections. www.cdc.gov/ncidod/dbmd/diseaseinfo/campylobacter_t.htm

Danmap 2000 (2001) Chapter on Campylobacter. Eds. Bager, F. and Emborg, H-D., Danish Zoonosis Centre, Copenhagen, Denmark, pp. 26-28.

Dingle, K.E., Colles, F.M., Ure, R., Wagenaar, J.A., Duim, B., Bolton, F.J., Fox, A.J., Wareing, D.R.A. and Maiden, M.C.J. (2002) Emerging Infectious Diseases, 8, 9, on line www.cdc.gov/ncidod/EID/vol8no9/02-0122.htm

Fallacara, D.M., Monahan, C.M., Morishita, T.Y. and Wack, R.F. (2001) Avian Diseases, 45, 128-135.

Guevremont, E., Sirois, M. and Quessy, S. (2001) Salinpork 2001, Proceedings of the 4th International Symposium on the Epidemiology and Control of Salmonella and other Food-Borne Pathogens in Pork. 406-408.

House of Lords, Select Committee on Science and Technology (1998) Section on Campylobacter, In Resistance to Antibiotics and other Antimicrobial Agents, p. 61.

Kramer, J.M., Frost, J.A., Bolton, F.J. and Wareing, D.R.A. (2000) Journal of Food Protection, 63, 12, 1654-1659.

Mevius, D.J., Veldman, K.T., van der Giessen, A. and van Leeuwen, W.J. (2000) Tijdschrift voor Diergeneeskunde, 125, 143-146.

Saenz, Y., Zarazaga, M., Lantero, M., Gastanares, M.J., Baquero, F. and Torres, C. (2000) Antimicrobial Agents and Chemotherapy, 44, 2, 267-271.

Smerdon, W.J., Adak, G.K., OBrien, S.J., Gillespie, I.A. and Reacher, M. (2001) Communicable Disease and Public Health, 4, 4, 259-267.

SVARM 2001 (2002) Chapter on Resistance in zoonotic bacteria, National Veterinary Institute, Uppsala, Sweden, pp.14-19

Teale, C. J. (2002) The Pig Journal, 49, 52-69 (abstract)

Von Weber, A., Lembke, C. and Schafer, R. (1984) Der Praktische Tierarzt, 11, 995-998.

 

*Octagon technical papers on-line:  index

 

- top of page -

~ www.octagon-services.co.uk ~