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					A Dangerous Piggyback Ride:
The Emergence of Swine-associated MRSA

          John M. Balbus, MD MPH
         American Public Health Association
          San Diego, October 25-29, 2008
               Agenda
• History of MRSA
• Clinical/Public Health import of MRSA
• Emergence of a swine MRSA strain
• Livestock-human transmission
• MRSA and agricultural antibiotic use
• What can be done
    Some numbers…
• 10.4 million • Pounds of antibiotics fed to US pigs,
                 1997
• 18,650                          • Number of US deaths from MRSA,
                                    2005

• 1961                            • Year MRSA first cultured


• 3.2                             • Pounds of bacon consumed per
                                    capita US, 1998

http://www.thepigsite.com/articles/7/markets-and-economics/1344/factors-affecting-us-pork-consumption
                                Non-Therapeutic Drug Use by Species
Estimated Total Usage in Pounds (Millions)




                                             12

                                             10
                                              8
                                                                                                      Non-HUD*
                                              6
                                                                                                      HUD*
                                              4

                                              2
                                                     95%            21%            40%
                                              0
                                                  Swine (42%)   Poultry (43%)   Cattle (15%)

                                                                                    *HUD: Human Use Drug
                                                                 Species
                                                                                          Source: UCS estimates
What is MRSA?
 • Methicillin-resistant
   Staphylococcus aureus, a
   pathogenic bacteria


 • Methicillin resistance signifies
   resistance to other clinically
   important β-lactam antibiotics
     History of resistant S. aureus
• 1940s: > 50% S. aureus resistant to penicillins
• 1960: methicillin introduced
• 1961: first MRSA strains identified
• 1967: multi-drug resistant MRSA seen
• 1993: community-acquired (CA-) MRSA identified
• 2005: MRSA reported widespread on pig farms in
  Europe


Grundmann H, et al. Emergence and resurgence of meticillin-resistant Staphylococcus aureus as a public-health
threat. Lancet 368; 2006
        Clinical significance of MRSA
• MRSA carriage common
• Frequently causes
  skin/soft tissue infections
  (93%)
• Invasive infections less
  frequent but serious


 Klevens RM, et al. Invasive Methicillin-Resistant Staphylococcus aureus Infections in the United States. JAMA 298
 (15) 2007
     Public Health Significance of MRSA

• 94,360 invasive infections and 18,650
  deaths in US in 2005
• Invasive infections: 32/100,000 persons
        – 2x greater than S. pneumoniae (14); and
        – 30x more than H. influenzae (<1)
• Longer hospitalizations, increased costs,
  and higher mortality
Klevens RM, et al. Invasive Methicillin-Resistant Staphylococcus aureus Infections in the United States. JAMA 298 (15) 2007
Cosgrove SE, et al. Comparison of mortality associated with methicillin-resistant and methicillin-susceptible Staphylococcus aureus
bacteremia: a meta-analysis. Clin Infect Dis. 36(1): 2003
                            The Netherlands:
        the beginnings of an ST398 epidemic
  • Historically low MRSA carriage (~1%)

  • Aggressive “search and destroy” policy

  • 2004 and 2005: screening found several
    ST398 cases in vets/pig farmers
        – Same strain in pigs
        – First suggestion of pig—human
          transmission
Voss A et al. Methicillin resistant Staphylococcus aureus in Pig Farming. EID 11(12); 2005.
Huijsdens XW et al. Community-acquired MRSA and pig-farming. Annals Clin Micro & Antimicro, 5(26) 2006
                   Dutch case-control study
• Elevated Odds Ratio for NT-MRSA (ST398)
     – pig farmers: 12.2 (95% CI 3.1-48.6)
     – cattle farmers 19.7 (95% CI 2.3-169.5)




van Loo I, et al. Emergence of Methicillin-Resistant Staphylococcus aureus of Animal Origin in Humans. EID 13(12): 2007
     MRSA carriage--Netherlands
• 32% (23/95) of cases NT (non-typable)
• NT-MRSA related to exposure to pigs or calves
      – OR: 327; 95% CI, 38-2514




  Typable and NT-MRSA in Amphia Hospital, Netherlands, 2002-2006

van Rijen MML, et al. Increase in a Dutch Hospital of Methicillin-Resistant Staphylococcus aureus Related to Animal
Farming. CID 46: 2008
         Prevalence of ST398 in pigs
• Dutch abattoirs: 39% (209/540)
  of pigs ST398 colonized

• All slaughterhouses (n=9), 81%
  of farms ST398(+)

• All tested isolates (n=44)
  resistant to tetracycline
  “…reflecting the high and predominant use
  of tetracyclines in pig husbandry”



  de Neeling AJ, et al. High prevalence of methicillin resistant Staphylococcus aureus in pigs. Vet Micro 122: 2007
        Pig MRSA and antibiotic use
• 23% (7/31) Dutch
  farms with ST398
  colonized pigs

• OR = 30.0 for ST398
  on farms regularly
  using antibiotics
  (95% CI: 2.8 to 322)

van Duijkeren E, et al. Transmission of methicillin-resistant Staphylococcus aureus strains between different kinds of pig
farms. Vet Micro 126: 2008
                                  Belgian Study
 • 44% (663/1500) pigs MRSA (+)—all ST398
 • 38% (48/127) pig farmers MRSA (+)—all ST398
           2 X 2 Table of MRSA carriage in pigs and humans by farm:




 • MRSA colonization of pig farmers 23-fold higher
   (37.8% vs 1.6%) than control population

Denis O, et al. Urgent Investigation into the Necessity of Modifying MRSA Prevention and Therapy Strategies in
Belgium with respect to Pig Farming. 2007
                           Antibiotic resistance of MRSA ST398 strains
                           found in Belgian pigs and pig farmers, 2007
    100
     90
     80
     70
     60
     50
     40
     30
     20
     10
       0




                                                                                                                                                                                             Cotrimoxazole
                                                                                                                                                                                                             Trimethoprim


                                                                                                                                                                                                                                           Chloramphenicol
                                                                                                                                                                                                                            Sulfonamides
                                                                                                                                                                                  Rifampin
                                                                                   Linezolid
                                                                                               Gentamicin




                                                                                                                                                                                                                                                                                        lincomycin
                           Clindamycin




                                                                                                                                                                    Minocycline
                                                                                                                         Kanamycin




                                                                                                                                                                                                                                                                            Mupirocin
                                                                   Ciprofloxacin




                                                                                                                                                                                                                                                                                                     pristinamycin
            Erythromycin




                                                                                                            Tobramycin


                                                                                                                                     Spectinomycin
                                         Tylosin




                                                                                                                                                                                                                                                             Fusidic acid
                                                                                                                                                     Tetracycline
                                                   Quinupristin-




      Pig Farmers (n = 48)                                                         Pigs (n = 663)

Adapted from: Denis O, et al. Urgent Investigation into the Necessity of Modifying MRSA Prevention and Therapy
Strategies in Belgium with respect to Pig Farming. 2007
      Risk factors: Human MRSA carriage
            on Belgian pig farms (III)




    Dose-response relationship: MRSA risk and frequency of pig contact

Denis O, et al. Urgent Investigation into the Necessity of Modifying MRSA Prevention and Therapy Strategies in Belgium
with respect to Pig Farming. 2007
      Contaminated Dutch Meat Samples
        Percent of Dutch Meat Samples with
                   MRSA Strain
               byMRSA by Strain
35%
30%
25%
20%
15%
10%
5%
0%
          Beef         Veal       Lamb  Pork Chicken Turkey  Fowl                              Game   total
                                     MRSA ST398 MRSA non-ST398

                    • Low dose: all quantified samples with < 10 cfu/g
                    • Imported and domestic meat products contaminated
                    • Unclear where contaminated: slaughterhouse or farm
      Voedsel en waren autoriteit. Prevalence of MRSA in meat, 2007. Available at:
      http://www.vwa.nl/portal/page?_pageid=119,1639827&_dad=portal&_schema=PORTAL&p_file_id=25742
  Livestock – Human MRSA transmission:
            A conceptual model
                 Animal mingling:
                      -Farms
                    -Abattoirs
                                         Veterinarians             Hospitalized
                                                                     patients
                                           Farmers
                     Pigs/
Antibiotic use       Cattle                Raw meat

                                          CAFO                        Public
                                          Air plume?                 carriage


 MRSA selection/              Animal-high risk human     High risk-general
 transmission between         MRSA transmission          public transmission
 farm animals
  Worldwide Detection of ST398




ST398 reported: Austria, Belgium, Canada, Cape Verde, China, Finland,
France, Germany, Singapore, Spain, United Kingdom, United States
          Clinical disease and ST398
• Bacteremia (Hong Kong)
• Pneumonia, PVL gene seen (China)
• Endocarditis (Netherlands)
• Ventilator-Associated Pneumonia (Germany)
• Osteomyelitis (Scotland)
• Soft tissue infections (multiple countries)
Yu F, et al. Prevalence of Staphylococcus aureus carrying Panton–Valentine leukocidin genes among isolates from
hospitalised patients in China CMI 14: 2008
                                Closer to home
• Ontario: MRSA carriage
  prevalence:
       – 45% (9/20) of farms,
       – 25% (71/285) of pigs, and
       – 20% (5/25) of pig farmers
• 59% of MRSA was ST398
• Iowa, Illinois 2008:
       – 70% of 209 swine carried ST398
       – 45% of workers in second study of
         IA farms
Khanna T, et al. Methicillin resistant Staphylococcus aureus colonization in pigs and pig farmers. Vet Micro 128: 2008
Smith T, ICEID, ASM abstracts
Surveillance : Is anyone looking?
• Europe: Well-developed (EARSS)
• US: No national MRSA surveillance—
  USDA does not test livestock
• FY09 funding for FDA-USDA to conduct
  MRSA testing
     Addressing the problem

• Establish baseline and scope
  – Conduct studies on US farms
  – Food surveillance in US
• Include MRSA in FDA risk assessments
• Eliminate non-essential uses of antibiotics in
  farm animals
  – Preservation of Antibiotics for Medical Treatment
    Act (PAMTA)

				
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