Zoonotic disease pathogens in fish used for pedicure.
A survey during the spring of 2011 identified 279 fish spas in the United Kingdom, and the number has probably increased since then (1). The Fish Health Inspectorate of the Centre for Environment, Fisheries & Aquaculture Science estimates that each week 15,000-20,000 G. rufa fish are imported from Indonesia and other countries in Asia into the United Kingdom through London Heathrow Airport (the main border inspection post for the import of live fish). However, ichthyotherapy has now reportedly been banned in several US states and Canada provinces because of sanitary concerns (1). In the United Kingdom, a limited number of infections after fish pedicures have been reported (1). Unfortunately, little is known about the types of bacteria and other potential pathogens that might be carried by these fish and the potential risks that they might pose to customers or to ornamental and native fish.
On April 12, 2011, the Fish Heath Inspectorate investigated a report of a disease outbreak among 6,000 G. rufa fish from Indonesia that had been supplied to UK pedicure spas. Affected fish showed clinical signs of exophthalmia and of hemorrhage around the gills, mouth, and abdomen. More than 95% of the fish died before the remaining fish were euthanized. Histopathologic examinations identified systemic bacterial infections with small gram-positive cocci, mostly in the kidneys, spleen, and liver. Bacterial isolates cultured from affected fish were identified as Streptococcus agalactiae (group B Streptococcus) according to a combination of biochemical test results (API Strep; bioMerieux, Marcy l'Etoile, France), Lancefield grouping with serotype B (Oxoid Limited, Basingstoke, UK), and molecular (partial 16S rRNA gene sequencing) testing methods.
Multilocus sequence typing of a representative isolate (11013; online Technical Appendix Table) (2) indicated that it was a sequence type (ST) 261 S. agalactiae strain (http:// pubmlst.org/sagalactiae). This same ST261 profile was first identified in an isolate (ATCC 51487) from a diseased tilapia in Israel (3). The clinical appearance of the disease and the diagnostic results suggested that S. agalactiae was the causative agent of the fish illness and deaths.
To determine whether S. agalactiae and other bacterial pathogens might be carried more widely by these fish, from May 5, 2011, through June 30, 2011, the Fish Health Inspectorate of the Centre for Environment, Fisheries & Aquaculture Science visited Heathrow Airport 5 times to intercept and sample consignments of G. rufa from Indonesia. A taxonomically diverse range of bacteria were identified (online Technical Appendix Table, Figure 2), including a variety of human pathogens capable of causing invasive soft tissue infections. These pathogens included Aeromonas spp. (4), potentially pathogenic clinical-type Vibrio vulnificus isolates (online Technical Appendix Figure 2) (5), non-serotype O1 or O139 cholera toxin-negative V. cholerae isolates (online Technical Appendix Figure 2) (6), Mycobacteria (7), and S. agalactiae (3,8). Isolates were resistant to a variety of antimicrobial drugs, including tetracyclines, fluoroquinolones, and aminoglycosides (online Technical Appendix Table). Other studies have also reported high levels of multidrug resistance in bacteria associated with imported ornamental fish (9).
Water is a well-recognized source of bacterial skin infections in humans. V. vulnificus can cause wound infections and primary septicemia, resulting in high mortality rates, especially among persons with predisposing risk conditions (e.g., liver disease, diabetes, or impaired immune function) (5). S. agalactiae is a common cause of skin and soft tissue infections, especially in older adults and those with chronic diseases such as diabetes mellitus (8). Although S. agalactiae ST261 is not considered to be one of the genotypes typically associated with invasive disease in humans (3), a fish-adapted strain could eventually take advantage of the opportunity afforded by repeated exposure and thereby also affect humans. Additionally, Mycobacteria spp. can occasionally cause disease in humans through contact with fish (M. marinum), and pedicure treatments have previously been associated with M. fortuitum infections (10).
Recently, the risks associated with exposure to G. rufa fish were reported to be low (1). To date, there are only a limited number of reports of patients who might have been infected by this exposure route (1). However, our study raises some concerns over the extent that these fish, or their transport water, might harbor potential zoonotic disease pathogens of clinical relevance. In particular, patients with underlying conditions (such as diabetes mellitus or immunosuppression) should be discouraged from undertaking such treatments, especially if they have obvious breaks in the skin or abrasions. This risk can probably be reduced by use of certified disease-free fish reared in controlled facilities under high standards of husbandry and welfare.
The UK Department for Environment Food and Rural Affairs provided funding for this study through projects FA001 and FB002.
David W. Verner-Jeffreys, Craig Baker-Austin, Michelle J. Pond, Georgina S. E. Rimmer, Rose Kerr, David Stone, Rachael Griffin, Peter White, Nicholas Stinton, Kevin Denham, James Leigh, Nicola Jones, Matthew Longshaw, and Stephen W. Feist
Author affiliations: Centre for Environment, Fisheries & Aquaculture Science Weymouth Laboratory, Weymouth, UK (D.W. Verner-Jeffreys, C. Baker-Austin, M.J. Pond, G.S.E. Rimmer, R. Kerr, D. Stone, R. Griffin, P. White, N. Stinton, K. Denham, M. Longshaw, S.W. Feist); University of Nottingham, Sutton Bonington, UK (J. Leigh); and Oxford Radcliffe University Hospitals, Headington, UK (N. Jones)
(1.) Health Protection Agency Fish Spa Working Group. Guidance on the management of the public health risks from fish pedicures: draft for consultation. 2011 Aug 31 [cited 2012 Mar 21]. http:// www.hpa.org.uk/webc/HPAwebFile/ HPAwebC/1317131045549
(2.) Jones N, Bohnsack JF, Takahashi S, Oliver KA, Chan MS, Kunst F, et al. Multilocus sequence typing system for group B Streptococcus. J Clin Microbiol. 2003;41:2530-6. http://dx.doi. org/10.1128/JCM.41.6.2530-2536.2003
(3.) Evans JJ, Bohnsack JF, Klesius PH, Whiting AA, Garcia JC, Shoemaker CA, et al. Phylogenetic relationships among Streptococcus agalactiae isolated from piscine, dolphin, bovine and human sources: a dolphin and piscine lineage associated with a fish epidemic in Kuwait is also associated with human neonatal infections in Japan. J Med Microbiol. 2008;57:1369-76. http:// dx.doi.org/10.1099/jmm.0.47815-0
(4.) Janda JM, Abbott SL. The genus Aeromonas: taxonomy, pathogenicity, and infection. Clin Microbiol Rev. 2010;23:35-73. http://dx.doi.org/10.1128/CMR.00039-09
(5.) Jones MK. Oliver, JD. Vibrio vulnificus: disease and pathogenesis. Infect Im mun. 2009;77:1723-33. http://dx.doi. org/10.1128/IAI.01046-08
(6.) Morris JG. Non-O group-1 Vibrio cholera--a look at the epidemiology of an occasional pathogen. Epidemiol Rev. 1990;12:179-91.
(7.) Wagner D, Young LS. Nontuberculous mycobacterial infections: a clinical review. Infection. 2004;32:257-70. http:// dx.doi.org/10.1007/s15010-004-4001-4
(8.) Skoff TH, Farley MM, Petit S, Craig AS, Schaffner W, Gershman K, et al. Increasing burden of invasive group B streptococcal disease in non-pregnant adults, 1990-2007. Clin Infect Dis. 2009;49:8592. http://dx.doi.org/10.1086/599369
(9.) Verner-Jeffreys DW, Welch TJ, Schwarz T, Pond MJ, Woodward MJ, Haig SJ, et al. High prevalence of multidrug-tolerant bacteria and associated antimicrobial resistance genes isolated from ornamental fish and their carriage water. PLoS ONE. 2009;4:e8388. http://dx.doi.org/10.1371/ journal.pone.0008388
(10.) De Groote MA, Huitt G. Infections due to rapidly growing mycobacteria. Clin Infect Dis. 2006;42:1756-63. http://dx.doi. org/10.1086/504381
Address for correspondence: David W. Verner-Jeffreys, Cefas Weymouth Laboratory, The Nothe, Barrack Rd, Weymouth, Dorset DT4 8UB, UK; email: firstname.lastname@example.org
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|Author:||Verner-Jeffreys, David W.; Baker-Austin, Craig; Pond, Michelle J.; Rimmer, Georgina S.E.; Kerr, Rose|
|Publication:||Emerging Infectious Diseases|
|Article Type:||Letter to the editor|
|Date:||Jun 1, 2012|
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