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Peer-Reviewed Journal Tracking and Analyzing Disease Trends pages 579–768 EDITOR-IN-CHIEF D. Peter Drotman Managing Senior Editor EDITORIAL BOARD Polyxeni Potter, Atlanta, Georgia, USA Dennis Alexander, Addlestone Surrey, United Kingdom Senior Associate Editor Timothy Barrett, Atlanta, GA, USA Brian W.J. Mahy, Bury St. Edmunds, Suffolk, UK Barry J. Beaty, Ft. Collins, Colorado, USA Associate Editors Martin J. Blaser, New York, New York, USA Paul Arguin, Atlanta, Georgia, USA Christopher Braden, Atlanta, GA, USA Charles Ben Beard, Ft. Collins, Colorado, USA Carolyn Bridges, Atlanta, GA, USA Ermias Belay, Atlanta, GA, USA Arturo Casadevall, New York, New York, USA David Bell, Atlanta, Georgia, USA Kenneth C. Castro, Atlanta, Georgia, USA Corrie Brown, Athens, Georgia, USA Louisa Chapman, Atlanta, GA, USA Charles H. Calisher, Ft. Collins, Colorado, USA Thomas Cleary, Houston, Texas, USA Michel Drancourt, Marseille, France Vincent Deubel, Shanghai, China Paul V. Effl er, Perth, Australia Ed Eitzen, Washington, DC, USA David Freedman, Birmingham, AL, USA Daniel Feikin, Baltimore, MD, USA Peter Gerner-Smidt, Atlanta, GA, USA Kathleen Gensheimer, Cambridge, MA, USA Stephen Hadler, Atlanta, GA, USA Duane J. Gubler, Singapore Nina Marano, Atlanta, Georgia, USA Richard L. Guerrant, Charlottesville, Virginia, USA Martin I. Meltzer, Atlanta, Georgia, USA Scott Halstead, Arlington, Virginia, USA David Morens, Bethesda, Maryland, USA David L. Heymann, London, UK J. Glenn Morris, Gainesville, Florida, USA Charles King, Cleveland, Ohio, USA Patrice Nordmann, Paris, France Keith Klugman, Atlanta, Georgia, USA Tanja Popovic, Atlanta, Georgia, USA Takeshi Kurata, Tokyo, Japan Didier Raoult, Marseille, France S.K. Lam, Kuala Lumpur, Malaysia Pierre Rollin, Atlanta, Georgia, USA Stuart Levy, Boston, Massachusetts, USA Ronald M. Rosenberg, Fort Collins, Colorado, USA John S. MacKenzie, Perth, Australia Dixie E. Snider, Atlanta, Georgia, USA Marian McDonald, Atlanta, Georgia, USA Frank Sorvillo, Los Angeles, California, USA John E. McGowan, Jr., Atlanta, Georgia, USA David Walker, Galveston, Texas, USA Tom Marrie, Halifax, Nova Scotia, Canada David Warnock, Atlanta, Georgia, USA J. Todd Weber, Stockholm, Sweden Philip P. Mortimer, London, United Kingdom Henrik C. Wegener, Copenhagen, Denmark Fred A. Murphy, Galveston, Texas, USA Barbara E. Murray, Houston, Texas, USA Founding Editor P. Keith Murray, Geelong, Australia Joseph E. McDade, Rome, Georgia, USA Stephen M. Ostroff, Harrisburg, Pennsylvania, USA Copy Editors Karen Foster, Thomas Gryczan, Nancy Mannikko, David H. Persing, Seattle, Washington, USA Beverly Merritt, Carol Snarey, P. Lynne Stockton Richard Platt, Boston, Massachusetts, USA Gabriel Rabinovich, Buenos Aires, Argentina Production Ann Jordan, Carole Liston, Shannon O’Connor, Mario Raviglione, Geneva, Switzerland Reginald Tucker David Relman, Palo Alto, California, USA Editorial Assistant Carrie Huntington Connie Schmaljohn, Frederick, Maryland, USA Social Media Sarah Logan Gregory Tom Schwan, Hamilton, Montana, USA Ira Schwartz, Valhalla, New York, USA Tom Shinnick, Atlanta, Georgia, USA Bonnie Smoak, Bethesda, Maryland, USA Emerging Infectious Diseases is published monthly by the Centers for Disease Control and Prevention, 1600 Clifton Road, Mailstop D61, Atlanta, GA 30333, Rosemary Soave, New York, New York, USA USA. Telephone 404-639-1960, fax 404-639-1954, email [email protected]. P. Frederick Sparling, Chapel Hill, North Carolina, USA Robert Swanepoel, Johannesburg, South Africa The opinions expressed by authors contributing to this journal do not neces- sarily refl ect the opinions of the Centers for Disease Control and Prevention or Phillip Tarr, St. Louis, Missouri, USA the institutions with which the authors are affi liated. Timothy Tucker, Cape Town, South Africa All material published in Emerging Infectious Diseases is in the public do- Elaine Tuomanen, Memphis, Tennessee, USA main and may be used and reprinted without special permission; proper citation, John Ward, Atlanta, Georgia, USA however, is required. Mary E. Wilson, Cambridge, Massachusetts, USA Use of trade names is for identifi cation only and does not imply endorsement by the Public Health Service or by the U.S. Department of Health and Human Services. ∞ Emerging Infectious Diseases is printed on acid-free paper that meets the requirements of ANSI/NISO 239.48-1992 (Permanence of Paper) Emerging Infectious Diseases • www.cdc.gov/eid • Vol. 17, No. 4, April 2011 April 2011 On the Cover Hand Hygiene Campaigns, Infl uenza, Eugène-Ernest Hillemacher and Absenteeism in Schoolchildren, (1818–1887) Cairo, Egypt ................................................619 Edward Jenner Vaccinating a Boy (1884) M. Talaat et al. Oil on canvas (73.1 cm × 92.7 cm) Overall absences decreased in the intervention group. Copyright Wellcome Library, London Orthopoxvirus DNA in Eurasian Lynx, Sweden ..............................................626 About the Cover p. 763 M. Tryland et al. Synopsis This virus in lynx poses a possible threat to humans. Legionella longbeachae Genome Sequence of SG33 Strain and Legionellosis .......................................579 and Recombination between H. Whiley and R. Bentham Myxoma Viruses .........................................633 A global increase in infections is associated with soils C. Camus-Bouclainville et al. and potting mixes. The poxvirus vaccine sequence has multiple origins. Research Shedding of Pandemic (H1N1) 2009 Carriage of Streptococcus pneumoniae Virus among Health Care Personnel, 3 Years after Start of Vaccination Seattle, Washington ...................................639 Program .......................................................584 M. Kay et al. J. Spijkerman et al. Shedding may occur even after treatment. Carriage of vaccine serotype decreased, but carriage of nonserotypes increased. Complete Sequence and Molecular p. 682 Epidemiology of IncK Epidemic Plasmid Nosocomial Pandemic (H1N1) 2009, Encoding bla .....................................645 CTX-M-14 United Kingdom, 2009–2010 ......................592 J.L. Cottell et al. J.E. Enstone et al. This plasmid is disseminated worldwide in Escherichia Infections were underestimated and associated with coli isolated from humans and animals. severe illness and death. Genomic Analysis of Highly Virulent Isolate of African Swine Fever Virus.........599 H275Y Mutant Pandemic (H1N1) 2009 p. 685 D.A.G. Chapman et al. Virus in Immunocompromised Patients ...653 Sequence information will facilitate research on C. Renaud et al. vaccine development. Oseltamivir resistance emerges frequently in these patients. Diarrheagenic Pathogens in Polymicrobial Infections ............................606 B. Lindsay et al. One third of diarrheal infections were caused by Mumps Complications and Effects multiple pathogens, often in nonrandom combinations. of Mumps Vaccination, England and Wales, 2002–2006 ................................661 Bordetella petrii Infection with C.-F. Yung et al. Long-lasting Persistence in Human .........612 Vaccination can reduce the odds of more severe A. Le Coustumier et al. illness in those with mumps. Infection can persist in persons with chronic obstructive pulmonary disease. Emerging Infectious Diseases • www.cdc.gov/eid • Vol. 17, No. 4, April 2011 Coxiella burnetii from Ruminants in Q Fever Outbreak, the Netherlands ..........668 H.I.J. Roest et al. April 2011 A unique genotype, related to a human case, predominated in the dairy goat population. 726 Establishment of Vaccinia Virus Cantagalo Strain in Amazon Biome, Brazil Policy Reviews J.C. Quixabeira-Santos et al. 730 Vaccinia Virus Infections in Martial Arts Remaining Questions about Gym, Maryland, 2008 Clinical Variola Major .................................676 C.M. Hughes et al. J.M. Lane 734 Hepatitis A Virus Vaccine Escape Variants There are serious public health issues regarding this and Potential New Serotype Emergence disease. U. Pérez-Sautu et al. Should Remaining Stockpiles Another Dimension of Smallpox Virus (Variola) Be Destroyed? ............................................681 738 Edward Jenner Museum R.S. Weinstein W. Foege Relegating smallpox to the autoclave of extinction would be ill-advised. Letters p. 720 Dispatches 741 Acute Cytomegalovirus Pneumonitis in Patient with Lymphomatoid Granulomatosis 684 Parapoxvirus Infections of Red Deer, Italy A. Scagliarini et al. 742 Livestock-associated Staphylococcus aureus in Childcare Worker 688 Bacterial Meningitis and Haemophilus infl uenzae Type b Conjugate Vaccine, 744 Sequence Analysis of Feline Malawi Coronaviruses and the Circulating D.W. McCormick and E.M. Molyneux Virulent/Avirulent Theory 691 Rapid Genotyping of Swine Infl uenza 746 Effects of Vaccination against Pandemic Viruses (H1N1) 2009 among Japanese Children P.W.Y. Mak et al. 747 Pandemic (H1N1) 2009 in 3 Wildlife 695 Molecular Discrimination of Sheep Bovine Species, San Diego, California p. 759 Spongiform Encephalopathy from Scrapie 749 Hemagglutinin 222 Variants in Pandemic L. Pirisinu et al. (H1N1) 2009 Virus 699 Recent Clonal Origin of Cholera in Haiti 751 Effect of School Closure from Pandemic A. Ali et al. (H1N1) 2009, Chicago, Illinois 702 Drug-Resistant Pandemic (H1N1) 2009, 753 Imported Rabies, European Union and South Korea Switzerland, 2001–2010 S.Y. Shin et al. 754 Cytomegalovirus Viremia, Pneumonitis, 705 Seasonality of Cat-Scratch Disease, and Tocilizumab Therapy France, 1999–2009 756 Concurrent Infl uenza and Shigellosis, D. Sanguinetti-Morelli et al. Papua New Guinea, 2009 708 Characteristics of Children Hospitalized for Pandemic (H1N1) 2009, Malaysia H.I.M. Ismail et al. In Memoriam 711 Human Metapneumovirus Infection in Wild 759 In Memoriam: Frank John Fenner Mountain Gorillas (1914–2010) G. Palacios et al. 714 Highly Pathogenic Avian Infl uenza Virus About the Cover Infection in Feral Raccoons, Japan T. Horimoto et al. 763 The Fragrance of the Heifer’s Breath 718 Secondary and Tertiary Transmission of Vaccinia Virus from a US Military Service Etymologia Member 680 Variola and Vaccination G.E. Young et al. Erratum 722 High Rates of Staphylococcus aureus 758 Vol. 16, No. 12 USA400 Infection, Northern Canada G.R. Golding et al. Emerging Infectious Diseases • www.cdc.gov/eid • Vol. 17, No. 4, April 2011 Legionella longbeachae and Legionellosis Harriet Whiley and Richard Bentham Reported cases of legionellosis attributable to legionelloses typically are associated with water systems Legionella longbeachae infection have increased worldwide. in the built environment, such as cooling towers, spas, In Australia and New Zealand, L. longbeachae has been showers, and other warm water systems (1,2). Protozoa a known cause of legionellosis since the late 1980s. All play a major role in the multiplication and dissemination cases for which a source was confi rmed were associated of Legionella spp. in natural environments. The parasitism with potting mixes and composts. Unlike the situation of amoebae and ciliates is well documented, and this with other Legionella spp., L. longbeachae–contaminated parasitic capability is the basis of human disease through water systems in the built environment that cause disease infection of human lung macrophages (1,2). have not been reported. Spatially and temporally linked L. longbeachae was fi rst isolated in 1980 from a outbreaks of legionellosis associated with this organism also have not been reported. Sporadic cases of disease patient with pneumonia in Long Beach, California, USA seem to be limited to persons who have had direct contact (3). A second serogroup of L. longbeachae was discovered with potting soil or compost. Long-distance travel of the during the same year (4). Neither of these reports suggested organism resulting in infection has not been reported. These a recognized source of infection. factors indicate emergence of an agent of legionellosis that In Europe, L. pneumophila is responsible for 95% differs in etiology from other species and possibly in route of of cases of Legionnaires’ disease. Of the remaining 5%, disease transmission. the most common causative agent is L. longbeachae (5). In Australia, New Zealand, and Japan, reported cases of Legionella spp. were fi rst identifi ed as organisms L. longbeachae infection occur as often as cases of L. of public health signifi cance in 1976 and are now pneumophila infection (6–8). Within the past decade, the recognized as the causative agent of legionellosis. L. number of L. longbeachae reports has increased markedly pneumophila was the species responsible for this initial across Europe and parts of Asia (9–15). disease outbreak and has remained the major cause of legionellosis (1,2). The clinical manifestations of Potting Mixes legionellosis range from no symptoms to acute atypical L. pneumophila is primarily aquatic and endemic pneumonia and multisystem disease (2). The term to warm water in the built environment (e.g., cooling legionellosis refers collectively to the clinical syndromes towers, shower heads, and water fountains) and in natural resulting from Legionella spp. infection, i.e., Legionnaires’ environments (e.g., rivers and lakes) (1,2). It is transmitted disease (a Legionella spp.–derived pneumonic infection) from the environment through inhalation of aerosol or and Pontiac fever (an acute, self-limited febrile illness aspiration of Legionella spp.–contaminated particles (1,2). that has been linked serologically and by culture to L. longbeachae is rarely isolated from aquatic environments Legionella spp.) (1,2). Community- and hospital-acquired (16,17). The primary environmental reservoir of L. longbeachae remains unknown; however, the major source Author affi liation: Flinders University, Adelaide, South Australia, of human infection is considered to be commercial potting Australia mixes and other decomposing materials, such as bark and sawdust (5,8,18,19). No reports of L. longbeachae DOI: 10.3201/eid1704.100446 Emerging Infectious Diseases • www.cdc.gov/eid • Vol. 17, No. 4, April 2011 579 SYNOPSIS infection from water systems in the built environment have emerging trend of increasing numbers of reported L. been confi rmed. longbeachae cases (12,18). Recent analysis of the L. longbeachae genome has demonstrated that it is highly adapted to the soil Detection environment. The genome encodes for a range of proteins Detection of Legionella spp. by culture techniques is that might assist in the invasion and degradation of plant insensitive. Overgrowth of culture media with competing material (20). These enzyme systems are not present in fl ora is a major problem (1,2). This problem is heightened L. pneumophila. This work supports the hypothesis of for detection of L. longbeachae in potting mixes. Potting a possible environmental association with certain plant mixes have a high microbial load and contain spore- species (8,18). forming bacteria and fungi associated with composting. The link between potting mix and legionellosis was As a result, heat pretreatment of potting mixes tends to established in 1989 when a cluster of L. longbeachae stimulate germination of spores and rapid overgrowth of infections was detected in South Australia. Investigations the agar medium, rather than reduce competing fl ora. Acid identifi ed commercial potting mixes as the source of pretreatment is the preferred option (18). The variable nature, disease (18). Since then, L. longbeachae commonly has pH, buffering capacity, and humic content of commercial been isolated from fresh potting mixes and some of its compost and potting mixes means that the duration of acid components but less commonly from natural soils, which pretreatment is best tailored to the individual sample rather suggests that the composting process may be a catalyst than being generically applied (12,18). for growth. The heat and high moisture content during Molecular methods (quantitative PCR) have been used composting may allow for multiplication of several recently to quantitatively detect Legionella spp. in potting Legionella species to detectable levels (18). The route mixes when culture methods gave negative results (11). of transmission of L. longbeachae from contaminated Improved but nonquantifi able detection in potting soils environmental samples remains unknown (7,18). also have been reported after amoebic enrichment of soil In 1990, a study determining the incidence of samples (8). Legionella spp. in potting mix found that more than two thirds (33/45) of Australian potting mixes and none (0/19) Disease Prevalence of European potting mixes tested positive for Legionella Clinical presentations of L. longbeachae infections spp. (18). The authors postulated that the discrepancy are similar to those of other legionelloses (21). Risk between incidence of L. longbeachae infection in factors for infection in common with other Legionella Australia and the rest of the world, particularly Europe, infections are smoking, preexisting medical conditions, was attributable to the content of commercial potting mix. and immunosuppression. Gardening activities and use In Australia, potting mix is made mostly from composted of potting mixes are risk factors that are so far unique to pine waste products, such as sawdust and hammer-milled L. longbeachae infection (7). The disease predominantly bark. In Europe, peat is the main component of potting mix affects persons <50 years of age, and reports suggest the (16,18). In 2001, a similar study in Japan found that 2 of 24 median age for infection is slightly higher for L. longbeachae commercial potting mixes contained L. longbeachae. The than for L. pneumophila (2,7,16,21). In addition, fewer main component of Japanese potting mix is composted deaths tend to be associated with L. longbeachae infection wood products, particularly composted oak. The Japanese than with L. pneumophila (21). The virulence factors study also found that an amoebic enrichment of the associated with L. longbeachae clearly differ from those of potting mixes resulted in 9 of 24 potting mixes testing L. pneumophila, which may help explain the differences in positive for L. longbeachae. This fi nding demonstrated disease prevalence and severity (20). that L. longbeachae can parasitize soil protozoa and that Recently, L. longbeachae–derived Legionnaires’ it was present in potting mixes but at numbers lower than disease has increased worldwide. In the Netherlands the limit detected by using culture (8). Genomic analysis during 2000–2004, the fi rst 5 reported cases of L. subsequently confi rmed this parasitic capability (20). In longbeachae–derived pneumonia were reported (13). 2008, testing for Legionella spp. was conducted on 46 Potting mix was associated with infection when analysis commercial potting mixes in Switzerland. Two of 46 found a genotypically identical strain of L. longbeachae were culture positive for L. longbeachae and almost half in the patient’s sputum and in the potting mix. Two other (21/46) for Legionella spp. Most (41/46) of the potting patients of the 5 had indistinguishable genotypes, 1 of mixes tested positive by quantitative PCR for Legionella whom had visited the same gardening center as the index spp. Two thirds of these potting mixes contained peat as patient. Unfortunately, further analysis of the cluster was the base component. This result contradicted previous not possible because 3 of the patients died after hospital studies on European potting mixes but supported the admission (13). 580 Emerging Infectious Diseases • www.cdc.gov/eid • Vol. 17, No. 4, April 2011 L. longbeachae and Legionellosis In Thailand, a population-based survey was conducted Experimentally, both L. pneumophila and L. during 2003–2004 on 556 pneumonia patients >18 years of longbeachae infected the ciliate Tetrahymena pyriformis, age who received chest radiographs and etiologic testing. although protozoan susceptibility to infection varied This study found no positive cases of L. pneumophila and according to strain differences and available nutrients (24). 20 (5%) cases of L. longbeachae. The global increase in In addition, although in situ L. pneumophila can infect and infection rates is associated with soils and potting mixes multiply within Acanthamoeba castellanii, L. longbeachae This study did not identify an environmental source of is unable to do so (25). Recently both L. pneumophila and infection (10). In 2004, a 25-year-old woman in Spain who L. longbeachae have been shown to colonize and persist had systemic lupus erythematosus died of community- within the intestinal tracts of Caenorhabditis nematodes in acquired L. longbeachae–derived pneumonia (14). laboratory assays and soil environments. Legionella spp. During 2008–2009, Scotland recorded a cluster of replicated within the intestinal tract but did not invade Legionnaires’ disease caused by L. longbeachae. Potting surrounding tissue and were excreted as differentiated mix was associated with all 3 cases of infection. L. forms similar in structure to protozoan cysts. This study longbeachae isolates from patients and potting mix were suggested that nematodes may serve as natural hosts for genotyped by amplifi ed fragment-length polymorphism. Legionella spp. and assist in their propagation throughout The genotypes isolated from the fi rst 2 patients matched soil environments. The ability of L. longbeachae to infect the genotypes from the associated potting mixes. No isolate protozoan and metazoan hosts allows for long-term was available from the third patient, but the genotype from contamination of environmental sites (26). The ability to the potting mix matched the genotype from the fi rst patient. survive protozoan cyst formation might also explain ability The fi rst 2 patients had contact with the same brand of of L. longbeachae to endure the composting process and potting mix, which contained composted green waste (heat survive in desiccated potting mixes (16,18). treated at 65°C for 5–10 days) and 30%–50% peat that had not been heat treated. The second patient also had contact Disease Transmission with a second brand of potting mix that contained 75%– Spatially and temporally linked Legionnaires’ disease 80% peat that had not been heat treated. The third patient outbreaks associated with L. longbeachae have never been had contact with compost made from expanded wood fi ber, confi rmed. The fi rst cluster of cases detected in South coir, and bark (22). Australia was reported as seasonally but not geographically These reports contrast with previous reports of L. related (27). Seasonal clustering of cases during spring and longbeachae in Europe. In 1999, the European Working autumn has been noted in Australia and overseas (22,27). Group on Legionella Infections reported only 2 cases of L. Cases of disease typically are sporadic and statistically longbeachae from a total of 337 (<1%) reported Legionella associated with potting mix use and gardening activities spp. infections (22). In 2008, L. longbeachae was noted (28,29). The route of disease transmission remains as the dominant species among non–L. pneumophila uncertain, although close proximity or direct contact infections in Europe (23). with composts and potting mixes support hand-to-mouth, The number of reported L. longbeachae cases might aspiration, or aerosolization routes of infection (7). No not truly represent the total numbers because the infection reports have been published that detail infection associated in many patients might go undiagnosed. Standard routine with long-distance travel of L. longbeachae, which diagnostic testing for pneumonia patients involves a contrasts markedly with the considerable distances traveled legionellosis urine antigen test, which detects only L. by other Legionella spp. during disease outbreaks (2). pneumophila serogroup 1 (22). Also, many patients with A recent report detailed an outbreak of L. longbeachae Pontiac fever might not require hospitalization and might infection in a commercial nursery (28). In this instance, not be aware they have a Legionella spp. infection (1). Pontiac fever was the clinical presentation. Workers were in an enclosed facility without respiratory protection and with Survival in the Environment considerable potential for dust and aerosol generation. This The mechanisms that enable Legionella spp. to is the fi rst report of either Pontiac fever or a temporally and infect protozoa also enable opportunistic infection of the spatially confi rmed outbreak of legionellosis associated alveolar macrophages within human lungs. Legionella spp. with L. longbeachae (28). infect and multiply within protozoan hosts in the absence Reported cases of infection in Asia, Europe, and the of any other supporting nutrients (2). The relationship United States follow a similar pattern of sporadic disease between L. pneumophila and a range of protozoan hosts linked to direct exposure to potting mix and compost has been documented in detail (1,2). The relationship (9,10,13,22,29). The rarity of outbreaks of disease and between L. longbeachae and protozoan hosts is not as well prerequisite for direct exposure suggest an alternative route understood. of transmission of disease to other Legionella spp., and the Emerging Infectious Diseases • www.cdc.gov/eid • Vol. 17, No. 4, April 2011 581 SYNOPSIS literature alludes to this information (7,18). Concentrations include human health risk assessment, Legionella spp. ecology, of the organism per gram of potting mix have been reported and control and bioremediation of contaminated soils. that are comparable to those associated with Legionnaires’ disease per milliliter attributed to water systems (1,2,12). References In addition, other disease-causing legionellae are present in potting mixes (8,18). In only 1 instance has potting 1. Fields BS, Benson RF, Besser RE. Legionella and Legionnaires’ dis- mix been (inconclusively) implicated as a possible source ease: 25 years of investigation. Clin Microbiol Rev. 2002;15:506– of Legionnaires’ disease from an organism other than L. 26. DOI: 10.1128/CMR.15.3.506-526.2002 2. Bartram J, Chartier Y, Lee JV, Pond K, Surman-Lee S. Legionella longbeachae (30). Why potting mix is a source of infection and the prevention of legionellosis. Geneva: World Health Organiza- from only this species remains a mystery. tion; 2007. Currently, no strategies are available to control or 3. McKinney RM, Porschen RK, Edelstein PH, Bissett ML, Harris PP, eliminate Legionella spp. in potting mixes. Awareness Bondell SP, et al. Legionella longbeachae species nova, another eti- ologic agent of human pneumonia. Ann Intern Med. 1981;94:739– of health risks associated with handling compost and 43. potting mixes protects against disease; the precise nature 4. Bibb WF, Sorh RJ, Thomason BN, Hicklin MD, Steigerwalt AG, of this protective effect is unknown (7). In Australia, all Brenner DJ, et al. Recognition of a second serogroup of Legionella bagged potting mixes and compost carry a health warning longbeachae. J Clin Microbiol. 1981;14:674–7. 5. Joseph CA. Surveillance of Legionnaires’ disease in Europe. In: and recommendations for how to avoid infection. These Marre R, Abu Kwaik J, Bartlett C, Ciancitto NP, Fields BSs, Frosch recommendations include using a face mask, avoiding M, et al, editors. Legionella. Washington: American Society for Mi- inhalation of dust and aerosols, and washing hands after crobiology; 2002. p. 311–7. using the material (31). 6. Montanaro-Punzengruber JC, Hicks L, Meyer W, Gilbert GL. Aus- tralian isolates of Legionella longbeachae are not a clonal popula- tion. J Clin Microbiol. 1999;37:3249–54. Conclusions 7. O’Connor BA, Carman J, Eckert K, Tucker G, Givney R, Cameron L. longbeachae infections have accounted for a major S. Does using potting mix make you sick? Results from a Legionella proportion of legionelloses in Australia and New Zealand longbeachae case–control study in South Australia. Epidemiol In- fect. 2007;135:34–9. DOI: 10.1017/S095026880600656X since the late 1980s (7). Recently, the global incidence 8. Koide M, Arakaki N. Saito Atsushi. Distribution of Legionella long- of reported L. longbeachae infections has increased beachae and other legionellae in Japanese potting soils. J Infect Che- (9,23,23,28). Factors explaining this emergence of infections mother. 2001;7:224–7. DOI: 10.1007/s101560170017 are unknown but may be result in part from improved 9. Kubota M, Tomii K, Tachikawa R, Harada Y, Seo R, Kaji R, et al. Legionella longbeachae pneumonia infection from home garden soil surveillance (23). In all reports, disease transmission is [in Japanese]. Nihon Kokyuki Gakkai Zasshi. 2007;45:698–703. associated with soils, composts, and potting mixes rather 10. Phares CR, Wangroongsarb P, Chantra S, Paveenkitiporn W, Ton- than with water systems, with which other Legionella spp. della M, Benson RF, et al. Epidemiology of severe pneumonia infections are associated (7,18.27). The mechanism of L. caused by Legionella longbeachae, Mycoplasma pneumoniae, and Chlamydia pneumoniae: 1-year, population-based surveillance for longbeachae transmission remains unknown, but close severe pneumonia in Thailand. Clin Infect Dis. 2007;45:e147–55. association with contaminated material is a recurrent theme DOI: 10.1086/523003 (7). Long-distance travel of the organism and subsequent 11. Kümpers P, Tiede A, Kirschner P, Girke J. Ganser, A, Peest D. Le- infection has not been documented, which may suggest gionnaires’ disease in immunocompromised patients: a case report of Legionella longbeachae pneumonia and review of the literature. J that disease is not transmitted through aerosol inhalation Med Microbiol. 2008;57:384–7. DOI: 10.1099/jmm.0.47556-0 (7,18,27). The environmental reservoir for this Legionella 12. Casati S, Gioria-Martinoni A, Gaia V. Commercial potting soils species is yet to be identifi ed, and association with a range as an alternative infection source of Legionella pneumophila and of plant materials has been postulated (7,18,20). Isolation other Legionella species in Switzerland. Clin Microbiol Infect. 2009;15:571–5. DOI: 10.1111/j.1469-0691.2009.02742.x from peat-based potting mixes confounds this theory to 13. den Boer JW, Yzerman EPF, Jansen R, Bruin JP, Verhoef LPB, Neve some extent (12,13). Control strategies for this emerging G, et al. Legionnaires’ disease and gardening. Clin Microbiol Infect. disease are limited to published warnings on bagged 2007;13:88–91. DOI: 10.1111/j.1469-0691.2006.01562.x products relating to handling and exposure (7,22,31). 14. García C, Ugalde E, Campo AB, Miñambres E, Kovács N. Fatal case of community-acquired pneumonia caused by Legionella long- beachae in a patient with systemic lupus erythematosus. Eur J Clin Microbiol Infect Dis. 2004;23:116–8. DOI: 10.1007/s10096-003- Dr Whiley is a postgraduate student at Flinders University, 1071-7 Adelaide, South Australia, Australia. Her research focuses on 15. Diederen BM, van Zwet AA, Van der Zee A, Peeters MF. Com- the molecular detection of Legionella spp. and other opportunist munity-acquired pneumonia caused by Legionella longbeachae in intracellular pathogens in environmental systems. an immunocompromised patient. Eur J Clin Microbiol Infect Dis. 2005;24:545–8. DOI: 10.1007/s10096-005-1368-9 Dr Bentham is associate professor in public health 16. Ruehlemann SA, Crawford GR. Panic in the potting shed: the as- sociation between Legionella longbeachae serogroup 1 and potting microbiology at Flinders University. His research interests soils in Australia. Med J Aust. 1996;164:36–8. 582 Emerging Infectious Diseases • www.cdc.gov/eid • Vol. 17, No. 4, April 2011 L. longbeachae and Legionellosis 17. Saint CP, Ho LA. PCR test for the identifi cation and discrimination 25. Neumeister B, Schöniger S, Faigle M, Eichner M, Dietz K. Multi- of Legionella longbeachae serogroups 1 and 2. J Microbiol Meth- plication of different Legionella species in Mono Mac 6 cells and in ods. 1999;37:245–53. DOI: 10.1016/S0167-7012(99)00070-6 Acanthamoeba castellanii. Appl Environ Microbiol. 1997;63:1219– 18. Steele TW, Lanser J, Sangster N. isolation of Legionella long- 24. beachae serogroup 1 from potting mixes. Appl Environ Microbiol. 26. Brassinga AK, Kinchen JM, Cupp ME, Day SR, Hoffman PS, Sifri 1990;56:49–53. CD. Caenorhabditis is a metazoan host for Legionella. Cell Micro- 19. Doyle RM, Cianciotto NP, Banvi S, Manning PA, Heuzenroeder biol. 2010;12:343–61. DOI: 10.1111/j.1462-5822.2009.01398.x MW. 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Legionnaires’ disease due 29. Centers for Disease Control and Prevention. Legionnaires’ disease to Legionella longbeachae and Legionella pneumophila: compari- associated with potting soil—California, Oregon, and Washington, son of clinical features, host-related risk factors and outcomes. Clin May–June 2000. MMWR Morb Mortal Wkly Rep. 2000;49:771–8. Microbiol Infect. 2009; [Epub ahead of print]. DOI: 10.1111/j.1469- 30. Wallis L, Robinson P. Soil as a source of Legionella pneumophi- 0691.2009.02920.x la serogroup 1. Aust N Z J Public Health. 2005;29:518–20. DOI: 22. Pravinkumar SJ, Edwards G, Lindsay D, Redmond S, Stirling J, 10.1111/j.1467-842X.2005.tb00242.x House R, et al. A cluster of Legionnaires’ disease caused by Legi- 31. Australian Standard 4454-2003. Composts, potting mixes and onella longbeachae linked to potting compost in Scotland, 2008– mulches. 3rd ed. Sydney (NSW, Australia): Standards Australia In- 2009. Euro Surveill. 2010;15:19496. ternational Ltd.; 2003. 23. Joseph CA, Ricketts KD; European Working Group for Legionella Infections. Legionnaires’ disease in Europe 2007–2008. Euro Sur- Address for correspondence: Richard Bentham, School of the veill. 2010;15:19493. Environment, Environmental Health, Flinders University, PO Box 2100, 24. Steele TW, McLennan AM. Infection of Tetrahymena pyriformis by Legionella longbeachae and other Legionella species found in pot- Adelaide, SA 5001, Australia; email: richard.bentham@fl inders.edu.au ting mixes. Appl Environ Microbiol. 1996;62:1081–3. Emerging Infectious Diseases • www.cdc.gov/eid • Vol. 17, No. 4, April 2011 583 RESEARCH Carriage of Streptococcus pneumoniae 3 Years after Start of Vaccination Program, the Netherlands Judith Spijkerman, Elske J.M. van Gils, Reinier H. Veenhoven, Eelko Hak, Ed P.F. Yzerman, Arie van der Ende, Alienke J. Wijmenga-Monsuur, Germie P.J.M. van den Dobbelsteen, and Elisabeth A.M. Sanders To evaluate the effectiveness of the 7-valent persons (1). All pneumococcal disease is preceded by pneumococcal conjugate vaccine (PCV7) program, we nasopharyngeal colonization (2). To date, slightly >90 conducted a cross-sectional observational study on serotypes have been identifi ed. Young children, among nasopharyngeal carriage of Streptococcus pneumoniae whom nasopharyngeal carriage rates are highest, are the 3 years after implementation of the program in the main reservoir for pneumococcal spread in families and the Netherlands. We compared pneumococcal serotypes in community (3). 329 prebooster 11-month-old children, 330 fully vaccinated In the United States and other industrialized 24-month-old children, and 324 parents with age-matched countries, widespread use of the 7-valent pneumococcal pre-PCV7 (unvaccinated) controls (ages 12 and 24 months, conjugate vaccine (PCV7) (Prevenar; Pfi zer, New York, n = 319 and n = 321, respectively) and 296 of their parents. PCV7 serotype prevalences before and after PCV7 NY, USA) for children has led to a dramatic decline implementation, respectively, were 38% and 8% among in PCV7-serotype invasive pneumococcal disease 11-month-old children, 36% and 4% among 24-month- (IPD), not only in vaccinated children (4) but also in old children, and 8% and 1% among parents. Non-PCV7 unvaccinated persons of all ages (5,6). This indirect serotype prevalences were 29% and 39% among 11-month- effect has substantially contributed to favorable cost- old children, 30% and 45% among 24-month-old children, effectiveness estimates of the vaccination program (7,8). and 8% and 15% among parents, respectively; serotypes However, shifts toward nasopharyngeal carriage of non- 11A and 19A were most frequently isolated. PCV7 PCV7 serotypes may eventually counterbalance the direct serotypes were largely replaced by non-PCV7 serotypes. and indirect benefi ts of the vaccine, assuming that non- Disappearance of PCV7 serotypes in parents suggests PCV7 serotypes will display similar disease potential strong transmission reduction through vaccination. (9–12). Early evaluation of the effect of pneumococcal vaccination on serotype distribution in disease is hampered Streptococcus pneumoniae (pneumococcus) is a major by the relative infrequency of IPD and the diffi culty of cause of respiratory and invasive disease worldwide, identifying causative agents in respiratory diseases such particularly in children <5 years of age and elderly as pneumonia or in otitis media. Therefore, surveillance of nasopharyngeal carriage of pneumococci in vaccinated Author affi liations: University Medical Center, Utrecht, the and in unvaccinated persons provides another useful Netherlands (J. Spijkerman, E.J.M. van Gils, E.A.M. Sanders); tool for monitoring how vaccination affects circulating Spaarne Hospital, Hoofddorp, the Netherlands (J. Spijkerman, pneumococcal serotypes. E.J.M. van Gils, R.H. Veenhoven); University Medical Center, In the Netherlands, as part of the national immunization Groningen, the Netherlands (E. Hak); Regional Laboratory of Public program (NIP), vaccination with PCV7 was introduced for Health, Haarlem, the Netherlands (E.P.F. Yzerman); Academic all infants born after March 31, 2006, in a 3+1 schedule Medical Center, Amsterdam, the Netherlands (A. van der Ende); of vaccinations at 2, 3, 4, and 11 months with no catch- and Netherlands Vaccine Institute, Bilthoven, the Netherlands (A.J. up campaign. To evaluate how this PCV7 vaccination Wijmenga-Monsuur, G.P.J.M. van den Dobbelsteen) program affected prevalence of pneumococcal serotypes after 3 years, we conducted a cross-sectional observational DOI: 10.3201/eid1704101115 584 Emerging Infectious Diseases • www.cdc.gov/eid • Vol. 17, No. 4, April 2011

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