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Infections from leisure-time activities
Microbes and Infection, 3, 2001, 509−514 © 2001 Éditions scientifiques et médicales Elsevier SAS. All rights reserved S128645790101406X/REV
Review
Infections from leisure-time activities David Schlossberg* Medical Services, Merck & Co., Inc., West Point, PA 19486, USA
ABSTRACT – Leisure-time activities expose us to a variety of infections. The traveler confronts new pathogens and vectors. Camping, hiking and gardening have attendant risks, as does exposure to fresh and salt water. Adventuresome eating poses gastronomic threats, and pets, sexual exposure and organized sports each contribute distinctive infectious risks to participants. © 2001 Éditions scientifiques et médicales Elsevier SAS infection / leisure / travel
1. Introduction Developed society tends to increase its leisure time. We swim, hike, garden, travel abroad, pamper our pets, engage in sports and eat adventurously. Often, in our abandon in these playful pursuits we ignore their risks. But perils exist, and many infectious diseases can result from our leisuretime activities. This review discusses the most common types of leisure activities, identifying in each instance the attendant risks of infection that may spoil the fun.
2. Travel We all love to travel, but infectious risks abound. A rich historical lore accompanies the infectious risks of travel. Such dangers were well-known to invading armies: for example, when Napoleon invaded Russia in 1812, he lost tens of thousands of troops to typhus before encountering any enemy fusillades. The ease of foreign travel and the millions of potential patients who cross international borders daily, require increasing consideration of both local and exotic infections. The infectious considerations regarding travel may be divided into pre-travel and post-travel categories. Thus, prior to foreign travel, a general medical kit should be assembled; the infectious disease concerns of the kit center around an antimicrobial agent for turista, (e.g., ciprofloxacin), anti-malarial prophylaxis, and insect repellants. Immunizations must supplement routine childhood protection with consideration of vaccines for yellow fever, cholera, hepatitis A and hepatitis B, influenza, pneumococcal infection, meningococcal infection, Japanese encephalitis virus, plague, rabies and typhoid fever. Deci*Correspondence and reprints. E-mail address: [email protected] (D. Schlossberg). Microbes and Infection 2001, 509-514
sions regarding individual vaccines vary with projected behavior and destination, and current recommendations may be sought at the Centers for Disease Control and Prevention in Atlanta, Georgia [1]. Upon return, the traveler may present to his physician with a variety of syndromes, and the differential diagnosis will depend on clues from the patient’s areas of travel and activities. Thus, gastroenteritis raises the possibility of bacterial infection (Salmonella, Shigella, Campylobacter, Aeromonas, Yersinia, Vibrio), toxin-induced illness (due to Escherichia coli, Clostridium difficile, fish and shellfish poisoning), or viral infection (Rotavirus and Norwalk). Longer incubation periods and prolonged symptoms frequently suggest parasitosis due to Entamoeba, Giardia, Dientamoeba, Cryptosporidium, Isospora, Microsporidia or Cyclospora. There are geographic clues that may help in differential diagnosis, for example, the association of giardiasis with St Petersburg (the ’Trotskys’), Aeromonas with Thailand, Shigella with Mexico, and Cyclospora with Nepal [2]. Rash and fever in the returning traveler suggest rickettsial infection, viral infection with HIV or dengue, syphilis and typhoid fever. It has recently been appreciated that HIV patients returning from southeast Asia may develop disseminated infection with Penicillium marneffei and present with fever and a papular rash. Some returning travelers manifest eosinophilia as part of their illness. These patients should be evaluated for intestinal parasites such as roundworm, pinworm, whipworm and, especially in AIDS, strongyloides. With the appropriate geography, schistosomiasis and filariasis (both loa loa and onchocerciasis) may explain the combination of fever and eosinophilia. At times, fever alone (without specific localizing symptomatology) is the presenting complaint. These patients often have hepatitis A, amoebic liver abscess, early tick typhus, malaria or salmonellosis, but less common causes 509
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of this presentation require consideration of brucellosis, tuberculosis, early HIV, leishmaniasis, and trypanosomiasis [2]. The WHO reports that yellow fever transmission is on the increase, especially in travelers from the United States to South America and Africa, so a presentation of hepatitis is not always due to the more common hepatotropic viruses. [3]. Sometimes the pattern of fever can provide a clinical clue; thus, relapsing fever suggests brucellosis and borreliosis, while persistent fever is more characteristic of typhoid; dengue often displays a characteristic saddleback pattern. Double quotidien fevers may accompany kala-azar. Malaria classically relapses, but its fevers at times are misleadingly hectic, with multiple daily spikes, either early in the course prior to synchronization, or because of infection with more than one plasmodium species. Skin lesions in the returning traveler can appear to be non-healing ’boils’ that are actually due to myiasis (from the Botfly or the Tumbu fly), linear patterns suggestive of cutaneous larva migrans, and ulcerations from leishmaniasis, diphtheria or syphilis. Some patients develop pneumonia after travel, and most of the time the etiology is not exotic; but when it is, unusual causes of fever and pulmonary infiltrate should be considered, including malaria, plague, melioidosis, helminthic migration, and paraccocidoidomycosis. Tuberculosis appears to represent a significant risk to children who travel to high-risk countries, particularly Mexico, Central America and China, and some advocate testing children routinely upon return from visiting high-risk foci. Tuberculosis can apparently be acquired on an airplane if an infectious passenger coughs enough during a prolonged flight. However, an occasional patient returns from a long flight with fever, cough, and pulmonary infiltrate but is found to have not infection but pulmonary embolization from prolonged sitting; this has been nicknamed the ‘economy class syndrome’. It is not always the human passengers that bring disease from a travel destination; Vectors such as tsetse flies, sandflies and mosquitoes may hitch a ride in the luggage hold or passenger compartment of an airplane, causing infection in patients who live near the airport. Between 1969 and 1999, 87 cases of ‘airport malaria’ were documented in 12 different countries [4]. Conveyances other than airplanes can contribute to travel-related infection: cruise ships have been sources of food-borne illness and respiratory infections, including influenza; it has been pointed out that cruise ships present infection control challenges similar to those in hospitals and nursing homes; in addition, the average cruise length is 6 days, during which time many infections can be incubated, transmitted, and dispersed to multiple passengers with varied destinations [5]. Screening patients after foreign travel, especially to the tropics, need not be routine, but should be undertaken after long-term residence and should include CBC, urinalysis, liver function tests, hepatitis B virus, HIV, serology for shistosomiasis (when appropriate) and stool examination for ova and parasites [2]. Even after short-term travel, screening children with purified protein derivative may be advisable, as noted above [6]. 510
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3. Camping and hiking Camping and hiking are popular activities in many countries, in patients of all ages. These outdoor activities expose adherents to a variety of arthropods, which torment humans by stings, bites, envenomation and hypersensitivity; in addition, they are also efficient vectors of infection. Although many of the arthropods are found worldwide, the illnesses they spread reflect their geography. Thus, location alone may dictate whether a tick spreads Colorado tick fever, Powasson encephalititis, Crimean-Congo hemorrhagic fever, central European encephalitis, ehrlichiosis, Lyme disease, Q Fever, borreliosis, babesiosis or tularemia. Clearly, physicians must know the patterns of tick-borne illness in areas their patients live in, or visit. Rickettsial infections spread by ticks include the well-known illnesses Rocky Mountain spotted fever and Israeli spotted fever (tick typhus), but a number of Rickettsiae have been described only recently, including R. africae, R. japonica, R. felis, R. mongolotimonae and R. slovaca. Ticks do not always cause disease by transmitting infection; tick paralysis, caused by over 60 species of ticks worldwide, may mimic such classic infectious syndromes as polio, botulism, Guillain-Barre syndrome and infectious myelitis [7]. Animal-associated mites spread encephalitis, murine typhus and rickettsialpox, and mosquitoes, of course, carry malaria, dengue, yellow fever and encephalitis. True flies carry classic scourges of mankind such as loiasis and tularemia (deer fly), onchocerciasis (black fly), trypanosomiasis (tsetse fly) and leishmaniasis, bartonellosis and sand fly fever (sand fly). Even the lowly flea commands respect for its ability to transmit murine typhus and one of mankind’s oldest enemies, plague. In addition to arthropods, campers and hikers risk infection from giardia when drinking from sparkling mountain streams and histoplasmosis if they explore bat caves or inhale the fungus from soil contaminated with the droppings of starlings, blackbirds, pigeons or chickens. Some campers purify their drinking water with iodine-containing preparations; on occasion this practice has resulted in transient thyrotoxicosis following a backpacking adventure (’travelers’ thyrotoxicosis’). As the clinical presentation of thyrotoxicosis can mimic systemic infection, with fever, sweats and weight loss, such patients should be questioned carefully about exposure to or ingestion of iodine [8].
4. Gardening Gardening enthusiasts are at risk from cutaneous lacerations from plants and gardening tools, and may contract infections from pathogens classically associated with soil and plants. Thus, a syndrome of cutaneous nodular lymphangitis in a gardener, particularly a rose fancier, most commonly results from sporotrichosis, but may also follow inoculation with Nocardia and rapidly growing Mycobacteria [9]. These lymphocutaneous syndromes may be mistaken for bacterial/pyogenic infections if the association with soil and plant exposure is not recognized. Microbes and Infection 2001, 509-514
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Respiratory and even systemic disease from histoplasmosis and blastomycosis can result from inhaling these organisms from the soil, and barefoot gardeners risk strongyloidiasis and hookworm infestation from larval penetration of their unprotected feet.
5. The sea Most of the earth is water, and we delight in visiting the ocean and its shores. However, a variety of infections can tarnish this pleasure. Localized infection with Mycobacterium marinum and Erysipelothrix may complicate minor abrasions of the skin; much more invasive soft-tissue infection due to vibrios (especially V. vulnificus and V. damsela) may require extensive debridement and could progress to septicemia in immunosupressed patients or those with liver disease. A pruritic rash within hours of swimming indicates schistosome dermatitis or ’swimmer’s itch’; this eruption follows penetration of the swimmer’s skin with nonhuman schistosomal cercariae, and blossoms on areas of exposed skin. In contrast, seabather’s eruption, from the nematocysts of coelenterate larvae trapped underneath swimwear, occurs on the skin that was covered by bathing suits. While swimmer’s itch occurs in fresh as well as salt water, seabather’s eruption is seen only after exposure to salt water. Swimmer’s ear, an external otitis following water exposure, may be extremely painful and require antimicrobial and anti-inflammatory therapy. Even a moonlight stroll along the beach can be threatening: the dinoflagellates or plankton that cause discoloration of the water (blooms, or red tide) may on occasion be aerosolized by the pounding surf and cause neurologic and respiratory symptoms by their inhalation. Dinoflagellates producing brevetoxin have done this, as have pfisteria, which causes mysterious neurologic illnesses including memory loss [10].
6. Freshwater Freshwater has its own attendant risks. A papular dermatitis due to Pseudomonas may follow immersion in a pool, hot tub, spa or water slide. Soft tissue trauma allows introduction of Aeromonas, which can cause invasive cellulitis. Less invasive skin pathogens, causing indolent nodular or ulcerative lesions, include M. marinum and Prototheca. Swimming pool conjunctivitis follows exposure to water-borne adenovirus, while a potentially more destructive keratitis may indicate amoebic infection. Victims of near-drowning are at risk from pneumonia due to Legionella (which is found even in thermal ponds), as well as Aeromonas, Buckholderia, Pseudallescheria and Chromobacterium violaceum, the last species often associated with skin and liver lesions [11]. Encephalitis after fresh water exposure, especially after diving, requires consideration of amoebic central nervous system infection due to Naegleria fowleri, while a more benign ’aseptic’ meningitis under these circumstances is a common manifestation of leptospirosis, having contaminated the water from the urine of an infected animal. Microbes and Infection 2001, 509-514
Review
7. Food Food is a common source of leisure-related infections. Often resembling gastroenteritis with associated neurologic phenomena, fish and shellfish poisoning results most often from dinoflagellates in the marine food chain. When they bloom, these organisms can turn the water red. This phenomenon probably explains the appearance of bloody water and subsequent morbidity and mortality noted even in biblical times [12]. As noted earlier, the concentration may be great enough to cause symptoms even without ingestion, from aerosolization in the surf. When ingested, however, syndromes from eating shellfish contaminated with these dinoflagellates may be paralytic, neurotoxic, amnesic and diarrheic, depending on the particular toxin present. Ciguatera fish poisoning presents as gastroenteritis with a varying array of neurologic phenomena; it results from eating large reef fishes that have ingested these toxin-producing dinoflagellates. Alternatively, fish poisoning may result from a histamine reaction from the bacterial decomposition of fish (scombroid) or from the tetrodotoxin in puffer fish (Fugu in Japan) that produces dramatic neurologic symptoms, including respiratory paralysis, and carries a 60% mortality rate [13]. All these toxins are heat stable, so that cooking does not protect the adventuresome diner. An interesting syndrome described in Europe and the USA is Haff disease [14], in which buffalo fish consumption causes rhabdomyolysis due to a heat-stable toxin. This illness differs from most other seafood-related disease in that it is spread by a freshwater fish and, unlike other fish-related toxic illnesses, has no neurologic features. Contaminated shellfish can spread infection due to the Norwalk virus and hepatitis A virus. Many regional foods (e.g., sushi, ceviche) that are served raw, pickled, steeped in lime juice, soaked in alcohol, salted, smoked or buried, are still able to transmit infection [15]. Even cooking or microwaving is frequently inadequate. Thus, anisakiasis, from ocean fish, causes severe immediate abdominal pain, relieved when the worm is removed endoscopically. Freshwater fish carry, among other parasites, Diphyllobothrium latum, Eustrongylides and Gnathostoma; infection with Gnathostoma results in larvae migrating through the host, causing migratory swellings in addition to abdominal pain, cough and eosinophilic meningitis. Of course, cholera is the prototypical bacterial infection resulting from eating raw seafood. Raw beef and pork spread Taenia saginata and T. solium, respectively. A recent outbreak of cysticerciasis in members of an orthodox community in New York [16] was spread by infected housekeepers from Latin America who had taeniasis and shed eggs in their stools. Trichinosis is acquired from undercooked pork as well as bear and wild boar. Thorough cooking of these meats results in a dark gray coloration of the dish, but many diners prefer their meat on the pink side. However, as the late Dr Louis Weinstein would say, “a little pink, a little trichinosis”. Poorly cooked hamburger has caused multiple outbreaks of hemorrhagic colitis due to E. coli O157:H7, with complications of hemolytic uremic syndrome and thrombotic thrombocytopenic purpura. Toxoplasmosis results 511
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from eating rare beef and other meats, such as lamb in kibbee; and unpasteurized milk and cheese (ever more popular among the health-food conscious) carry Listeria, Salmonella, Campylobacter and Yersinia.
8. Animals Much leisure activity is lavished on animals, whether as pets or encountered in the course of other pursuits. Man’s best friend, the dog, has transmitted many infections to its owners, from rabies to a panoply of cutaneous, gastrointestinal and systemic illnesses. Cellulitis from Pasteurella multocida may complicate a dog bite, and this organism can become invasive, especially in hosts compromised by liver disease, extremes of age and pregnancy. Capnocytophaga canimorsus may also complicate dog bites, and this organism is prone to cause devastating complications in patients compromised by splenectomy or alcoholism. Salmonella and Campylobacter may infect the gastrointestinal tract of dogs (especially puppies) which then spread the infection to their owners. Leptospirosis is spread through dogs’ urine, and can be excreted many months after the animal is no longer symptomatic from its infection. Parasitic infections spread by this favorite pet include cryptosporidiosis, isospora, dirofilaria, visceral larva migrans, creeping eruption, echinococcus, and dypilidium. Dermatologic infestation results from dogs’ mites (cheyletiellosis, canine scabies), fleas, and fungal dermatophytes. Cats are associated with a variety of infections. Bartonella (formerly Rochalimaea) henselae is now known to be associated with cats, in whom it frequently causes prolonged and asymptomatic bacteremia. Transmission of B. henselae from cats to man probably occurs via cat fleas. In humans, B. henselae is the cause of cat scratch disease and is a cause of bacillary angiomatosis and parenchymal peliosis in immunocompromised patients, particularly those with AIDS. Fecal–oral transmission from cat to man may result in infection with the bacterial pathogens Campylobacter and Salmonella and a variety of parasites, particularly Cryptosporidium, Toxoplasma and Toxocara. Such classic illnesses as plague, tularemia and a pertussislike syndrome caused by Bordetella bronchiseptica may be acquired from cats, and cat bites, like dog bites, are known to predispose to infection with Pasteurella multocida. Unlike dog bites, however, the cat’s bite wound is more likely to result in osteomyelitis or septic arthritis, especially when the injury involves soft tissues closely overlying bones and joints. This predisposition results from the cats’ teeth, which are sharp and narrow and essentially inject the organisms deeply into a wound. Cats also spread Q Fever, caused by Coxiella burnetii, especially after exposure to parturient cats or their aborted tissue. Birds are favorite pets, but they, too, place their owners at risk. Psittacosis, caused by Chlamydia psittaci, was once thought to result only from exposure to psittacine birds. However, it is now appreciated that this organism may infect most, if not all, avian species and the disease is more 512
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accurately called ornithosis. Birds do not have to appear ill to transmit psittacosis, as they may shed the organism long after their acute illness has abated. Also, the exposure to infected birds may be trivial; although some devotees (and subsequent patients) have been known to kiss their parrots, other victims of ornithosis have merely visited public bird parks. Bird exposure also places man at risk from infection with mosquito-borne arboviruses, Cryptococcus and Histoplasma (from contaminated soil) and, following recent observations in Hong Kong, possibly influenza. Man and rodents have shared an ancient infectious relationship. Different types of rodents tend to be associated with specific infections. Thus, lymphocytic choriomeningitis (LCM) is commonly associated with hamsters; plague, yersiniosis and salmonellosis with guinea pigs; murine typhus and rat bite fevers with rats; and plague with prairie dogs in the southwest US. Mice have shown the ability to spread LCM, rickettsialpox and Salmonella, and most recently the Hantavirus pulmonary syndrome (HPS) has been associated with mouse exposure. HPS is a severe cardiopulmonay illness with 40–60% mortality, seen in North and South America and recently in Central America [17]. A systemic or gastrointestinal infection in a patient with reptile exposure should raise the suspicion of salmonellosis. This is most commonly associated with pet turtles, but is also seen with iguanas and other lizards, snakes, and the Komodo dragon [18] (figure 1). Severe respiratory illness in patients exposed to elephants raises the possibility of TB, which has been transmitted from a zoo elephant to its handlers. Monkeys have been associated with Salmonella, Shigella, TB, herpes B and hepatitis A infection. Finally, fish exposure poses certain infectious risks. Aquariumassociated skin lesions are often due to M. marinum, while non-aquarium fish exposures commonly cause cellulitis or more invasive infections due to Erysipelothrix. A recent outbreak of Streptococcus iniae cellulitis was traced to contamination of Tilapia fish with this organism; the organism was transmitted only to the Asian customers of a fish market who bought the fish live and apparently inoculated themselves from the fish’s spines and bones during preparation. Other customers bought the fish after it had been scaled and cleaned and the appendages removed, presumably thereby reducing the potential for infection [19].
9. Sporting activities Some sporting activities result in acquisition of infections. Contact sports that may cause bleeding have spread hepatitis B [20] and possibly AIDS [21]. Position statements have been published regarding the spread of HIV and other blood-borne pathogens in contact sports [22]. Even without bleeding, direct contact with skin or indirect contact via equipment and clothing may result in transmission of erythrasma and impetigo. Herpes simplex virus has occurred in outbreak form among members of high school and college wrestling teams and among rugby players. Football games seem to provide an unusually fertile opportunity to share pathogens via close physical contact; thus, actual outbreaks of enteroviral meningitis Microbes and Infection 2001, 509-514
Infections from leisure-time activities
Review
Leisure time is part of our lives. Our choice is not whether to indulge, but how. The infectious risks can not be eliminated entirely, but an appreciation of their pathogenesis and epidemiology can help us minimize their occurrence and recognize them in our patients.
References
Figure 1. The iguana, a popular pet and denizen of many vacation sites, is also a reservoir of Salmonella.
and acute gastroenteritis due to Norwalk virus have occurred among members of high school and college football teams [23, 24]. As noted above, water exposure may spread diseases such as conjunctivitis, otitis externa and leptospirosis, and these may attack participants in sporting activities such as canoeing and competitive swimming.
10. Sexually transmitted diseases Sexually transmitted disease (STD) may certainly be related to ‘leisure time’. The traditional aspect of the major STDs will not be reviewed here, but some general comments are in order. Of the leisure activities associated with STDs, travel seems to be the most important. Travelers are more likely to engage in casual sex, drink and experiment with drugs than they are at home. The adventurous explorer may thus affect himself, fellow travelers, or the local population. Returning travelers with symptoms of local or systemic disease should be questioned about sexual practices during their travels. Studies of risk behavior in international travelers [25, 26] suggest that it is extremely common to have had new sexual partners while abroad, with many patients reporting multiple new partners; men were more likely than women to have had a new partner, and the likelihood of new sexual experience further correlated with a longer sojourn, a history of paying for sex, and a previous STD. Microbes and Infection 2001, 509-514
[1] http://www.cdc.gov/travel. [2] Wolfe M.S., in: Schlossberg D. (Ed.), Infections of Leisure, ASM Press, Washington, 1999, pp. 361–383. [3] Morb. Mortal Wkly Rep. 49 (14) (2000). [4] Bull WHO 78 (2000) 995–998. [5] Miller J.M., Tam T.W.S., Maloney S., Fukuda K., Cox N., Hockin J., Keretesz D., Klimov A., Cetron M., Cruise Ships: High-risk passengers and the global spread of new influenza viruses, Clin. Infect. Dis. 31 (2000) 433–438. [6] Lobato M.N., Hopewell P.C., Mycobacterium tuberculosis infection after travel to or contact with visitors from countries with a high prevalence of tuberculosis, Am. J. Respir. Crit. Care Med. 159 (1998) 1871–1875. [7] Cunha A.A. (Ed.), Tickborne Infectious Diseases, Dekker, New York, 2000. [8] Mueller B., Diem P., Burgi U., Travelers’ Thyrotoxicosis Revisited, Arch. Intern. Med. 158 (1998) 1723. [9] Kostman J.R., DiNubile M., Nodular Lymphangitis: A distinctive but often unrecognized syndrome, Ann. Intern. Med. 118 (1993) 883–888. [10] Morris J.G., Pfiesteria, “The Cell from Hell,” and other Toxic Algal Nightmares, Clin. Infect. Dis. 28 (1999) 1191–1198. [11] Dworzack D.L., in: Schlossberg D. (Ed.), Infections of Leisure, ASM Press, Washington, D.C, 1999. [12] Exodus 7:20. [13] Clemence M., Guerrant R.L., in: Schlossberg D. (Ed.), Infections of Leisure, ASM Press, Washington, D.C., 1999. [14] Buchholz U., Mouzin E., Dickey R., Moolenaar R., Sass N., Mascola, Haff Disease: From the Baltic Sea to the U.S. Shore, Emerg. Infect. Dis. 6 (2000) 192–195. [15] Griffiths J.K., in: Schlossberg D. (Ed.), Infections of Leisure, ASM Press, Washington, D.C., 1999. [16] Schantz P.M., Moore A.C., Munoz J., Hartman B., Schaefer J.A., Aron A.M., Persaud D., Sarti E., Wjilson M., Flisser A., Neurocysticercosis in an Orthodox Jewish Community in New York City, N. Engl. J. Med. 327 (1992) 692–695. [17] Morb. Mortal Wkly Rep. 49 (205) (2000). [18] Chomel B.B., in: Schlossberg D. (Ed.), Infections of Leisure, ASM Press, Washington, D.C., 1999. [19] Weinstein M.R., Litt M., Kertesz D.A., Wyper P., Rose D., Coulter M., McGeer A., Facklam R., Ostach C., Willey B., Borczyk A., Low D., Invasive Infections Due to a Fish Pathogen, Streptococcus iniae, N. Engl. J. Med. 337 (1997) 589–594. [20] Kashiwagi S., Hayashi J., Ikematsu H., Nishigori S., Ishihara K., Kaji M., An Outbreak of hepatitis B in Members of a High School Sumo Wrestling Club, JAMA 248 (1982) 213–214. 513
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[21] Torre D., Sampietro C., Ferraro G., Zeroli C., Speranza F., Transmission of HIV-1 Infection via Sports Injury, Lancet 335 (1990) 1105. [22] American Medical Society for Sports Medicine and American Academy of Sports Medicine, Human Immunodeficiency Virus (HIV) and Other Blood-borne Pathogens in Sports (joint position statement), Am. J. Sports Med. 23 (1995) 510–514. [23] Alexander J.P., Chapman L.E., Pallansch M.A., Stephenson W.T., Torok T.J., Anderson L.J., Coxsackievirus B2 infection and Aseptic Meningitis: A Focal Outbreak Among Members of a High School Football Team, J. Infect. Dis. 167 (1993) 1201–1205.
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[24] Becker K.M., Moe C.L., Southwick K.L., MacCormack J.N., Transmission of Norwalk Virus During a Football Game, N. Engl. J. Med. 343 (2000) 1223–1230. [25] Hawkes G., Hart G.J., Bletsoe E., Shergold C., Johnson A.M., Risk Behavior and STD Acquisition in Genitourinary Clinic Attenders Who Have Travelled, Genitourin Med. 71 (1995) 351–354. [26] Hawkes S.G., Hart G.J., Johnson A.M., Shergold C., Ross E., Herbert K.M., Mortimer P., Parry J.V., Mabey D., Risk Behavior and HIV Prevalence in International Travellers, AIDS 8 (1994) 247–252.
Microbes and Infection 2001, 509-514
Review
Infections from leisure-time activities David Schlossberg* Medical Services, Merck & Co., Inc., West Point, PA 19486, USA
ABSTRACT – Leisure-time activities expose us to a variety of infections. The traveler confronts new pathogens and vectors. Camping, hiking and gardening have attendant risks, as does exposure to fresh and salt water. Adventuresome eating poses gastronomic threats, and pets, sexual exposure and organized sports each contribute distinctive infectious risks to participants. © 2001 Éditions scientifiques et médicales Elsevier SAS infection / leisure / travel
1. Introduction Developed society tends to increase its leisure time. We swim, hike, garden, travel abroad, pamper our pets, engage in sports and eat adventurously. Often, in our abandon in these playful pursuits we ignore their risks. But perils exist, and many infectious diseases can result from our leisuretime activities. This review discusses the most common types of leisure activities, identifying in each instance the attendant risks of infection that may spoil the fun.
2. Travel We all love to travel, but infectious risks abound. A rich historical lore accompanies the infectious risks of travel. Such dangers were well-known to invading armies: for example, when Napoleon invaded Russia in 1812, he lost tens of thousands of troops to typhus before encountering any enemy fusillades. The ease of foreign travel and the millions of potential patients who cross international borders daily, require increasing consideration of both local and exotic infections. The infectious considerations regarding travel may be divided into pre-travel and post-travel categories. Thus, prior to foreign travel, a general medical kit should be assembled; the infectious disease concerns of the kit center around an antimicrobial agent for turista, (e.g., ciprofloxacin), anti-malarial prophylaxis, and insect repellants. Immunizations must supplement routine childhood protection with consideration of vaccines for yellow fever, cholera, hepatitis A and hepatitis B, influenza, pneumococcal infection, meningococcal infection, Japanese encephalitis virus, plague, rabies and typhoid fever. Deci*Correspondence and reprints. E-mail address: [email protected] (D. Schlossberg). Microbes and Infection 2001, 509-514
sions regarding individual vaccines vary with projected behavior and destination, and current recommendations may be sought at the Centers for Disease Control and Prevention in Atlanta, Georgia [1]. Upon return, the traveler may present to his physician with a variety of syndromes, and the differential diagnosis will depend on clues from the patient’s areas of travel and activities. Thus, gastroenteritis raises the possibility of bacterial infection (Salmonella, Shigella, Campylobacter, Aeromonas, Yersinia, Vibrio), toxin-induced illness (due to Escherichia coli, Clostridium difficile, fish and shellfish poisoning), or viral infection (Rotavirus and Norwalk). Longer incubation periods and prolonged symptoms frequently suggest parasitosis due to Entamoeba, Giardia, Dientamoeba, Cryptosporidium, Isospora, Microsporidia or Cyclospora. There are geographic clues that may help in differential diagnosis, for example, the association of giardiasis with St Petersburg (the ’Trotskys’), Aeromonas with Thailand, Shigella with Mexico, and Cyclospora with Nepal [2]. Rash and fever in the returning traveler suggest rickettsial infection, viral infection with HIV or dengue, syphilis and typhoid fever. It has recently been appreciated that HIV patients returning from southeast Asia may develop disseminated infection with Penicillium marneffei and present with fever and a papular rash. Some returning travelers manifest eosinophilia as part of their illness. These patients should be evaluated for intestinal parasites such as roundworm, pinworm, whipworm and, especially in AIDS, strongyloides. With the appropriate geography, schistosomiasis and filariasis (both loa loa and onchocerciasis) may explain the combination of fever and eosinophilia. At times, fever alone (without specific localizing symptomatology) is the presenting complaint. These patients often have hepatitis A, amoebic liver abscess, early tick typhus, malaria or salmonellosis, but less common causes 509
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of this presentation require consideration of brucellosis, tuberculosis, early HIV, leishmaniasis, and trypanosomiasis [2]. The WHO reports that yellow fever transmission is on the increase, especially in travelers from the United States to South America and Africa, so a presentation of hepatitis is not always due to the more common hepatotropic viruses. [3]. Sometimes the pattern of fever can provide a clinical clue; thus, relapsing fever suggests brucellosis and borreliosis, while persistent fever is more characteristic of typhoid; dengue often displays a characteristic saddleback pattern. Double quotidien fevers may accompany kala-azar. Malaria classically relapses, but its fevers at times are misleadingly hectic, with multiple daily spikes, either early in the course prior to synchronization, or because of infection with more than one plasmodium species. Skin lesions in the returning traveler can appear to be non-healing ’boils’ that are actually due to myiasis (from the Botfly or the Tumbu fly), linear patterns suggestive of cutaneous larva migrans, and ulcerations from leishmaniasis, diphtheria or syphilis. Some patients develop pneumonia after travel, and most of the time the etiology is not exotic; but when it is, unusual causes of fever and pulmonary infiltrate should be considered, including malaria, plague, melioidosis, helminthic migration, and paraccocidoidomycosis. Tuberculosis appears to represent a significant risk to children who travel to high-risk countries, particularly Mexico, Central America and China, and some advocate testing children routinely upon return from visiting high-risk foci. Tuberculosis can apparently be acquired on an airplane if an infectious passenger coughs enough during a prolonged flight. However, an occasional patient returns from a long flight with fever, cough, and pulmonary infiltrate but is found to have not infection but pulmonary embolization from prolonged sitting; this has been nicknamed the ‘economy class syndrome’. It is not always the human passengers that bring disease from a travel destination; Vectors such as tsetse flies, sandflies and mosquitoes may hitch a ride in the luggage hold or passenger compartment of an airplane, causing infection in patients who live near the airport. Between 1969 and 1999, 87 cases of ‘airport malaria’ were documented in 12 different countries [4]. Conveyances other than airplanes can contribute to travel-related infection: cruise ships have been sources of food-borne illness and respiratory infections, including influenza; it has been pointed out that cruise ships present infection control challenges similar to those in hospitals and nursing homes; in addition, the average cruise length is 6 days, during which time many infections can be incubated, transmitted, and dispersed to multiple passengers with varied destinations [5]. Screening patients after foreign travel, especially to the tropics, need not be routine, but should be undertaken after long-term residence and should include CBC, urinalysis, liver function tests, hepatitis B virus, HIV, serology for shistosomiasis (when appropriate) and stool examination for ova and parasites [2]. Even after short-term travel, screening children with purified protein derivative may be advisable, as noted above [6]. 510
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3. Camping and hiking Camping and hiking are popular activities in many countries, in patients of all ages. These outdoor activities expose adherents to a variety of arthropods, which torment humans by stings, bites, envenomation and hypersensitivity; in addition, they are also efficient vectors of infection. Although many of the arthropods are found worldwide, the illnesses they spread reflect their geography. Thus, location alone may dictate whether a tick spreads Colorado tick fever, Powasson encephalititis, Crimean-Congo hemorrhagic fever, central European encephalitis, ehrlichiosis, Lyme disease, Q Fever, borreliosis, babesiosis or tularemia. Clearly, physicians must know the patterns of tick-borne illness in areas their patients live in, or visit. Rickettsial infections spread by ticks include the well-known illnesses Rocky Mountain spotted fever and Israeli spotted fever (tick typhus), but a number of Rickettsiae have been described only recently, including R. africae, R. japonica, R. felis, R. mongolotimonae and R. slovaca. Ticks do not always cause disease by transmitting infection; tick paralysis, caused by over 60 species of ticks worldwide, may mimic such classic infectious syndromes as polio, botulism, Guillain-Barre syndrome and infectious myelitis [7]. Animal-associated mites spread encephalitis, murine typhus and rickettsialpox, and mosquitoes, of course, carry malaria, dengue, yellow fever and encephalitis. True flies carry classic scourges of mankind such as loiasis and tularemia (deer fly), onchocerciasis (black fly), trypanosomiasis (tsetse fly) and leishmaniasis, bartonellosis and sand fly fever (sand fly). Even the lowly flea commands respect for its ability to transmit murine typhus and one of mankind’s oldest enemies, plague. In addition to arthropods, campers and hikers risk infection from giardia when drinking from sparkling mountain streams and histoplasmosis if they explore bat caves or inhale the fungus from soil contaminated with the droppings of starlings, blackbirds, pigeons or chickens. Some campers purify their drinking water with iodine-containing preparations; on occasion this practice has resulted in transient thyrotoxicosis following a backpacking adventure (’travelers’ thyrotoxicosis’). As the clinical presentation of thyrotoxicosis can mimic systemic infection, with fever, sweats and weight loss, such patients should be questioned carefully about exposure to or ingestion of iodine [8].
4. Gardening Gardening enthusiasts are at risk from cutaneous lacerations from plants and gardening tools, and may contract infections from pathogens classically associated with soil and plants. Thus, a syndrome of cutaneous nodular lymphangitis in a gardener, particularly a rose fancier, most commonly results from sporotrichosis, but may also follow inoculation with Nocardia and rapidly growing Mycobacteria [9]. These lymphocutaneous syndromes may be mistaken for bacterial/pyogenic infections if the association with soil and plant exposure is not recognized. Microbes and Infection 2001, 509-514
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Respiratory and even systemic disease from histoplasmosis and blastomycosis can result from inhaling these organisms from the soil, and barefoot gardeners risk strongyloidiasis and hookworm infestation from larval penetration of their unprotected feet.
5. The sea Most of the earth is water, and we delight in visiting the ocean and its shores. However, a variety of infections can tarnish this pleasure. Localized infection with Mycobacterium marinum and Erysipelothrix may complicate minor abrasions of the skin; much more invasive soft-tissue infection due to vibrios (especially V. vulnificus and V. damsela) may require extensive debridement and could progress to septicemia in immunosupressed patients or those with liver disease. A pruritic rash within hours of swimming indicates schistosome dermatitis or ’swimmer’s itch’; this eruption follows penetration of the swimmer’s skin with nonhuman schistosomal cercariae, and blossoms on areas of exposed skin. In contrast, seabather’s eruption, from the nematocysts of coelenterate larvae trapped underneath swimwear, occurs on the skin that was covered by bathing suits. While swimmer’s itch occurs in fresh as well as salt water, seabather’s eruption is seen only after exposure to salt water. Swimmer’s ear, an external otitis following water exposure, may be extremely painful and require antimicrobial and anti-inflammatory therapy. Even a moonlight stroll along the beach can be threatening: the dinoflagellates or plankton that cause discoloration of the water (blooms, or red tide) may on occasion be aerosolized by the pounding surf and cause neurologic and respiratory symptoms by their inhalation. Dinoflagellates producing brevetoxin have done this, as have pfisteria, which causes mysterious neurologic illnesses including memory loss [10].
6. Freshwater Freshwater has its own attendant risks. A papular dermatitis due to Pseudomonas may follow immersion in a pool, hot tub, spa or water slide. Soft tissue trauma allows introduction of Aeromonas, which can cause invasive cellulitis. Less invasive skin pathogens, causing indolent nodular or ulcerative lesions, include M. marinum and Prototheca. Swimming pool conjunctivitis follows exposure to water-borne adenovirus, while a potentially more destructive keratitis may indicate amoebic infection. Victims of near-drowning are at risk from pneumonia due to Legionella (which is found even in thermal ponds), as well as Aeromonas, Buckholderia, Pseudallescheria and Chromobacterium violaceum, the last species often associated with skin and liver lesions [11]. Encephalitis after fresh water exposure, especially after diving, requires consideration of amoebic central nervous system infection due to Naegleria fowleri, while a more benign ’aseptic’ meningitis under these circumstances is a common manifestation of leptospirosis, having contaminated the water from the urine of an infected animal. Microbes and Infection 2001, 509-514
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7. Food Food is a common source of leisure-related infections. Often resembling gastroenteritis with associated neurologic phenomena, fish and shellfish poisoning results most often from dinoflagellates in the marine food chain. When they bloom, these organisms can turn the water red. This phenomenon probably explains the appearance of bloody water and subsequent morbidity and mortality noted even in biblical times [12]. As noted earlier, the concentration may be great enough to cause symptoms even without ingestion, from aerosolization in the surf. When ingested, however, syndromes from eating shellfish contaminated with these dinoflagellates may be paralytic, neurotoxic, amnesic and diarrheic, depending on the particular toxin present. Ciguatera fish poisoning presents as gastroenteritis with a varying array of neurologic phenomena; it results from eating large reef fishes that have ingested these toxin-producing dinoflagellates. Alternatively, fish poisoning may result from a histamine reaction from the bacterial decomposition of fish (scombroid) or from the tetrodotoxin in puffer fish (Fugu in Japan) that produces dramatic neurologic symptoms, including respiratory paralysis, and carries a 60% mortality rate [13]. All these toxins are heat stable, so that cooking does not protect the adventuresome diner. An interesting syndrome described in Europe and the USA is Haff disease [14], in which buffalo fish consumption causes rhabdomyolysis due to a heat-stable toxin. This illness differs from most other seafood-related disease in that it is spread by a freshwater fish and, unlike other fish-related toxic illnesses, has no neurologic features. Contaminated shellfish can spread infection due to the Norwalk virus and hepatitis A virus. Many regional foods (e.g., sushi, ceviche) that are served raw, pickled, steeped in lime juice, soaked in alcohol, salted, smoked or buried, are still able to transmit infection [15]. Even cooking or microwaving is frequently inadequate. Thus, anisakiasis, from ocean fish, causes severe immediate abdominal pain, relieved when the worm is removed endoscopically. Freshwater fish carry, among other parasites, Diphyllobothrium latum, Eustrongylides and Gnathostoma; infection with Gnathostoma results in larvae migrating through the host, causing migratory swellings in addition to abdominal pain, cough and eosinophilic meningitis. Of course, cholera is the prototypical bacterial infection resulting from eating raw seafood. Raw beef and pork spread Taenia saginata and T. solium, respectively. A recent outbreak of cysticerciasis in members of an orthodox community in New York [16] was spread by infected housekeepers from Latin America who had taeniasis and shed eggs in their stools. Trichinosis is acquired from undercooked pork as well as bear and wild boar. Thorough cooking of these meats results in a dark gray coloration of the dish, but many diners prefer their meat on the pink side. However, as the late Dr Louis Weinstein would say, “a little pink, a little trichinosis”. Poorly cooked hamburger has caused multiple outbreaks of hemorrhagic colitis due to E. coli O157:H7, with complications of hemolytic uremic syndrome and thrombotic thrombocytopenic purpura. Toxoplasmosis results 511
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from eating rare beef and other meats, such as lamb in kibbee; and unpasteurized milk and cheese (ever more popular among the health-food conscious) carry Listeria, Salmonella, Campylobacter and Yersinia.
8. Animals Much leisure activity is lavished on animals, whether as pets or encountered in the course of other pursuits. Man’s best friend, the dog, has transmitted many infections to its owners, from rabies to a panoply of cutaneous, gastrointestinal and systemic illnesses. Cellulitis from Pasteurella multocida may complicate a dog bite, and this organism can become invasive, especially in hosts compromised by liver disease, extremes of age and pregnancy. Capnocytophaga canimorsus may also complicate dog bites, and this organism is prone to cause devastating complications in patients compromised by splenectomy or alcoholism. Salmonella and Campylobacter may infect the gastrointestinal tract of dogs (especially puppies) which then spread the infection to their owners. Leptospirosis is spread through dogs’ urine, and can be excreted many months after the animal is no longer symptomatic from its infection. Parasitic infections spread by this favorite pet include cryptosporidiosis, isospora, dirofilaria, visceral larva migrans, creeping eruption, echinococcus, and dypilidium. Dermatologic infestation results from dogs’ mites (cheyletiellosis, canine scabies), fleas, and fungal dermatophytes. Cats are associated with a variety of infections. Bartonella (formerly Rochalimaea) henselae is now known to be associated with cats, in whom it frequently causes prolonged and asymptomatic bacteremia. Transmission of B. henselae from cats to man probably occurs via cat fleas. In humans, B. henselae is the cause of cat scratch disease and is a cause of bacillary angiomatosis and parenchymal peliosis in immunocompromised patients, particularly those with AIDS. Fecal–oral transmission from cat to man may result in infection with the bacterial pathogens Campylobacter and Salmonella and a variety of parasites, particularly Cryptosporidium, Toxoplasma and Toxocara. Such classic illnesses as plague, tularemia and a pertussislike syndrome caused by Bordetella bronchiseptica may be acquired from cats, and cat bites, like dog bites, are known to predispose to infection with Pasteurella multocida. Unlike dog bites, however, the cat’s bite wound is more likely to result in osteomyelitis or septic arthritis, especially when the injury involves soft tissues closely overlying bones and joints. This predisposition results from the cats’ teeth, which are sharp and narrow and essentially inject the organisms deeply into a wound. Cats also spread Q Fever, caused by Coxiella burnetii, especially after exposure to parturient cats or their aborted tissue. Birds are favorite pets, but they, too, place their owners at risk. Psittacosis, caused by Chlamydia psittaci, was once thought to result only from exposure to psittacine birds. However, it is now appreciated that this organism may infect most, if not all, avian species and the disease is more 512
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accurately called ornithosis. Birds do not have to appear ill to transmit psittacosis, as they may shed the organism long after their acute illness has abated. Also, the exposure to infected birds may be trivial; although some devotees (and subsequent patients) have been known to kiss their parrots, other victims of ornithosis have merely visited public bird parks. Bird exposure also places man at risk from infection with mosquito-borne arboviruses, Cryptococcus and Histoplasma (from contaminated soil) and, following recent observations in Hong Kong, possibly influenza. Man and rodents have shared an ancient infectious relationship. Different types of rodents tend to be associated with specific infections. Thus, lymphocytic choriomeningitis (LCM) is commonly associated with hamsters; plague, yersiniosis and salmonellosis with guinea pigs; murine typhus and rat bite fevers with rats; and plague with prairie dogs in the southwest US. Mice have shown the ability to spread LCM, rickettsialpox and Salmonella, and most recently the Hantavirus pulmonary syndrome (HPS) has been associated with mouse exposure. HPS is a severe cardiopulmonay illness with 40–60% mortality, seen in North and South America and recently in Central America [17]. A systemic or gastrointestinal infection in a patient with reptile exposure should raise the suspicion of salmonellosis. This is most commonly associated with pet turtles, but is also seen with iguanas and other lizards, snakes, and the Komodo dragon [18] (figure 1). Severe respiratory illness in patients exposed to elephants raises the possibility of TB, which has been transmitted from a zoo elephant to its handlers. Monkeys have been associated with Salmonella, Shigella, TB, herpes B and hepatitis A infection. Finally, fish exposure poses certain infectious risks. Aquariumassociated skin lesions are often due to M. marinum, while non-aquarium fish exposures commonly cause cellulitis or more invasive infections due to Erysipelothrix. A recent outbreak of Streptococcus iniae cellulitis was traced to contamination of Tilapia fish with this organism; the organism was transmitted only to the Asian customers of a fish market who bought the fish live and apparently inoculated themselves from the fish’s spines and bones during preparation. Other customers bought the fish after it had been scaled and cleaned and the appendages removed, presumably thereby reducing the potential for infection [19].
9. Sporting activities Some sporting activities result in acquisition of infections. Contact sports that may cause bleeding have spread hepatitis B [20] and possibly AIDS [21]. Position statements have been published regarding the spread of HIV and other blood-borne pathogens in contact sports [22]. Even without bleeding, direct contact with skin or indirect contact via equipment and clothing may result in transmission of erythrasma and impetigo. Herpes simplex virus has occurred in outbreak form among members of high school and college wrestling teams and among rugby players. Football games seem to provide an unusually fertile opportunity to share pathogens via close physical contact; thus, actual outbreaks of enteroviral meningitis Microbes and Infection 2001, 509-514
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Leisure time is part of our lives. Our choice is not whether to indulge, but how. The infectious risks can not be eliminated entirely, but an appreciation of their pathogenesis and epidemiology can help us minimize their occurrence and recognize them in our patients.
References
Figure 1. The iguana, a popular pet and denizen of many vacation sites, is also a reservoir of Salmonella.
and acute gastroenteritis due to Norwalk virus have occurred among members of high school and college football teams [23, 24]. As noted above, water exposure may spread diseases such as conjunctivitis, otitis externa and leptospirosis, and these may attack participants in sporting activities such as canoeing and competitive swimming.
10. Sexually transmitted diseases Sexually transmitted disease (STD) may certainly be related to ‘leisure time’. The traditional aspect of the major STDs will not be reviewed here, but some general comments are in order. Of the leisure activities associated with STDs, travel seems to be the most important. Travelers are more likely to engage in casual sex, drink and experiment with drugs than they are at home. The adventurous explorer may thus affect himself, fellow travelers, or the local population. Returning travelers with symptoms of local or systemic disease should be questioned about sexual practices during their travels. Studies of risk behavior in international travelers [25, 26] suggest that it is extremely common to have had new sexual partners while abroad, with many patients reporting multiple new partners; men were more likely than women to have had a new partner, and the likelihood of new sexual experience further correlated with a longer sojourn, a history of paying for sex, and a previous STD. Microbes and Infection 2001, 509-514
[1] http://www.cdc.gov/travel. [2] Wolfe M.S., in: Schlossberg D. (Ed.), Infections of Leisure, ASM Press, Washington, 1999, pp. 361–383. [3] Morb. Mortal Wkly Rep. 49 (14) (2000). [4] Bull WHO 78 (2000) 995–998. [5] Miller J.M., Tam T.W.S., Maloney S., Fukuda K., Cox N., Hockin J., Keretesz D., Klimov A., Cetron M., Cruise Ships: High-risk passengers and the global spread of new influenza viruses, Clin. Infect. Dis. 31 (2000) 433–438. [6] Lobato M.N., Hopewell P.C., Mycobacterium tuberculosis infection after travel to or contact with visitors from countries with a high prevalence of tuberculosis, Am. J. Respir. Crit. Care Med. 159 (1998) 1871–1875. [7] Cunha A.A. (Ed.), Tickborne Infectious Diseases, Dekker, New York, 2000. [8] Mueller B., Diem P., Burgi U., Travelers’ Thyrotoxicosis Revisited, Arch. Intern. Med. 158 (1998) 1723. [9] Kostman J.R., DiNubile M., Nodular Lymphangitis: A distinctive but often unrecognized syndrome, Ann. Intern. Med. 118 (1993) 883–888. [10] Morris J.G., Pfiesteria, “The Cell from Hell,” and other Toxic Algal Nightmares, Clin. Infect. Dis. 28 (1999) 1191–1198. [11] Dworzack D.L., in: Schlossberg D. (Ed.), Infections of Leisure, ASM Press, Washington, D.C, 1999. [12] Exodus 7:20. [13] Clemence M., Guerrant R.L., in: Schlossberg D. (Ed.), Infections of Leisure, ASM Press, Washington, D.C., 1999. [14] Buchholz U., Mouzin E., Dickey R., Moolenaar R., Sass N., Mascola, Haff Disease: From the Baltic Sea to the U.S. Shore, Emerg. Infect. Dis. 6 (2000) 192–195. [15] Griffiths J.K., in: Schlossberg D. (Ed.), Infections of Leisure, ASM Press, Washington, D.C., 1999. [16] Schantz P.M., Moore A.C., Munoz J., Hartman B., Schaefer J.A., Aron A.M., Persaud D., Sarti E., Wjilson M., Flisser A., Neurocysticercosis in an Orthodox Jewish Community in New York City, N. Engl. J. Med. 327 (1992) 692–695. [17] Morb. Mortal Wkly Rep. 49 (205) (2000). [18] Chomel B.B., in: Schlossberg D. (Ed.), Infections of Leisure, ASM Press, Washington, D.C., 1999. [19] Weinstein M.R., Litt M., Kertesz D.A., Wyper P., Rose D., Coulter M., McGeer A., Facklam R., Ostach C., Willey B., Borczyk A., Low D., Invasive Infections Due to a Fish Pathogen, Streptococcus iniae, N. Engl. J. Med. 337 (1997) 589–594. [20] Kashiwagi S., Hayashi J., Ikematsu H., Nishigori S., Ishihara K., Kaji M., An Outbreak of hepatitis B in Members of a High School Sumo Wrestling Club, JAMA 248 (1982) 213–214. 513
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[21] Torre D., Sampietro C., Ferraro G., Zeroli C., Speranza F., Transmission of HIV-1 Infection via Sports Injury, Lancet 335 (1990) 1105. [22] American Medical Society for Sports Medicine and American Academy of Sports Medicine, Human Immunodeficiency Virus (HIV) and Other Blood-borne Pathogens in Sports (joint position statement), Am. J. Sports Med. 23 (1995) 510–514. [23] Alexander J.P., Chapman L.E., Pallansch M.A., Stephenson W.T., Torok T.J., Anderson L.J., Coxsackievirus B2 infection and Aseptic Meningitis: A Focal Outbreak Among Members of a High School Football Team, J. Infect. Dis. 167 (1993) 1201–1205.
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[24] Becker K.M., Moe C.L., Southwick K.L., MacCormack J.N., Transmission of Norwalk Virus During a Football Game, N. Engl. J. Med. 343 (2000) 1223–1230. [25] Hawkes G., Hart G.J., Bletsoe E., Shergold C., Johnson A.M., Risk Behavior and STD Acquisition in Genitourinary Clinic Attenders Who Have Travelled, Genitourin Med. 71 (1995) 351–354. [26] Hawkes S.G., Hart G.J., Johnson A.M., Shergold C., Ross E., Herbert K.M., Mortimer P., Parry J.V., Mabey D., Risk Behavior and HIV Prevalence in International Travellers, AIDS 8 (1994) 247–252.
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