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{{Notability|Neologisms |date=September 2008}} {{notable|Neologisms |date=September 2008}}
'''Wilderness diarrhea''' (WD), also called '''wilderness-acquired diarrhea''' (WAD) or '''backcountry diarrhea''', is a variety of ] (TD) in which backpackers, hikers, campers and other outdoor recreationalists are infected during temporary visits to relatively remote natural areas.<ref name="Zell1992">{{cite journal |author=Zell SC |title=Epidemiology of Wilderness-acquired Diarrhea: Implications for Prevention and Treatment |journal=J Wilderness Med |volume=3 |issue=3 |pages=241-9 |year=1992 |url=http://www.wemjournal.org/pdfserv/i0953-9859-003-03-0241.pdf |pmid= |doi= }}</ref> {{Fact|date=July 2008 | Is this the correct definition for "wilderness diarrhea"? Other ref does not discuss "wilderness diarrhea", only discusses "wilderness-acquired diarrhea". See Discussion. }} Risk factors include drinking untreated surface water and failure by the individual and his or her companions to maintain personal hygiene practices and clean cookware.<ref name="pmid16805145">{{cite journal |author=Hargreaves JS |title=Laboratory evaluation of the 3-bowl system used for washing-up eating utensils in the field |journal=Wilderness Environ Med |volume=17 |issue=2 |pages=94–102 |year=2006 |pmid=16805145 |doi= |url=http://www.wemjournal.org/wmsonline/?request=get-document&issn=1080-6032&volume=017&issue=02&page=0094 |quotation=Diarrhea is a common illness of wilderness travelers, occurring in about one third of expedition participants and participants on wilderness recreation courses. The incidence of diarrhea may be as high as 74% on adventure trips. …Wilderness diarrhea is not caused solely by waterborne pathogens, … poor hygiene, with fecal-oral transmission, is also a contributing factor}}</ref> Most cases are self-limited and the cause is most often never known. Some ] and ] researchers believe that the risks of WD have been over-stated and are poorly understood by the public. ]. '''Wilderness diarrhea''' (WD), also called '''wilderness-acquired diarrhea''' (WAD) or '''backcountry diarrhea''', is a variety of ] (TD) in which backpackers, hikers, campers and other outdoor recreationalists are infected during temporary visits to relatively remote natural areas.<ref name="Zell1992">{{cite journal |author=Zell SC |title=Epidemiology of Wilderness-acquired Diarrhea: Implications for Prevention and Treatment |journal=J Wilderness Med |volume=3 |issue=3 |pages=241-9 |year=1992 |url=http://www.wemjournal.org/pdfserv/i0953-9859-003-03-0241.pdf |pmid= |doi= }}</ref> {{Fact|date=July 2008 | Is this the correct definition for "wilderness diarrhea"? Other ref does not discuss "wilderness diarrhea", only discusses "wilderness-acquired diarrhea". See Discussion. }} Risk factors include drinking untreated surface water and failure by the individual and his or her companions to maintain personal hygiene practices and clean cookware.<ref name="pmid16805145">{{cite journal |author=Hargreaves JS |title=Laboratory evaluation of the 3-bowl system used for washing-up eating utensils in the field |journal=Wilderness Environ Med |volume=17 |issue=2 |pages=94–102 |year=2006 |pmid=16805145 |doi= |url=http://www.wemjournal.org/wmsonline/?request=get-document&issn=1080-6032&volume=017&issue=02&page=0094 |quotation=Diarrhea is a common illness of wilderness travelers, occurring in about one third of expedition participants and participants on wilderness recreation courses. The incidence of diarrhea may be as high as 74% on adventure trips. …Wilderness diarrhea is not caused solely by waterborne pathogens, … poor hygiene, with fecal-oral transmission, is also a contributing factor}}</ref> Most cases are self-limited and the cause is most often never known. Some ] and ] researchers believe that the risks of WD have been over-stated and are poorly understood by the public.{{WW}}


==Names and definitions== ==Names and definitions==
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==Causes== ==Causes==
There are three vectors for human infection by pathogens that cause WD: fecal-oral transmission, water, and contaminated food. The major factor governing the amount of pathogen pollution in surface water is human and animal activity in the watershed.<ref>{{harvard citation|Backer|2007|Ref=none|p=1374}}</ref> The most common pathogens that cause WD are ''Giardia'' and ''Cryptosporidium''. Other infectious agents may play a larger role than generally believed and include '']'', ], ], enterotoxogenic '']'', ''e. coli'' 0157:H7, '']'', and various viruses. More rarely, '']'', '']'', and '']'' may also cause disease.<ref>{{harvard citation|Backer|2007|Ref=none|p=1369}}</ref>


'']'', a common cause of WD, does not tolerate freezing and can remain viable for nearly three months in river water when the temperature is 10°C and about one month at 15–20°C in lake water. '']'', another WD pathogen, has been shown to survive in cold waters (4°C) for up to 18 months, and can even withstand freezing, although its viability is thereby greatly reduced.<ref name='Health Canada 2004'> {{Citation| first= | last=Prepared by Federal-Provincial-Territorial Committee on Drinking Water of the Federal-Provincial-Territorial Committee on Health and the Environment (2004)| coauthors=| contribution=Protozoa: Giardia and Cryptosporidium| title=Guidelines for Canadian Drinking Water Quality: Supporting Documentation| editor-first=| editor-last=| coeditors=| publisher=Health Canada| place=| pages=| date=| year=2004| id= | contribution-url=http://www.hc-sc.gc.ca/ewh-semt/alt_formats/hecs-sesc/pdf/pubs/water-eau/protozoa/protozoa.pdf| format=| accessdate=2008-08-07 }}</ref>
Infectious diarrhea acquired in the wilderness is caused by various bacteria, viruses and parasites, the most common of which are thought to be ''Giardia'' and ''Cryptosporidium''. Other infectious agents may play a larger role than generally believed ]
and include '']'', ], ], enterotoxogenic '']'', ''e. coli'' 0157:H7, '']'', and various viruses. More rarely, '']'', '']'', and '']'' may also cause disease.<ref>{{harvard citation|Backer|2007|Ref=none|p=1369}}</ref> Vectors for all of these causes are limited to fecal-oral transmission, and contaminated water and food. The major factor governing pathogen content of surface water is human and animal activity in the watershed.<ref>{{harvard citation|Backer|2007|Ref=none|p=1374}}</ref>.


Many other varieties of diarrhea-causing organisms, including '']'' and '']'', and hepatitis A virus, can survive freezing for weeks to months.<ref name="pmid3889393">{{cite journal |author=Dickens DL, DuPont HL, Johnson PC |title=Survival of bacterial enteropathogens in the ice of popular drinks |journal=JAMA |volume=253 |issue=21 |pages=3141–3 |year=1985 |month=June |pmid=3889393 |doi= |url=}}</ref> Virologists believe all surface water in the United States and Canada has the potential to contain human viruses, which cause a wide range of illnesses including diarrhea, polio and meningitis.<ref name="pmid10731899">{{cite journal |author=Backer H |title=In search of the perfect water treatment method |journal=Wilderness Environ Med |volume=11 |issue=1 |pages=1–4 |year=2000 |pmid=10731899 |doi= |url=}}</ref><ref name="isbn0-387-97162-9">{{cite book |author=Gerba C, Rose J |chapter=Viruses in Source and Drinking Water |editor=McFeters, Gordon A. ed.|title=Drinking water microbiology: progress and recent developments |publisher=Springer-Verlag |location=Berlin |year=1990 |pages=pp 380-399 |isbn=0-387-97162-9 |oclc= |doi= |accessdate=}}</ref><ref name="isbn0-442-00693-4">{{cite book |author=White, George W. |title=The handbook of chlorination and alternative disinfectants |publisher=Van Nostrand Reinhold |location=New York |year=1992 |edition=3rd edition |pages= |isbn=0-442-00693-4 |oclc= |doi= |accessdate=}}</ref>


It may be difficult to causally associate a particular case of diarrhea with a recent wilderness trip lasting only a few days because the incubation time may take longer than the length of time of the trip. Studies of long trips into the wilderness,<ref name=Boulware2003 /><ref name=Boulware2004 /> where the trip time is much longer than the mean incubation time of the disease, are less susceptible to these types of errors since the diarrhea is more likely to occur while the person is still in the wilderness.
Other significant causes of diarrhea are non-infectious, and include medications, stress, or a change in eating or exercise patterns. .


Giardia is ubiquitous outside of wilderness settings, and may affect 7.5 million Americans at any one time.<ref name='NYTimes1989'>{{cite news | first=Jane E. | last=Brody | coauthors= | title= HEALTH: Diagnostics; Test Unmasks a Parasitic Disease | date=1989 | publisher= | url =http://query.nytimes.com/gst/fullpage.html?res=950DE7DC1F3AF935A15753C1A96F948260&scp=5&sq=giardia&st=cse | work =NY Times | pages = | accessdate = 2008-08-07 | language = }}</ref>
In a study of causes of diarrhea at Grand Teton National Park, visitors suffering from active gastrointestinal complaints were invited to a free clinic. Of 178 people tested, 69% had no identifiable disease-causing pathogens. Campylobacter was the most common agent isolated at 23%, followed by Giardia at 8%. Campylobacter enteritis occurred most frequently in young adults who had been hiking in wilderness areas and was associated with drinking untreated surface water in the week before illness
According to a different estimate, about 7% of Americans are infected with giardia from all sources, wilderness and otherwise, although as few as 5% of an infected population may develop symptoms. It is mainly spread by fecal-oral or food-borne transmission.<ref name='Rockwell2003'> {{cite web |url=http://lomaprieta.sierraclub.org/pcs/articles/giardia.asp |title=Giardia Lamblia and Giardiasis With Particular Attention to the Sierra Nevada |accessdate=2008-08-07 |last=Rockwell |first=Robert L. |date=2003 |work=Peak Climbing Section, Loma Prieta Chapter, Sierra Club }}</ref> More than 34,000 cases were reported to state health departments in 1991, of which 19 outbreaks were waterborne, and two affected backpackers or campers.<ref name='TRWelch1995'>{{cite journal |author=Welch TR, Welch TP |title=Giardiasis as a threat to backpackers in the United States: a survey of state health departments |journal=Wilderness Environ Med |volume=6 |issue=2 |pages=162–6 |year=1995 |month=May |pmid=11995903 |doi= |url=}}</ref>


A ] was performed, with an initial screening of 104 articles, in which nine met inclusion criteria for epidemiological analysis. Of the nine articles that were analyzed, neither of two case reports (report of the diagnosis, treatment, and follow-up of an individual patient) met the criteria of the ] for waterborne disease outbreak. Two "prospective" studies (data on subjects who were followed forward in time) showed no significant association of backcountry water with infection. Of four studies that included control groups, none showed a significant relationship between backcountry water and infection. The conclusion was that North American wilderness waters are not a source of giardiasis.<ref name="pmid10737847">{{cite journal |author=Welch TP |title=Risk of giardiasis from consumption of wilderness water in North America: a systematic review of epidemiologic data |journal=Int. J. Infect. Dis. |volume=4 |issue=2 |pages=100–3 |year=2000 |pmid=10737847 |doi= |url=}}</ref><ref name= WelchTR2004>{{cite journal |author=Welch TR |title=Evidence-based medicine in the wilderness: the safety of backcountry water |journal=Wilderness Environ Med |volume=15 |issue=4 |pages=235–7 |year=2004 |pmid=15636372 |doi= |url=http://www.wemjournal.org/pdfserv/i1080-6032-015-04-0235.pdf |format=PDF}}</ref>
It may be difficult to associate a particular case of diarrhea with a recent wilderness trip of a few days because incubation of the disease may outlast the trip. Studies of trips <ref name=Boulware2003 /><ref name=Boulware2004 /> that are much longer than the average incubation period are less susceptible to these errors {{Fact|date=September 2008}}. To cause giardiasis, Giardia requires an ] of one to two weeks (average seven days), while Criptosporidium requires an average of seven days to cause cryptosporidiosis. Other bacterial and viral agents have shorter incubations, although hepatitis may require weeks.

A suspected case of wilderness diarrhea may be assessed within the general context of intestinal complaints. During any given four-week period, as many as 7.2% of Americans may experience some form of infectious or non-infectious diarrhea . There are an estimated 99 million annual cases of intestinal infectious disease in the United States , most commonly from viruses, followed by bacteria and parasites, including Giardia and Cryptosporidium. Giardia alone may infect up to 10% of Americans at any one time. However, because most carriers are asymptomatic, , there are only an estimated 2 million U.S. cases of symptomatic giardiasis annually, spread mostly by fecal-oral or food-borne transmission.<ref name='Rockwell2003'> {{cite web |url=http://lomaprieta.sierraclub.org/pcs/articles/giardia.asp |title=Giardia Lamblia and Giardiasis With Particular Attention to the Sierra Nevada |accessdate=2008-08-07 |last=Rockwell |first=Robert L. |date=2003 |work=Peak Climbing Section, Loma Prieta Chapter, Sierra Club }}</ref>


'']'' does not tolerate freezing and can remain viable for nearly three months in river water when the temperature is 10°C and about one month at 15–20°C in lake water. '']'' may survive in cold waters (4°C) for up to 18 months, and can even withstand freezing, although its viability is thereby greatly reduced.<ref name='Health Canada 2004'> {{Citation| first= | last=Prepared by Federal-Provincial-Territorial Committee on Drinking Water of the Federal-Provincial-Territorial Committee on Health and the Environment (2004)| coauthors=| contribution=Protozoa: Giardia and Cryptosporidium| title=Guidelines for Canadian Drinking Water Quality: Supporting Documentation| editor-first=| editor-last=| coeditors=| publisher=Health Canada| place=| pages=| date=| year=2004| id= | contribution-url=http://www.hc-sc.gc.ca/ewh-semt/alt_formats/hecs-sesc/pdf/pubs/water-eau/protozoa/protozoa.pdf| format=| accessdate=2008-08-07 }}</ref> Many other varieties of diarrhea-causing organisms, including '']'' and '']'', and hepatitis A virus, can survive freezing for weeks to months.<ref name="pmid3889393">{{cite journal |author=Dickens DL, DuPont HL, Johnson PC |title=Survival of bacterial enteropathogens in the ice of popular drinks |journal=JAMA |volume=253 |issue=21 |pages=3141–3 the potential to contain human viruses, which cause a wide range of illnesses including diarrhea, polio and meningitis.<ref |year=1985 |month=June |pmid=3889393 |doi= |url=}}</ref> Virologists believe all surface water in the United States and Canada has has the potential to contain human viruses, which cause a wide range of illnesses including diarrhea, polio and meningitis.<ref name="pmid10731899">{{cite journal |author=Backer H |title=In search of the perfect water treatment method |journal=Wilderness Environ Med |volume=11 |issue=1 |pages=1–4 |year=2000 |pmid=10731899 |doi= |url=}}</ref><ref name="isbn0-387-97162-9">{{cite book |author=Gerba C, Rose J |chapter=Viruses in Source and Drinking Water |editor=McFeters, Gordon A. ed.|title=Drinking water microbiology: progress and recent developments |publisher=Springer-Verlag |location=Berlin |year=1990 |pages=pp 380-399 |isbn=0-387-97162-9 |oclc= |doi= |accessdate=}}</ref><ref name="isbn0-442-00693-4">{{cite book |author=White, George W. |title=The handbook of chlorination and alternative disinfectants |publisher=Van Nostrand Reinhold |location=New York |year=1992 |edition=3rd edition |pages= |isbn=0-442-00693-4 |oclc= |doi= |accessdate=}}</ref>


==Degree of risk== ==Degree of risk==
The risk of acquiring infectious diarrhea in the wilderness arises from inadvertent ingestion of pathogens. Various studies have sought to estimate diarrhea rates among wilderness travelers and results have ranged widely. A number of these have either focused on only one pathogen, Giardia lamblia, or provided scant data. The risk of acquiring diarrhea in the wilderness arises from inadvertent ingestion of pathogens. Studies have been done to estimate diarrhea rates of wilderness travelers but for the most part they have either focused on only one pathogen, giardia lamblia, or provided scant data. A notable exception is a study of ] hikers.<ref name="Boulware2003"> {{cite journal |author=Boulware DR, Forgey WW, Martin WJ 2nd |title=Medical Risks of Wilderness Hiking |journal=Am J Med |volume=114 |issue=4 |pages=288-93 |year=2003 |pmid=12681456 |doi= }}</ref><ref name="Boulware2004">{{cite journal |author=Boulware DR |title=Influence of Hygiene on Gastrointestinal Illness Among Wilderness Backpackers |journal=J Travel Med |volume=11 |issue=1 |pages=27-33 |year=2004 |pmid=14769284 |doi= }}</ref>


===Appalachian Trail Study===
===Rate of Infection Studies===
An ] study of 280 long-distance hikers who each logged an average 139 days on the Appalachian Trail found that diarrhea was experienced by 56% of the ]. The occurrence of diarrhea was positively associated with the duration of exposure in the wilderness. The diarrhea rate was reduced among those who either consistently treated their drinking water or had good personal hygiene.


Those who consistently treated their water had a diarrhea rate of 45% compared to 69% for those who did so inconsistently. The worst diarrhea rate of 86% was among those who drank untreated surface water (streams or ponds) more than several times a week.
Gastrointestinal illnesses occurred at the rate of 0.26 per 1,000 days in the field among National Outdoor Leadership Schools participants in 2002-2005, and 0.20 incidents per 1,000 days during 1999-2002. These rates had declined from 0.44 per 1,000 days in 1984-1989. Program duration was from two weeks to three months in various wilderness settings primarily in North America, but also in South America, Asia, and Australia. NOLS instructors emphasize water treatment and hygiene. The complaints amounted to 23% of all illness reported in the programs during 2002-2005.


Those who washed their hands with soap and water routinely after defecation had a 36% diarrhea rate compared to 59% for those who didn't.
A study of 280 long-distance hikers on the ] <ref name="Boulware2003"> {{cite journal |author=Boulware DR, Forgey WW, Martin WJ 2nd |title=Medical Risks of Wilderness Hiking |journal=Am J Med |volume=114 |issue=4 |pages=288-93 |year=2003 |pmid=12681456 |doi= }}</ref><ref name="Boulware2004">{{cite journal |author=Boulware DR |title=Influence of Hygiene on Gastrointestinal Illness Among Wilderness Backpackers |journal=J Travel Med |volume=11 |issue=1 |pages=27-33 |year=2004 |pmid=14769284 |doi= }}</ref> who each logged an average 139 hiking days found that diarrhea was reported via questionaire by 56% of the participants. Those who consistently treated their water had a diarrhea rate of 45% compared to 69% for those who did so inconsistently. A rate of 86% was found among those who drank untreated surface water (streams or ponds) more than several times a week. Those who washed their hands with soap and water routinely after defecation had a rate of 36%, compared with 59% for those who didn't. The majority of the 2,100-mile Appalachian Trail traverses woodlands in non-wilderness settings, including about 10% in New Jersey, Southern New York and Connecticut.


===Other Studies===
Studies of shorter duration hikes resulted in a lower rate of infection or illness, which is expected because of less exposure. In one study, an illness rate of 3-5% was found.<ref name=Zell1992 />. Another study of backpackers in California found a Giardia infection rate of 5.7% but no symptomatic giardiasis. An additional 16.7% of subjects in the California study developed mild gastrointestinal illness, but no Giardia infection.<ref name='Zell93'> {{cite journal|title=Cyst acquisition rate for Giardia lamblia in backcountry travelers to Desolation Wilderness, Lake Tahoe|journal=Journal of Wilderness Medicine|date=1993|first=S. C.|last=Zell|coauthors=S. K. Sorenson|volume=4|issue=2|pages=147-54|id= |url=http://www.wemjournal.org/wmsonline/?request=get-abstract&issn=0953-9859&volume=004&issue=02&page=0147|format=|accessdate= }}</ref>


In a separate project at Grand Teton National Park, visitors suffering from active gastrointestinal complaints were invited to a free clinic. Of 178 cases tested, ] was the most common agent isolated at 28%, followed by Giardia at 8%. ] and ] were not isolated and 69% of subjects had no identifiable pathogen.<ref name=Zell1992 />
A separate 1992 questionaire survey of 180 hikers who completed the Applalachian trail found that 63% of subjects reported having diarrhea at least one time during the course of their trip. In 58% of these cases, the duration of the diarrhea was two days or less. Only 7% of all subjects drank exclusively from protected water, with the majority consuming unprotected or untreated water about once a month. There were no significant differences in the frequency of diarrhea between those who drank untreated water and those who treated their water. Authors speculated that the lack of correlation was because of the small size of the study, or incorrect use of filters or disinfectants. Authors also cited an earlier study suggesting that inadequately prepared or unrefrigerated food is a common cause of gastroenteritis in campers.


In a 1991 giardiasis survey of 48 state health departments in the United States, 34,348 cases were reported. Of these, 19 were attributed to contaminated drinking water and 2 were reported among campers and backpackers. <ref name=TRWelch1995 />
A questionaire of 155 backpackers who completed the Long Trail in Vermont was analyzed in 1993 and found 10.7% of 74 through-hikers and 3.8% of 76 section hikers reported gastrointestinal complaints. Through hikers reported an average of 25 days to complete the trail; section hikers completed the trail in an average of 4.7 years. The 270-mile Long Trail intermittantly traverses wilderness settings. Authors speculated that through-hikers had more opportunity than section hikers to ingest contaminated food and water.


Ingesting 10 – 25 Giardia cysts results in a 33% risk of detectable cysts in stools, and a significantly smaller risk of symptomatic giardiasis. Between 0.108 and 0.003 Giardia cysts per liter of water were measured in a 1984 survey of 18 backcountry sites in California's Sierra Nevada. The same survey detected no Giardia at 66 additional sites. Another survey completed in 1990 of three Sierra Nevada sites on 10 different dates, found concentrations between 0.0 and 0.62 cysts per liter.<ref name=Rockwell2003 /> An additional survey by Backpacker Magazine of several backcountry sites was completed in 2003. The highest concentration that survey found was 1.5 Giardia cysts per liter. Drinking seven liters of such water may result in a minimum infective dose.<ref name= WelchTR2004 />
in a 2000 review of four separate field studies, Steven Zell of the University of Nevada's medical school concluded that the general rate of infectious diarrhea acquired in the wilderness "is probably less than 10%, with scant data placing it in the 3% to 5% range." The studies's separate findings on infection rates ranged from 65% to 3%. The studies, two of which included stool sampling, were in the Uintah and Escalante regions of Utah and in Rocky Mountain National Park in Colorado and involved from 53 to 160 subjects. The hike-duration in one of the studies was two weeks. Duration wasn't specified in the other three studies. Howard Backer, author of the water disinfection chapter of a standard reference work ''Wilderness Medicine,'' said in an editorial on Zell's project that he agreed "with much of risk analysis." . In the editorial, Backer said "there is much misunderstanding, verging on paranoia, about the risk of acquiring diarrhea from microorganisms resident in wilderness water," and that fecal-oral transmission may be the most common vector for backcountry Giardia infection. Backer, however, disagreed with Zell's suggestion that routine disinfection of water may be unwarranted during relatively brief backcountry visits.

An additional study of 41 backpackers in California's Sierra Nevada conducted later by Zell and the U.S. Geological Survey, Water Resources Division, found a Giardia infection rate of 5.7% in stool samples, but no symptomatic giardiasis. A further 16.7% of subjects in this study developed mild gastrointestinal illness, but no Giardia infection. Duration of hikes wasn't specified. Water sampling from three popular stream sites within the study area revealed cyst contaminations in the single digit range for every 100 gallons filtered. Ingestion of 10 cysts is considered a minimum infective dose.

====Backcountry Water Quality Surveys====

Other sampling surveys have focused on micro-organism content of backcountry water.

Between 0.108 and 0.003 Giardia cysts per liter of water were measured in a 1984 survey of 18 backcountry sites in California's Sierra Nevada. The same survey detected no Giardia at 66 additional sites. Ingesting 10 Giardia cysts is regarded in the minimum infective dose. Another survey completed in 1990 of three Sierra Nevada sites on 10 different dates, found concentrations between 0.0 and 0.62 cysts per liter.].

An additional survey by Backpacker Magazine of several backcountry sites was completed in 2003. The highest concentration that survey found was 1.5 Giardia cysts per liter. .

A further survey of 23 sites in the Sierra Nevada in 2003 sought to mesure coliform bacteria, used as indicators of fecal pollution. Coliforms were detected at eight of the sites. . Very low levels were measured in six of eight sites. Two sites had moderate levels. Author Robert Derlet of the University of California Davis medical school expressed the view that "bacteria, and not protozoa such as Giardia, pose a greater risk of causing water-borne disease in humans."

Derlet performed a similar survey in 2007 of 37 sites in Kings Canyon and Sequoia national parks and found coliforms at 14 sites. None of the 11 sites classified as wild areas had coliforms; two of 12 sites classified as backpack and day-hike areas had coliforms and 12 of 14 sites classified as pack animal areas had coliforms. Data by risk category was consistent with prior studies in the immediate region, as well as data from the entire Sierra consisting of nearly 600 samples analyzed by Derlet from 2001-2007.
Elsewhere, the author expresses the view that the risk of giardiasis from backcountry water has been "well over-stated." and that "perhaps less than 1% of streams in the Sierra would have Giardia significant enough to cause infection in humans."

====Other Studies====

A survey of available literature on the risk of giardiasis from consumption of wilderness water in North America in 2000 by TP Welch of the Tulane School of Public Health found a high incidence of confirmed giardiasis among outdoor recreationalists, but little association between drinking backcountry water and acquiring giardiasis. ]. Of 104 articles identified in the initial screening, nine met the inclusion criteria. In the articles analyzed, neither of two case reports (report of the diagnosis, treatment, and follow-up of an individual patient) met the criteria of the Centers for Disease Control for waterborne disease outbreak. Two "prospective" studies (data on subjects who were followed forward in time) showed no significant association of backcountry water with infection. Of four studies that included control groups, none showed a significant relationship between backcountry water and infection.

In a 1991 giardiasis survey of 48 state health departments in the United States, 34,348 cases were reported. Of these, 19 were attributed to contaminated drinking water and 2 were reported among campers and backpackers. <ref name='TRWelch1995'>{{cite journal |author=Welch TR, Welch TP |title=Giardiasis as a threat to backpackers in the United States: a survey of state health departments |journal=Wilderness Environ Med |volume=6 |issue=2 |pages=162–6 |year=1995 |month=May |pmid=11995903 |doi= |url=}}</ref>


==Symptoms== ==Symptoms==
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==Prevention== ==Prevention==
Since WD can be caused by fecal-oral transmission, contaminated water, and contaminated food, prevention methods should address these causes. Also it was found that on very long trips, taking multivitamins was associated with a reduction of WD.<ref name=Boulware2003 /><ref name=Boulware2004 />


The risk of fecal-oral transmission of pathogens can be reduced by good hygiene. This includes: washing hands after urination and defecation; and washing eating utensils with warm soapy water.<ref name=Boulware2004 /> Additionally a three-bowl system can be used for washing eating utensils.<ref name="pmid16805145"/>
Since wilderness-acquired diarrhea can be caused by fecal-oral transmission, contaminated water, and contaminated food, prevention methods should address these causes.
The risk of fecal-oral transmission of pathogens can be reduced by good hygiene, including washing hands eating utensils with warm soapy water on a timely basis.<ref name=Boulware2004 /> Additionally a three-bowl system can be used for washing eating utensils.<ref name="pmid16805145"/>


Various filters and chemicals are available for treating drinking water..<ref name='Adachi2007'>{{cite encyclopedia |last=Adachi |first=Javier A. |author= |authorlink= |coauthors=Howard D. Backer, and Herbert L. Dupont |editor=Paul S. Auerbach |encyclopedia=Wilderness Medicine |title=Infectious Diarrhea from Wilderness and Foreign Travel |url= |accessdate= |edition= |date= |year=2007 |publisher= |volume= |location= |id= |doi= |pages=1418 |quote= }}</ref> (see ]). Factors in choice may inlude the number of people involved, space and weight considerations, the quality of available water, personal taste and preferences, and fuel availability. Authoritative guidelines caution that safety judgments cannot reliably be made based on the mere appearances of a water source. One key to prevention is therefore various filters and chemical treatments.<ref name='Adachi2007'>{{cite encyclopedia |last=Adachi |first=Javier A. |author= |authorlink= |coauthors=Howard D. Backer, and Herbert L. Dupont |editor=Paul S. Auerbach |encyclopedia=Wilderness Medicine |title=Infectious Diarrhea from Wilderness and Foreign Travel |url= |accessdate= |edition= |date= |year=2007 |publisher= |volume= |location= |id= |doi= |pages=1418 |quote= }}</ref> (see ]). The choice depends upon the number of people involved, space and weight considerations, the quality of available water, personal taste and preferences, and fuel availability. If ''Giardia lamblia'' is an uncommon isolate and WAD (wilderness-acquired diarrhea) is infrequent, then it may not be cost effective to recommend filtering for recreationalists involved in short-duration trips.<ref name="Zell1992" />
Careful attention to personal hygiene can help prevent the spread of infection.<ref name=Boulware2004 />


In a study of long-distance backpacking, it was found that water filters were used more consistently than chemical disinfectants. Inconsistent use of iodine or chlorine may be due to disagreeable taste, extended treatment time or treatment complexity due to water temperature and turbidity.<ref name=Boulware2003 /> In a study of long-distance backpacking, it was found that water filters were used more consistently than chemical disinfectants. Inconsistent use of iodine or chlorine may be due to disagreeable taste, extended treatment time or treatment complexity due to water temperature and turbidity.<ref name=Boulware2003 />


Because methods based on ], such as iodine and chlorine, do not kill ''Cryptosporidium'', and because filtration misses some viruses, the best protection may require a two-step process of either filtration or coagulation-], followed by ]. Boiling is effective in all situations. Because methods based on ], such as iodine and chlorine, do not kill ''Cryptosporidium'', and because filtration misses some viruses, the best protection may require a two-step process of either filtration or coagulation-], followed by ]. Boiling is effective in all situations, but won't improve the water's taste.


Iodine resins, if combined with microfiltration to remove resistant cysts, are also a viable single-step process, but may not be effective under all conditions. New one-step techniques using chlorine dioxide, ozone, and UV radiation may prove effective, but still require validation.<ref name='Backer2002'>{{cite journal |author=Backer H |title=Water disinfection for international and wilderness travelers |journal=Clin. Infect. Dis. |volume=34 |issue=3 |pages=355–64 |year=2002 |month=February |pmid=11774083 |doi= |url=http://www.journals.uchicago.edu/doi/full/10.1086/324747?cookieSet=1}}</ref> Iodine resins, if combined with microfiltration to remove resistant cysts, are also a viable single-step process, but may not be effective under all conditions. New one-step techniques using chlorine dioxide, ozone, and UV radiation may prove effective, but still require validation.<ref name='Backer2002'>{{cite journal |author=Backer H |title=Water disinfection for international and wilderness travelers |journal=Clin. Infect. Dis. |volume=34 |issue=3 |pages=355–64 |year=2002 |month=February |pmid=11774083 |doi= |url=http://www.journals.uchicago.edu/doi/full/10.1086/324747?cookieSet=1}}</ref>
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Ultraviolet (UV) light for water disinfection is well established and widely used for large applications, like municipal water systems. A small portable UV device, called a Steri-pen, is now available for hikers. According to the manufacturer, it meets standards set forth in the U.S. EPA Guide Standard and Protocol for Testing Microbiological Water Purifiers.<ref>{{harvard citation|Backer|2007|Ref=none |p=1411}}</ref> Ultraviolet (UV) light for water disinfection is well established and widely used for large applications, like municipal water systems. A small portable UV device, called a Steri-pen, is now available for hikers. According to the manufacturer, it meets standards set forth in the U.S. EPA Guide Standard and Protocol for Testing Microbiological Water Purifiers.<ref>{{harvard citation|Backer|2007|Ref=none |p=1411}}</ref>


Also, one study suggests that on very long trips, taking multivitamins may reduce its incidence. WD.<ref name=Boulware2003 /><ref name=Boulware2004 /> In summary, both careful attention to personal hygiene and water treatment have been shown to be important for preventing wilderness diarrhea.<ref name="pmid16805145"/><ref name=Boulware2003 /><ref name=Boulware2004 />

The backcountry medical text ''Wilderness Medicine,'' describes water disinfection and personal hygiene as one key to preventing wilderness diarrhea. Drinking untreated backcountry water is "like Russian roulette," according to its editor, Paul S. Auerbach, in an interview with REI.com. Auerbach added that while research has shown ''Giardia'' in wilderness water sources is "probably not as prevalent as once believed...it's still present". Howard Backer, author of ''Wilderness Medicine's'' guidelines on water disinfection, told the same publication that if a wilderness visitor is confident of untainted alpine water, "you're probably safe to drink it untreated," but that in areas with significant human or animal activity, the risk of infection makes precautionary disinfection a wise precaution.].

The text ''Medicine for Mountaineering and Other Wilderness Activities'' <ref>Seattle, Washington: The Mountaineers Books, 5th edition, 2001</ref>, also advises that disinfection and hygiene are necessary to avoid risk, although elsewhere, the same work notes that "exaggerated concern" has been raised about the issue.

Other commentators place relatively greater emphasis on preventative hygiene. Thomas R. Welch in a 2004 editorial in the journal ''Wilderness Medicine'' expressed the view that "stopping hand-to-mounth spread is the key to preventing gastrointestinal infection" and that routine universal treatment of water should be de-emphasized. ] Similarly, Robert L. Rockwell, an engineer whose writing and views on the topic of backcountry Giardia ] are frequently cited, believes that Giardia in the wilderness is typically acquired via the fecal-oral vector rather than from contaminated water. ]

One researcher, in discussing evidence for Giardia contamination of backountry water sources, suggested that if ''Giardia lamblia'' is an uncommon isolate and wilderness-acquired diarrhea is infrequent, then it may not be cost effective to recommend filtering for recreationalists involved in short-duration trips.<ref name="Zell1992" />
Careful attention to personal hygiene can help prevent the spread of infection.<ref name=Boulware2004 />


==Water disinfection== ==Water disinfection==
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==Footnotes== ==Footnotes==
{{reflist}} {{reflist}}



] ]

Revision as of 03:07, 10 September 2008

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Wilderness diarrhea (WD), also called wilderness-acquired diarrhea (WAD) or backcountry diarrhea, is a variety of traveler’s diarrhea (TD) in which backpackers, hikers, campers and other outdoor recreationalists are infected during temporary visits to relatively remote natural areas. Risk factors include drinking untreated surface water and failure by the individual and his or her companions to maintain personal hygiene practices and clean cookware. Most cases are self-limited and the cause is most often never known. Some medical and public health researchers believe that the risks of WD have been over-stated and are poorly understood by the public.

Names and definitions

As a variety of travelers' diarrhea, "wilderness diarrhea" is a form of infectious diarrhea, itself classified as a type of secretory diarrhea. These are all considered forms of gastroenteritis. The term may be applied in various remote areas of non-tropical developed countries (U.S., Canada, western Europe, etc.), but is less applicable in developing countries, and in the tropics, because of very different pathogens likely to be encountered there.

The term "backpacker’s diarrhea" might be an appropriate synonym for "Wilderness Diarrhea," but medical literature has traditionally reserved that term, with fair consistency, for giardiasis — a specific cause of "wilderness diarrhea."

Causes

There are three vectors for human infection by pathogens that cause WD: fecal-oral transmission, water, and contaminated food. The major factor governing the amount of pathogen pollution in surface water is human and animal activity in the watershed. The most common pathogens that cause WD are Giardia and Cryptosporidium. Other infectious agents may play a larger role than generally believed and include Campylobacter, hepatitis A virus, hepatitis E virus, enterotoxogenic E. coli, e. coli 0157:H7, Shigella, and various viruses. More rarely, Yersinia enterocolitica, Aeromonas hydrophila, and Cyanobacterium may also cause disease.

Giardia lamblia, a common cause of WD, does not tolerate freezing and can remain viable for nearly three months in river water when the temperature is 10°C and about one month at 15–20°C in lake water. Cryptosporidium, another WD pathogen, has been shown to survive in cold waters (4°C) for up to 18 months, and can even withstand freezing, although its viability is thereby greatly reduced.

Many other varieties of diarrhea-causing organisms, including Shigella and Salmonella typhi, and hepatitis A virus, can survive freezing for weeks to months. Virologists believe all surface water in the United States and Canada has the potential to contain human viruses, which cause a wide range of illnesses including diarrhea, polio and meningitis.

It may be difficult to causally associate a particular case of diarrhea with a recent wilderness trip lasting only a few days because the incubation time may take longer than the length of time of the trip. Studies of long trips into the wilderness, where the trip time is much longer than the mean incubation time of the disease, are less susceptible to these types of errors since the diarrhea is more likely to occur while the person is still in the wilderness.

Giardia is ubiquitous outside of wilderness settings, and may affect 7.5 million Americans at any one time. According to a different estimate, about 7% of Americans are infected with giardia from all sources, wilderness and otherwise, although as few as 5% of an infected population may develop symptoms. It is mainly spread by fecal-oral or food-borne transmission. More than 34,000 cases were reported to state health departments in 1991, of which 19 outbreaks were waterborne, and two affected backpackers or campers.

A meta-analysis was performed, with an initial screening of 104 articles, in which nine met inclusion criteria for epidemiological analysis. Of the nine articles that were analyzed, neither of two case reports (report of the diagnosis, treatment, and follow-up of an individual patient) met the criteria of the Centers for Disease Control for waterborne disease outbreak. Two "prospective" studies (data on subjects who were followed forward in time) showed no significant association of backcountry water with infection. Of four studies that included control groups, none showed a significant relationship between backcountry water and infection. The conclusion was that North American wilderness waters are not a source of giardiasis.

Degree of risk

The risk of acquiring diarrhea in the wilderness arises from inadvertent ingestion of pathogens. Studies have been done to estimate diarrhea rates of wilderness travelers but for the most part they have either focused on only one pathogen, giardia lamblia, or provided scant data. A notable exception is a study of Appalachian Trail hikers.

Appalachian Trail Study

An epidemiological study of 280 long-distance hikers who each logged an average 139 days on the Appalachian Trail found that diarrhea was experienced by 56% of the cohort. The occurrence of diarrhea was positively associated with the duration of exposure in the wilderness. The diarrhea rate was reduced among those who either consistently treated their drinking water or had good personal hygiene.

Those who consistently treated their water had a diarrhea rate of 45% compared to 69% for those who did so inconsistently. The worst diarrhea rate of 86% was among those who drank untreated surface water (streams or ponds) more than several times a week.

Those who washed their hands with soap and water routinely after defecation had a 36% diarrhea rate compared to 59% for those who didn't.

Other Studies

Studies of shorter duration hikes resulted in a lower rate of infection or illness, which is expected because of less exposure. In one study, an illness rate of 3-5% was found.. Another study of backpackers in California found a Giardia infection rate of 5.7% but no symptomatic giardiasis. An additional 16.7% of subjects in the California study developed mild gastrointestinal illness, but no Giardia infection.

In a separate project at Grand Teton National Park, visitors suffering from active gastrointestinal complaints were invited to a free clinic. Of 178 cases tested, Campylobacter was the most common agent isolated at 28%, followed by Giardia at 8%. Salmonella and Shigella were not isolated and 69% of subjects had no identifiable pathogen.

In a 1991 giardiasis survey of 48 state health departments in the United States, 34,348 cases were reported. Of these, 19 were attributed to contaminated drinking water and 2 were reported among campers and backpackers.

Ingesting 10 – 25 Giardia cysts results in a 33% risk of detectable cysts in stools, and a significantly smaller risk of symptomatic giardiasis. Between 0.108 and 0.003 Giardia cysts per liter of water were measured in a 1984 survey of 18 backcountry sites in California's Sierra Nevada. The same survey detected no Giardia at 66 additional sites. Another survey completed in 1990 of three Sierra Nevada sites on 10 different dates, found concentrations between 0.0 and 0.62 cysts per liter. An additional survey by Backpacker Magazine of several backcountry sites was completed in 2003. The highest concentration that survey found was 1.5 Giardia cysts per liter. Drinking seven liters of such water may result in a minimum infective dose.

Symptoms

The incubation period for giardiasis averages about 14 days and that of cryptosporidiosis about seven days. Certain other bacterial and viral agents have shorter incubation periods, although hepatitis may take weeks to manifest itself. The onset usually occurs within the first week of return from the field, but may also occur at any time while hiking.

Most cases begin abruptly and usually result in increased frequency, volume, and weight of stool. Typically, a hiker experiences at least four to five loose or watery bowel movements each day. Other commonly associated symptoms are nausea, vomiting, abdominal cramping, bloating, low fever, urgency, and malaise, and usually the appetite is affected. The condition is much more serious if there is blood or mucus in stools, abdominal pain, or high fever. Dehydration is a possibility. Life-threatening illness coming from WD is extremely rare.

Treatment

WD is typically self-limited, generally resolving without specific treatment. Oral rehydration therapy with rehydration salts is often beneficial to replace lost fluids and electrolytes. Clear, disinfected water or other liquids are routinely recommended.

Hikers who develop three or more loose stools in a 24-hour period — especially if associated with nausea, vomiting, abdominal cramps, fever, or blood in stools — should be treated by a doctor and may benefit from antibiotics, usually given for 3–5 days. Alternately, a single dose azithromycin or levofloxacin may be prescribed. If diarrhea persists despite therapy, travelers should be evaluated and treated for possible parasitic infection.

There is no effective antibiotic against Cryptosporidium, which can be quite dangerous to patients with compromised immune systems.

Prevention

Since WD can be caused by fecal-oral transmission, contaminated water, and contaminated food, prevention methods should address these causes. Also it was found that on very long trips, taking multivitamins was associated with a reduction of WD.

The risk of fecal-oral transmission of pathogens can be reduced by good hygiene. This includes: washing hands after urination and defecation; and washing eating utensils with warm soapy water. Additionally a three-bowl system can be used for washing eating utensils.

Authoritative guidelines caution that safety judgments cannot reliably be made based on the mere appearances of a water source. One key to prevention is therefore various filters and chemical treatments. (see Portable water purification). The choice depends upon the number of people involved, space and weight considerations, the quality of available water, personal taste and preferences, and fuel availability. If Giardia lamblia is an uncommon isolate and WAD (wilderness-acquired diarrhea) is infrequent, then it may not be cost effective to recommend filtering for recreationalists involved in short-duration trips. Careful attention to personal hygiene can help prevent the spread of infection.

In a study of long-distance backpacking, it was found that water filters were used more consistently than chemical disinfectants. Inconsistent use of iodine or chlorine may be due to disagreeable taste, extended treatment time or treatment complexity due to water temperature and turbidity.

Because methods based on halogens, such as iodine and chlorine, do not kill Cryptosporidium, and because filtration misses some viruses, the best protection may require a two-step process of either filtration or coagulation-flocculation, followed by halogenation. Boiling is effective in all situations, but won't improve the water's taste.

Iodine resins, if combined with microfiltration to remove resistant cysts, are also a viable single-step process, but may not be effective under all conditions. New one-step techniques using chlorine dioxide, ozone, and UV radiation may prove effective, but still require validation.

Ultraviolet (UV) light for water disinfection is well established and widely used for large applications, like municipal water systems. A small portable UV device, called a Steri-pen, is now available for hikers. According to the manufacturer, it meets standards set forth in the U.S. EPA Guide Standard and Protocol for Testing Microbiological Water Purifiers.

In summary, both careful attention to personal hygiene and water treatment have been shown to be important for preventing wilderness diarrhea.

Water disinfection

Two standard textbooks on backcountry medical issues promote water disinfection as a key means of preventing infection. Various commercial water treatment devices are described in detail, and most infectious diarrhea acquired in the U.S. wilderness is considered to be from water-borne pathogens, and effective prevention is therefore thought to require treatment of drinking water as well as proper sanitiation.

Drinking untreated water is something like Russian roulette. Giardia in wilderness water sources may probably not be as prevalent as once believed but it's still present. If a wilderness visitor is confident of untainted alpine water, it's probably safe to drink it untreated, but in areas with significant human or animal activity, treatment is critical in prevention.

Contamination of U.S. backcountry water sources is widespread and disinfection is necessary but exaggerated concern has been raised about the issue. An example is an alleged case where Government agencies have filtered hundreds of gallons of water from wilderness streams, found one or two organisms (far less than enough to be infective), and erected garish signs proclaiming the water hazardous.

See also

References

  • Backer, Howard D. (2007). "Chapter 61: Field Water Disinfection". In Auerbach, Paul S. ed. (ed.). Wilderness Medicine (5th edition ed.). Philadelphia, PA: Mosby Elsevier. pp. 1368–1417. {{cite book}}: |edition= has extra text (help); |editor= has generic name (help); Cite has empty unknown parameter: |coauthors= (help)

Footnotes

  1. ^ Zell SC (1992). "Epidemiology of Wilderness-acquired Diarrhea: Implications for Prevention and Treatment" (PDF). J Wilderness Med. 3 (3): 241–9.
  2. ^ Hargreaves JS (2006). "Laboratory evaluation of the 3-bowl system used for washing-up eating utensils in the field". Wilderness Environ Med. 17 (2): 94–102. PMID 16805145. Diarrhea is a common illness of wilderness travelers, occurring in about one third of expedition participants and participants on wilderness recreation courses. The incidence of diarrhea may be as high as 74% on adventure trips. …Wilderness diarrhea is not caused solely by waterborne pathogens, … poor hygiene, with fecal-oral transmission, is also a contributing factor
  3. (Backer 2007, p. 1374)
  4. (Backer 2007, p. 1369)
  5. Prepared by Federal-Provincial-Territorial Committee on Drinking Water of the Federal-Provincial-Territorial Committee on Health and the Environment (2004) (2004), "Protozoa: Giardia and Cryptosporidium" (PDF), Guidelines for Canadian Drinking Water Quality: Supporting Documentation, Health Canada, retrieved 2008-08-07 {{citation}}: Cite has empty unknown parameters: |coeditors= and |coauthors= (help)CS1 maint: numeric names: authors list (link)
  6. Dickens DL, DuPont HL, Johnson PC (1985). "Survival of bacterial enteropathogens in the ice of popular drinks". JAMA. 253 (21): 3141–3. PMID 3889393. {{cite journal}}: Unknown parameter |month= ignored (help)CS1 maint: multiple names: authors list (link)
  7. Backer H (2000). "In search of the perfect water treatment method". Wilderness Environ Med. 11 (1): 1–4. PMID 10731899.
  8. Gerba C, Rose J (1990). "Viruses in Source and Drinking Water". In McFeters, Gordon A. ed. (ed.). Drinking water microbiology: progress and recent developments. Berlin: Springer-Verlag. pp. pp 380-399. ISBN 0-387-97162-9. {{cite book}}: |editor= has generic name (help); |pages= has extra text (help)
  9. White, George W. (1992). The handbook of chlorination and alternative disinfectants (3rd edition ed.). New York: Van Nostrand Reinhold. ISBN 0-442-00693-4. {{cite book}}: |edition= has extra text (help)
  10. ^ Boulware DR, Forgey WW, Martin WJ 2nd (2003). "Medical Risks of Wilderness Hiking". Am J Med. 114 (4): 288–93. PMID 12681456.{{cite journal}}: CS1 maint: multiple names: authors list (link) CS1 maint: numeric names: authors list (link)
  11. ^ Boulware DR (2004). "Influence of Hygiene on Gastrointestinal Illness Among Wilderness Backpackers". J Travel Med. 11 (1): 27–33. PMID 14769284.
  12. Brody, Jane E. (1989). "HEALTH: Diagnostics; Test Unmasks a Parasitic Disease". NY Times. Retrieved 2008-08-07. {{cite news}}: Cite has empty unknown parameter: |coauthors= (help)
  13. ^ Rockwell, Robert L. (2003). "Giardia Lamblia and Giardiasis With Particular Attention to the Sierra Nevada". Peak Climbing Section, Loma Prieta Chapter, Sierra Club. Retrieved 2008-08-07.
  14. ^ Welch TR, Welch TP (1995). "Giardiasis as a threat to backpackers in the United States: a survey of state health departments". Wilderness Environ Med. 6 (2): 162–6. PMID 11995903. {{cite journal}}: Unknown parameter |month= ignored (help)
  15. Welch TP (2000). "Risk of giardiasis from consumption of wilderness water in North America: a systematic review of epidemiologic data". Int. J. Infect. Dis. 4 (2): 100–3. PMID 10737847.
  16. ^ Welch TR (2004). "Evidence-based medicine in the wilderness: the safety of backcountry water" (PDF). Wilderness Environ Med. 15 (4): 235–7. PMID 15636372.
  17. Zell, S. C. (1993). "Cyst acquisition rate for Giardia lamblia in backcountry travelers to Desolation Wilderness, Lake Tahoe". Journal of Wilderness Medicine. 4 (2): 147–54. {{cite journal}}: Unknown parameter |coauthors= ignored (|author= suggested) (help)
  18. Sanders JW, Frenck RW, Putnam SD; et al. (2007). "Azithromycin and loperamide are comparable to levofloxacin and loperamide for the treatment of traveler's diarrhea in United States military personnel in Turkey". Clin. Infect. Dis. 45 (3): 294–301. PMID 18688944. {{cite journal}}: Explicit use of et al. in: |author= (help); Unknown parameter |month= ignored (help)CS1 maint: multiple names: authors list (link)
  19. ^ Adachi, Javier A. (2007). "Infectious Diarrhea from Wilderness and Foreign Travel". In Paul S. Auerbach (ed.). Wilderness Medicine. p. 1418. {{cite encyclopedia}}: Unknown parameter |coauthors= ignored (|author= suggested) (help) Cite error: The named reference "Adachi2007" was defined multiple times with different content (see the help page).
  20. Backer H (2002). "Water disinfection for international and wilderness travelers". Clin. Infect. Dis. 34 (3): 355–64. PMID 11774083. {{cite journal}}: Unknown parameter |month= ignored (help)
  21. (Backer 2007, p. 1411)
  22. Wood, T. D. (2008). "Water: What Are the Risks?". REI.com. Retrieved 2008-08-07.
  23. Seattle, Washington: The Mountaineers Books, 5th edition, 2001
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