Free-ranging Rocky Mountain bighorn sheep and an outbreak of inflammatory bowel disease along the Clark Fork River in Plains, Montana.

2012·0.93 MB·English

by  Pierce, Ellen S.

Virulence3:6,546–550;October1,2012;G2012LandesBioscience
Free-ranging Rocky Mountain bighorn sheep
and an outbreak of inflammatory bowel disease
along the Clark Fork River in Plains, Montana
Ellen S. Pierce
Keywords: Mycobacterium avium paratuberculosis, inflammatory bowel disease, outbreak,
fecal-oral waterborne transmission, aerosolization
NineindividualswithulcerativecolitisorCrohndiseasegrewuporlivedinPlains,Montana,a1,200-personcommunity
adjacent to the Clark Fork River near herds of free ranging Rocky Mountain bighorn sheep. This inflammatory bowel
disease outbreak issimilar toothers that haveoccurred alongriverscontaminated by animalfeces.
Introduction combined prevalence rate of over 16,300/ movedtherebeforedevelopingsymptomsof
100,000.ThesethreeAmericaninflammat- IBD. Their average age at symptom onset
Overadecadeago,FredricksandRelman1 oryboweldisease(IBD)outbreaks,aswellas was22y,witharangefrom9to53y.The
proposed that the majority of so called particularly high rates of Crohn disease first case developed symptoms in 1995, the
“autoimmune” diseases such as ulcerative in Spokane, Washington in the US,6 last in 2008. Some of the cases lived in
colitis and Crohn disease (the two major Cardiff in Wales,7 Winnipeg, Manitoba in multiplehomesinPlains; Figure1 indicates
forms of inflammatory bowel disease) are Canada8,9 and Canterbury in New thehomethecasewaslivinginatthetimeof
actually infectious in etiology. They based Zealand9,10 have occurred in communities symptomonset.
theirproposalinpartonthepublicationin located near rivers, lakes and creeks whose As with previous outbreaks, the greatly
the medical literature of time-space “clus- surface waters are contaminated by dairy increased prevalence and incidence rates
ters,” which are groups of individuals, cattleand/ordomesticatedsheepfeces. support the idea of an infectious etiology.
whether related or not, who live near one Mycobacterium avium subspecies paratu- ThepointprevalencerateofIBDinPlains
another and develop a disease within a berculosis (MAP), the cause of a chronic is9/1,200,or750/100,000,almostdouble
relatively limited time period. gastrointestinal disease in dairy cattle, do- the normal prevalence rate in high incid-
Most published clusters are actually out- mestic sheep and otheranimalscalledJohne ence countries.4 Two of the Crohn cases
breaks, since “outbreak” refers to aggrega- (“Yo-knee”) disease,11 is excreted in an developedsymptomswithinathreemonth
tions of disease that are greater than infected animal’s feces and so is consistent period at most, for an incidence rate of
expected, while “clusters” are aggregations with the putative microorganism linked to two Crohn disease cases/1,200/3 mo,
that are not necessarily greater than previously reported IBD outbreaks. MAP is more than 75 times the “expected” rate
expected.2 In Mankato, Minnesota,3 seven the long-suspected cause of Crohn disease12 of 7.9 cases/100,000/year.4
of 285 contacted members of the Mankato andhasrecentlybeenproposedasthepossible Thefactthatthisandpreviouslyreported
WestHighSchoolclassof1981haveCrohn etiologicagentofulcerativecolitisaswell.13 IBDoutbreaksaswellasunusuallyhighrates
disease,an“extraordinary”prevalencerateof While previous IBD outbreaks have of Crohn disease have occurred near rivers,
2,400/100,000, in contrast to nearby beenlinkedtodairycattleand/ordomestic lakesandotherbodiesofwatercontaminated
Olmsted County, Minnesota’s prevalence sheep, the following is the first report of by a probably MAP-infected animal’s feces
rate of 174/100,000.4 In Forest, Virginia, an IBD outbreak associated with a wild suggeststhatapossiblerouteoftransmission
three of an estimated 60 individuals with animal, the free ranging Rocky Mountain ofMAPfromaninfectedanimaltohumans
Crohn disease or ulcerative colitis from a bighorn sheep. is indirect fecal-oral transmission via the
community of 8,006 developed Crohn inhalation of MAP-contaminated aeroso-
disease within a six month period, an lized water droplets. The inhalation of
incidenceratealmost50timestheexpected Findings and Discussion MAP-contaminated water droplets as a
rate.2InNorthport,Washingtonareported5 possible route of transmission of MAP
54 individuals from a community of 330 ThesevenCrohndiseaseandtwoulcerative from an infected animal’s feces to humans
have ulcerative colitis or Crohn disease, a colitis cases were either born in Plains or was first proposed by Hermon-Taylor and
Correspondenceto:EllenS.Pierce;Email:[email protected]
Submitted:07/30/12;Revised:09/07/12;Accepted:09/07/12
http://dx.doi.org/10.4161/viru.22121
546 Virulence Volume3Issue6
LETTERTOTHEEDITOR
Figure1. Mapofthe1995–2008Plains,MontanaIBDoutbreak.NotethatallofthecasehomesareadjacenttotheClarkForkRiveroralongoneofits
tributaries.
www.landesbioscience.com Virulence 547
colleaguesin200014toexplaintheongoing In outdoor environments,25,26 precipita- Mountain bighorn sheep (Fig.1). Given
outbreak15ofCrohndiseaseinCardiff,and tion, the movement of water against the the small size ofthe nearby beef herd (less
in 2005 his group identified MAP in the creek, stream or riverbank, and playing, than 20 head) and the low prevalence of
water of the Taff River that runs through swimming or splashing about are some of MAPinfectioninbeefcattle,36thebighorn
that city.7 In Forest, Virginia, both the themeansbywhichairbubblesarecreated sheep are the likely source of MAP
creeks that are the source of MAP-con- within natural bodies of water. The air contaminating the Clark Fork River.
taminated aerosolized water droplets, and bubblesthen“scavenge”32MAPorganisms Such sheep are known to be infected with
the dairy cows whose manure is contam- in the bulk water and those concentrated MAP, to develop gastrointestinal disease
inating those creeks, are literally in several in the surface microlayer.23 The jet and and to shed MAP in their feces.37-40
of the Forest cases’ backyards.7 In film drops created by the air bubbles Although MAP can be identified in
Northport, Washington, 400–500 small bursting from the water’s surface again human and Bighorn sheep blood,40,41
dairieswerelocatedalongtheSheepCreek further concentrate MAP organisms.25,26 tissue37,38,42 and feces39,43 and in droplets
thatrunsthroughNorthportinthe1940s, MAP is a member of the MAI aerosolizedfromnaturalbodiesofwater,33
1950sand1960s,andthedairybarnswere (Mycobacterium avium intracellulare) com- the author suffers from catastrophic and
deliberatelyconstructed abovethecreekso plex of microorganisms, which are pref- irreversible complications of Crohn dis-
manure was deposited directly into it. erentially aerosolized from natural bodies ease44 and is unable to further evaluate
While direct fecal-oral, rather than inhala- of water in very high concentrations.33,34 this outbreak. Attempts by the families in
tion, is a major route of transmission of Symptom onset for four of the nine this and the Forest, Virginia IBD out-
MAPfromonedairyanimaltoanother,the cases occurred in the summer months of breaks to elicit evaluation and investiga-
inhalation of MAP-contaminated aeroso- June,JulyorAugust,andforanotherfour tionby state publichealth authorities and
lized water droplets has been proposed16 cases in the fall months of October or the United States’ Center for Disease
and is now an experimentally documen- November, similar to the pattern of Control and Prevention have been met
ted17sourceofbovineintestinalinfection. symptom onset of acute gastrointestinal with either silence or repeated and
The aerosolization of MAP-contami- illnesses following periods of both high pointed refusal. In private correspond-
nated water into small droplets capable of precipitation(spring)andlow(summer)in ence, MAP researchers have expressed
being inhaled and reaching human alveoli areas with heavy livestock and thus their frustration with the refusal of IBD-
occursintwosteps,whetherinoutdooror manure density.35 Precipitation is one of related organizations and government
indoor environments. Indoors, MAP’s the mechanisms for air bubble and water agencies to fund any research related to
resistance to chlorination,18 production of droplet production and MAP organism MAP. One prominent researcher has
and adherence to biofilms,19 and adher- concentration as described in step two alluded to this difficulty, having to resort
ence to both plastic and metallic water of the aerosolization process, perhaps to “donations from people suffering from
pipes20,21 causes it to be concentrated in accounting for the increase in cases in Crohn disease, their families and
potable or drinking water.21,22 Outdoors, the summer months following northern friends.”9 The publication of yet another
MAP’s extremely hydrophobic cell wall hemisphere spring rainfall. Evaporation of American IBD outbreak will hopefully
causesittofloattoandbeconcentratedat water from the Clark Fork River in the begin to encourage a reappraisal of public
the surface23 of a natural body of water hot summer months further concentrates health and research priorities.
such as a river, lake or creek.24 MAP in the already concentrated surface
Step two of the aerosolization process is microlayeroftheriver as described instep Acknowledgments
theactualaerosolizationofwaterintosmall one of the aerosolization process, perhaps The author is indebted to the cases and
jet25 and film26 drops that further concen- accounting for the increase in cases in the their families who brought their outbreak
trate MAP organisms. In indoor environ- fall months. to her attention and gave written permis-
ments, the exit of water from bathroom Dairycattlewerethefirstanimalspecies sion to be included in this report. She is
faucets27andshowerheads28andplayingin described with gastrointestinal disease also most grateful for the assistance of an
baths filled with water are some of the caused by MAP infection, and are the employeeoftheUnitedStatesDepartment
mechanismsofwaterdropletaerosolization. probable source of MAP in the Forest, of Agriculture’s office in Plains, Montana
ThehistoricallyhighratesofIBDinurban Virginia2 and Northport, Washington5 for the preparation of and information
as compared with rural environments29 as American IBD outbreaks. There are, contained in Figure1, and, as always, Dr
well as the reported association between however, no dairy cattle within a 70-mile Dodie Ruzicki and the librarians of
Crohn disease and domestic hygiene30 radius of Plains. MAP is known to cause Providence Sacred Heart Medical Center
might not be due to the lack of exposure gastrointestinal disease inawidevarietyof and Children’s Hospital’s Health Sciences
toavarietyofentericorganismsbutinstead animalspecies other thandairycattle.11 In LibraryinSpokane,WAforthereferences.
tospecific exposure tohighlyconcentrated this outbreak, the two possible sources of The author declares that no competing
doses of MAP spraying out of shower- MAP are a single small beef cattle herd, interests exist. The author received no
heads31andbathtubfaucets.27 andthreelargeherdsoffreerangingRocky funding for this case report.
548 Virulence Volume3Issue6
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