SlideShare a Scribd company logo
1 of 7
Download to read offline
Risks of Recreational Exposure to Waterborne
Pathogens Among Persons With HIV/AIDS
in Baltimore, Maryland
Cynthia C. McOliver, MPH, Hanna B. Lemerman, MPH, Ellen K. Silbergeld, PhD, Richard D. Moore, MD, and Thaddeus K. Graczyk, PhD
Persons with HIV/AIDS are at high risk for
increased morbidity and mortality associated
with a range of opportunistic infections, some
of which are caused by Cryptosporidium. Cryp-
tosporidium species are of particular public
health and medical importance because they
are prevalent in surface waters of the United
States,1–7
are efficiently transmitted via water,8
and can be consumed in foods contaminated by
fecal matter.9–11
Exposures to Cryptosporidium
are common in the US population,12
and past
studies have demonstrated that Cryptosporidium
infections significantly contribute to illness and
mortality in persons with HIV/AIDS.13–15
In the
1980s, Cryptosporidium was identified as a major
opportunistic pathogen.16–21
Infection continues
to be frequently diagnosed in persons with HIV/
AIDS.22–27
Before the advent of highly active
antiretroviral therapy, Cryptosporidium was a
relatively common opportunistic infection even
in developed countries.28,29
Cryptosporidiosis manifests as an acute gas-
troenteritis, accompanied by cramps, anorexia,
vomiting, abdominal pains, fever, and chills29
and by histological presentation of gastrointesti-
nal mucosal injury.30,31
Persons with AIDS who
become infected with this parasite are at in-
creased risk of developing chronic and often life-
threatening diarrhea, biliary tract diseases, pan-
creatitis, colitis, and chronic asymptomatic infec-
tion and recurrence. These developments are
especially likely in those who are severely
immunosuppressed (CD4 counts<150 cells/
mL).29,32–35
Infection is diagnosed by the pres-
ence of oocysts in unpreserved or preserved
stools.36
Histological and ultrastructural exami-
nation of biopsy material for different Crypto-
sporidium life stages, detection of Cryptosporid-
ium DNA and antigens, and identification of
species through molecular techniques can also
aid in diagnosis.36–38
Cryptosporidium species are enteric proto-
zoan organisms and are prevalent in US
watersheds, especially in urban waters.1,6,39
These parasites have natural hosts in domestic
and wild animals such as cattle (especially new-
born calves), horses, fish, and birds.5,40–42
These
parasites cause cryptosporidiosis by infecting and
damaging the cells of the small intestine and
other organs.13,41
For persons with HIV/AIDS,
increased risk for infection by Cryptosporidium
has been related to sexual practices such as
engaging in sexual intercourse within the past 2
years, having multiple partners during that time,
and engaging in anal intercourse.43
Use of spas
and saunas has also been identified as a risk
factor.43
In the United States, Cryptosporidium is the
most commonly identified pathogen in cases
of recreationally acquired gastroenteritis44
;
the majority of those affected are children. In-
creased risk of cryptosporidiosis in persons with
HIV/AIDS has been associated with swim-
ming.45,46
US residents make an estimated 360
million annual visits to recreational water venues
such as swimming pools, spas, and lakes; swim-
ming is the second most popular physical activity
in the country and the most popular among
children.47
Recreational swimming, even in highly
chlorinated water, carries a high risk of expo-
sure to enteric pathogens, including Crypto-
sporidium, Norovirus, Shigella, Escherichia coli,
and Giardia.48
Cryptosporidiosis and some
other enteric illnesses are seasonal, with spikes in
occurrence in the summer months from contact
with recreational water venues.49
Extreme pre-
cipitation50
and high ambient temperatures51
can
also affect patterns of disease outbreaks. Because
not all infections with Cryptosporidium lead to
apparent illness or symptoms, infected persons
may unknowingly transmit these pathogens to
others, such as household members and other
recreationists.12,52
Cryptosporidiosis from swim-
ming, wading, and splashing is prevalent in the
United States.44,46,53,54
Risks from the presence of pathogens in
waterways include (1) waterborne gastroenter-
itis and other recreational water illnesses in
anglers and other recreationists44,55–59
; (2)
transmission of pathogens to humans from
Objectives. We assessed the prevalence of recreational activities in the
waterways of Baltimore, MD, and the risk of exposure to Cryptosporidium
among persons with HIV/AIDS.
Methods. We studied patients at the Johns Hopkins Moore Outpatient AIDS
Clinic. We conducted oral interviews with a convenience sample of 157 HIV/AIDS
patients to ascertain the sites used for recreational water contact within
Baltimore waters and assess risk behaviors.
Results. Approximately 48% of respondents reported participating in recrea-
tional water activities (fishing, crabbing, boating, and swimming). Men and
women were almost equally likely to engage in recreational water activities
(53.3% versus 51.3%). Approximately 67% (105 of 157) ate their own catch or that
of friends or family members, and a majority (61%, or 46 of 75) of respondents
who reported recreational water contact reported consumption of their own catch.
Conclusions. Baltimoreans with HIV/AIDS are engaging in recreational water
activities in urban waters that may expose them to waterborne pathogens
and recreational water illnesses. Susceptible persons, such as patients with
HIV/AIDS, should be cautioned regarding potential microbial risks from recrea-
tional water contact with surface waters. (Am J Public Health. 2009;99:
1116–1122. doi:10.2105/AJPH.2008.151654)
RESEARCH AND PRACTICE
1116 | Research and Practice | Peer Reviewed | McOliver et al. American Journal of Public Health | June 2009, Vol 99, No. 6
caught seafood acting as fomites, or surface
carriers60
; (3) food-borne gastroenteritis from
consumption of raw or improperly cooked fish
and shellfish61,62
; and (4) hand-to-mouth trans-
mission of pathogens while eating, drinking, or
smoking during activities such as fishing and
crabbing.7
Recreational water activities in the Balti-
more, Maryland, area take place in Jones Falls
and Baltimore Harbor. These and other
waterways are used for angling, crabbing,
swimming, kayaking, and boating (including
paddle boating).7,63
In addition, Baltimore-area
residents often catch and consume fish and crabs
from the Baltimore Harbor and local waterways,
many of which are already highly contaminated
by persistent chemicals such as mercury and
polychlorinated biphenyls.64
These activities are
known to increase risks of exposure to water-
borne pathogens through direct contact with
contaminated waters or through contact with or
handling and consumption of caught seafood
(fish, crabs, oysters).7,65,66
To investigate the potential contribution of
recreational water contact to Cryptosporidium
exposures among persons with HIV/AIDS, we
carried out a cross-sectional study at the Johns
Hopkins Moore Outpatient AIDS Clinic. The
Baltimore metropolitan area has a high preva-
lence rate of HIV/AIDS among both men and
women,67
and its population makes intensive
recreational use of a contaminated watershed. In
addition, laboratory experiments have indicated
that crabs can become superficially contami-
nated by Cryptosporidium and transfer the path-
ogen to hands.68
Local anglers are at risk from
Cryptosporidium on wild-caught fish.7
Our objective was to address the risks of
exposure to Cryptosporidium for an urban
subpopulation, persons with HIV/AIDS, as a
result of recreational contact with Baltimore
waterways. We also assessed the patterns and
locations of recreational water activities in
Baltimore waters.
METHODS
The Hopkins AIDS Care Program and
Moore Outpatient AIDS Clinic serve persons
from the entire Baltimore metropolitan region;
as of December 2008, approximately 3000
patients were being actively followed. Of these
31.3% were women, 78.2% were African
American, 20.1% were non-Hispanic White,
and 1.6% were Hispanic. Fifty percent of these
patients were intravenous drug users, 22%
were men who have sex with men, and 25%
were heterosexual. These demographics are
reflective of the AIDS epidemic in Baltimore
and central Maryland.
Study Design
We identified a convenience sampling of
patients that represented the typical clientele of
the Moore clinic; our overall sample target was
150 patients. Our study was conducted between
July 10 and September 17, 2007. Consent was
obtained from respondents. The study was
facilitated by R.D.M., the director of the clinic, as
well as Vivian Zhao, the clinic administrator.
Patients were ineligible if they worked with farm
animals, had contact with animals from a petting
zoo, or had previously completed the survey. No
personal identifiers were collected during the
course of the study. In total, 157 patients con-
sented and fulfilled the criteria to participate in
the study.
We used an oral interview format validated
in a pilot project.69
The survey was adminis-
tered in the lobby of the clinic and in a down-
stairs office between 9 AM and 2 PM. Participants
were asked to respond to questions about their
place of residence, age, gender, ethnicity, loca-
tions of recreational water activities (specifically
crabbing), patterns of activity, consumption of
wild-caught fish and crabs from Baltimore
waterways, and hand-washing habits during
recreational water activities. A Batimore County
watershed map was used to facilitate location of
sites used for recretional water activities (Figure
1). They also reported current and recent recre-
ational water activity by month and frequency
and responded to questions about potential risk
factors for Cryptosporidium transmission such as
contact with diapered children, consumption of
untreated water, travel overseas, pet ownership,
and wild-animal contact.
Most responses were qualitative (yes, no, not
applicable). We used a categorical frequency
scale to quantify monthly recreational activity
(e.g., 0–4 times/mo). The term recent referred to
any event occurring with the previous month.
Respondents were compensated with a $10
store gift card upon completion of the survey.
Responses to survey questions were checked
off or handwritten on the survey by C.C.M. and
2 other survey administrators. Respondents
were also encouraged to comment on the
survey and to ask any questions they thought
were relevant.
Statistical Analyses
Data were entered into Microsoft Excel
200370
and analyzed with STATA version
9.2.71
We made statistical comparisons with the
Fisher exact test and c2
test. Statistical signifi-
cance was set at .05. We used the 2-sided t test
for means to assess difference in age by cate-
gories. We assessed group differences with the
binomial test of proportions and used nonmiss-
ing data for estimations.
RESULTS
Participants were predominantly African
American and evenly distributed between men
and women (Table1). The participation rate was
more than 90% among clinic patients who were
approached. Demographic characteristics and
risk exposure behaviors of the study population
are presented in Table1and Table 2. Because of
small numbers, racial/ethnic groups other than
African American and non-Hispanic White
TABLE 1—Race/Ethnicity and Gender
Comparisons Between Study
Participants (n=157) and Clinic
Patients (n=1830) of the Johns
Hopkins Moore Outpatient AIDS Clinic:
Baltimore, MD, 2007
Participants Clinic Patientsa
Race/ethnicity, %
African American 86.6 74
Non-Hispanic White 7 23
Biracial 3.2 . . .
Hispanic 1.3 2
Other 0.6 1
Missing 1.3 . . .
Gender, %
Men 51.3 65
Women 48 35
Transgender 0.7 . . .
Age, y, median (range) 47 (27–75) 41 (19–88)
Note. Ellipses indicate data were not available or not
collected.
a
Data were from 2003 to 2007.
RESEARCH AND PRACTICE
June 2009, Vol 99, No. 6 | American Journal of Public Health McOliver et al. | Peer Reviewed | Research and Practice | 1117
were collapsed into 1 category, other (Hispanic,
Asian, biracial, and African). There were
75 women, 80 men, and 1 transgendered per-
son. One respondent did not provide gender
information.
The mean age of the 152 participants whose
age was reported was 47.2 68.4 years
(range=27–75 years). The median age was 47
years, with the age distribution slightly posi-
tively skewed (0.35). There was no difference
in age between respondents who engaged in
recreational water activities and those who did
not (P=.32). Ninety-five percent of the re-
spondents were 61 years or younger. Almost
half of the respondents (47.8%, or 75 persons)
TABLE 2—Participant Characteristics and Risk Behaviors, by Gender and Race/Ethnicity: Baltimore, MD, 2007
Gender Race/Ethnicity
Men (n=80) Women (n=75) African American (n=136) Non-Hispanic White (n=11) Other (n=8)
Age, y, mean 6SD (95% CI) 48.267.7 (46.5, 49.9) 46.168.9 (43.9, 48.1) 47.167.8 (45.8, 48.5) 4468.3 (37.6, 50.9) 51614.9 (38.5, 63.5)
Age, y, median (range) 49 (27–68) 45 (27–75) 47 (27–75) 48 (30–53) 50 (27–68)
Recreational water contact, No. (%)
Yes 41 (51.3) 40 (53.3) 71 (52.2) 5 (45.5) 5 (62.5)
No 39 (48.7) 35 (46.7) 65 (47.8) 6 (54.5) 3 (37.5)
Consumption of self-caught fish and crabs, No. (%)
Yes 24 (30) 22 (29.3) 41 (30.1) 3 (27.3) 2 (25)
No 3 (3.8) 3 (4) 4 (2.9) 2 (18.2) 0 (0)
Not applicablea
52 (65) 50 (66.7) 91 (66.9) 6 (54.5) 6 (75)
Missing 1 (1.25) 0 (0) 0 (0) 0 (0) 0 (0)
Consumption of others’ wild-caught fish and crabs
Yes 46 (57.5) 52 (69.3) 88 (64.7) 6 (54.5) 4 (50)
No 32 (40) 22 (29.3) 46 (33.8) 5 (45.5) 4 (50)
Missing 2 (2.5) 1 (1.4) 2 (1.5) 0 (0) 0 (0)
Handwashing during recreational activity, No. (%)
Yes 31 (38.8) 25 (33.3) 50 (36.8) 4 (36.4) 2 (25)
No 6 (7.5) 6 (8) 10 (7.4) 2 (18.2) 0 (0)
Not applicablea
41 (51.3) 40 (53.3) 72 (52.9) 5 (45.5) 5 (62.5)
Missing 2 (2.5) 4 (5.3) 4 (2.9) 0 (0) 1 (12.5)
Pets in home, No. (%)
Yes 29 (36.3) 29 (38.7) 51 (37.5) 5 (45.5) 2 (25)
No 49 (61.3) 44 (58.7) 84 (61.8) 4 (36.4) 6 (75)
Missing 2 (2.4) 2 (2.6) 1 (0.7) 2 (18.1) 0 (0)
Consumption of well water, No. (%)
Yes 4 (5) 4 (5.3) 7 (5.2) 1 (9.1) 0 (0)
No 74 (92.5) 70 (93.3) 128 (94.1) 9 (81.8) 8 (100)
Missing 2 (2.5) 1 (1.33) 1 (0.7) 1 (9.1) 0 (0)
Travel outside United States, No. (%)
Yes 1 (0.8) 1 (1.3) 1 (0.7) 0 (0) 1 (12.5)
No 77 (96.3) 73 (97.3) 134 (98.5) 10 (90.9) 7 (87.5)
Missing 2 (2.5) 1 (1.33) 1 (0.7) 1 (9.1) 0 (0)
Changing of baby diapers, No. (%)
Yes 13 (16.3) 26 (34.7) 34 (25) 2 (18.2) 3 (37.5)
No 65 (81.3) 47 (62.7) 101 (74.3) 7 (63.6) 5 (62.5)
Missing 2 (2.4) 2 (2.6) 1 (0.7) 2 (18.2) 0 (0)
Contact with wild animals, No. (%)
Yes 4 (5) 3 (4) 6 (4.4) 1 (9.1) 0 (0)
No 73 (91.3) 70 (93.3) 128 (94.1) 8 (72.7) 8 (100)
Missing 3 (3.7) 2 (2.7) 2 (1.5) 2 (18.2) 0 (0)
Note. CI=confidence interval. Totals across categories may not sum to total study population because of missing data.
a
Participant did not engage in this activity.
RESEARCH AND PRACTICE
1118 | Research and Practice | Peer Reviewed | McOliver et al. American Journal of Public Health | June 2009, Vol 99, No. 6
reportedsomeform of recreational wateractivity,
and 82 participants (52.2%) reported none.
Similar numbers of men and women engaged in
recreational water activity (39 and 35, respec-
tively), and similar numbers did not (41and 40).
The most common locations for reported
recreational water activity were the Baltimore
Harbor (Canton, Fells Point), Patapsco River
(Middle Branch Park, Harbor Hospital), and
Gunpowder River (Figure 2). These sites are
centrally located within the Baltimore County
watershed (Figure 1).72
Respondents gave mul-
tiple reasons for engaging in fishing and crab-
bing. The majority (n=75) reported that they
fished or crabbed for fun, recreation, and relax-
ation (68%) as well as for food or to supplement
diets (58.9%). Other reported reasons were
sharing caught fish and crabs (45%) and spend-
ing time with family or children (2.7%).
Among risk factors associated with Crypto-
sporidium infection and transmission, the most
commonly reported were changing baby dia-
pers (39 respondents, or 24.8%) and pets in
the home (58, or 36.9%). Eight respondents
(5.1%) reported well water consumption, 2
(1.3%) reported travel outside the United
States, and 7 (4.5%) reported contact with wild
animals (wild birds, raccoons, or deer). The
distribution of these risk factors by race/eth-
nicity and gender are shown in Table 2.
We estimated contact with wild-caught fish
and crabs by asking about consumption of fish
and crabs caught by others. Approximately
67% of participants (105 of 157) reported con-
sumption of their own catch or wild-caught fish
and crabs from friends or family members. A
majority (46 of 75, or 61%) of respondents who
reported recreational water contact ate their own
catch. Consumption of fish and crabs caught in
the wild by either friends or family members was
reported by approximately 80% (59 of 74) of
those who engaged in recreational water activity
and only 48% (38 of 79) of those who did not.
Respondents also provided data on their
frequency of recreational water activities (Ta-
ble 3), with the majority reporting taking part in
activities 1 to 4 times a month.
DISCUSSION
We found a high level of self-reported par-
ticipation in recreational water activity among
HIV/AIDS patients at an urban Baltimore
outpatient clinic. Respondents reported activi-
ties such as fishing, crabbing, boating, and
swimming, as well as consumption of their own
catch and wild-caught fish and crabs supplied
by friends or family members. Our study sam-
ple was representative of the larger clinic pop-
ulation; therefore, our findings could be gen-
eralized to the larger Moore Clinic patient
population, despite our small sample size.
These findings are relevant to public health in
light of recent findings of viable Cryptosporid-
ium in many of the waters commonly used by
our respondents and others in the region for
recreational water activities.7,67,73
To our knowledge, ours is the first study to
describe recreational water contact among
persons with HIV/AIDS. Another strength of
our study was an excellent participation rate of
more than 90% of clinic patients who were
approached for participation.
Limitations
Our study had several limitations. Respon-
dents were asked to recall recreational activi-
ties, including locations, activities, frequency,
and specific months of participation, a method
of data collection with a potential for recall bias.
Some participants could not describe or iden-
tify the specific sites they used for recreational
activities. Efforts were made to fill in these data
gaps with a Baltimore County watershed map
during the interview process.
Interviews took place in a clinical setting where
participants often had limited time to complete
surveys. Patients were free to leave at any point
during the interview to go to their appointments;
most returned to complete their surveys. Some
incomplete data collection and nonresponses
resulted from time restraints on both patients and
interviewers (who could not always review all
questions or double-check responses).
Language barriers may have prevented en-
rollment and participation of patients in the
study. However, fewer than 5 patients were
identified as having a language barrier. Some
respondents may have completed multiple
surveys during the course of the study period,
because no personal identifiers were collected.
However, efforts were made to limit participa-
tion to persons who reported not previously
completing our survey, and we used an ex-
emption form to exclude these persons.
Source. Baltimore County Environmental Protection and Resource Management Watershed Management Program.73
FIGURE 1—Map of Baltimore County watershed used during survey to identify sites of
recreational water activity: 2007.
RESEARCH AND PRACTICE
June 2009, Vol 99, No. 6 | American Journal of Public Health McOliver et al. | Peer Reviewed | Research and Practice | 1119
Conclusions
We found that persons with HIV/AIDS, a
subset of the urban population, frequently take
part in recreational water activities in the
Baltimore area. Unfortunately, this watershed
is contaminated by Cryptosporidium and other
enteric pathogens of concern for both healthy
and immunocompromised individuals.
This population is engaging in fishing and
crabbing not only for fun, sport, or recreation
but also for diet supplementation and subsis-
tence. Contact with fish and crabs during
preparation and handling may expose individ-
uals to Cryptosporidium via contamination of
hands, preparation and cooking surfaces, and
equipment. In addition, exposure may occur
from consumption of improperly cooked fish
and crabs. These recreational sites lack hand-
washing facilities, a concern because food
and beverages are commonly consumed there.
Pathogens such as Cryptosporidium are not
routinely monitored in surface waters and are
not included in existing fish advisories. As a
result, the general public, including immuno-
compromised and other highly susceptible
persons, are not aware of the risks of exposure
and infection posed by pathogens. This lack of
communication is a major public health failure,
not limited to but of particular concern for
persons who are immunocompromised. Regu-
latory agencies, watershed associations, and
others involved in recreational water programs
should inform themselves about the effect of
infectious pathogens in recreational waters and
develop routine surveillance, monitoring, and
notification systems to ensure the safety of
urban waters.
Physicians and other caregivers for per-
sons with HIV/AIDS should incorporate
questions about recreational water activities,
foreign travel, and other activities with po-
tential for pathogen exposure during routine
intake procedures and follow-up of patients
with acute or chronic gastroenteritis. In
addition, patients who are at high risk for
noncompliance with antiretroviral therapy
regimens or who are not receiving these
therapies should be counseled on the risk
factors for exposure and infection by Cryp-
tosporidium.
Future national health surveys should in-
clude questions about potential sources of
exposure to Cryptosporidium, as well as
about residence, foreign travel, and recrea-
tional water activities (including chlorinated
water venues such as swimming pools) to
accurately characterize the populations at
risk. j
About the Authors
At the time of the study, Cynthia C. McOliver, Ellen K.
Silbergeld, and Thaddeus K. Graczyk were with the
Bloomberg School of Public Health, Johns Hopkins Uni-
versity, Baltimore, MD. Hanna B. Lemerman was a student
at the School of Medicine, Johns Hopkins University,
Baltimore. Richard D. Moore is with the HIV Clinic, Johns
Hopkins University, Baltimore.
Request for reprints should be sent to Cynthia C.
McOliver, 615 N Wolfe St, Room W6005, Johns Hopkins
Bloomberg School of Public Health, Baltimore, MD 21205
(e-mail: cmcolive@jhsph.edu).
This article was accepted December 11, 2008.
Contributors
C.C. McOliver conducted the research, analyzed the
data, and drafted the article. H. B. Lemerman admin-
istered surveys, performed quality control of the sur-
vey data, checked references for the article, modified
tables, and edited drafts of the article. E. K. Silbergeld
and T. K. Graczyk designed the study and assisted with
the revision of the article. E. Silbergeld also reviewed
the study materials and helped develop the questions
for the survey. R. D. Moore facilitated participant re-
cruitment and clinic staff assistance and reviewed the
article.
Acknowledgments
This research was supported by a Johns Hopkins Center
for a Livable Future Faculty and Student Innovation
Grant (no. 1602030055).
The authors thank the staff and patients of the Moore
Clinic for participating in this research. We are especially
thankful for the advice and support of Cynthia Sears of
the Divisions of Infectious Diseases and Gastroenterology
at Johns Hopkins School of Medicine. Special thanks to
Preety Gadhoke and Carol Resnick for their assistance
with developing the surveys, Sean Evans for assistance
with administering the surveys, Ruth Quinn and Ellen
Wells for beta testing the surveys, and Marisa Caliri for
her untiring assistance with data entry and quality
assurance.
Human Participant Protection
All study protocols and materials received approval from
the Johns Hopkins School of Public Health committee on
human research.
Note. The number reporting activities includes multiple sites and activities.
FIGURE 2—Recreational water sites used by patients surveyed at the Johns Hopkins Moore
Outpatient AIDS Clinic, Baltimore, MD: 2007.
RESEARCH AND PRACTICE
1120 | Research and Practice | Peer Reviewed | McOliver et al. American Journal of Public Health | June 2009, Vol 99, No. 6
References
1. LeChevallier MW, Norton WD, Lee RG. Occurrence
of Giardia and Cryptosporidium spp. in surface water
supplies. Appl Environ Microbiol. 1991;57(9);2610–
2616.
2. Lisle JT, Rose JB. Cryptosporidium contamination of
water in the USA and UK: a mini-review. Aqua. 1995;
44(3);103–117.
3. Rose J, Lisle J, LeChevallier M. Waterborne crypto-
sporidiosis: incidence, outbreaks. treatment strategies.
Fayer R, ed. Cryptosporidium and Cryptosporidiosis. New
York, NY: CRC Press:1997:251.
4. Todd S, Phillips M, Marchin G, Upton S. Cryptospo-
ridium Giardia in surface waters in and around Manhat-
tan, Kansas. Trans Kans Acad Sci. 1991;94(3/4);
101–106.
5. Xiao L, Singh A, Limor J, Graczyk T, Gradus S, Lal A.
Molecular characterization of Cryptosporidium oocysts in
samples of raw surface water and wastewater. Appl
Environ Microbiol. 2001;67(3);1097–1101.
6. Arnone R, Walling J. Waterborne pathogens in
urban watersheds. J Water Health. 2007;5(1);149–162.
7. Roberts J, Silbergeld E, Graczyk T. A probabilistic
risk assessment of Cryptosporidium exposure among
baltimore urban anglers. J Toxicol Environ Health A.
2007;70(18);1568–1576.
8. Fayer R. Cryptosporidium: a water-borne zoonotic
parasite. Vet Parasitol. 2004;126(1-2);37–56.
9. Centers for Disease Control and Prevention. Food-
borne outbreak of cryptosporidiosis—Spokane, Wash-
ington, 1997. MMWR Morb Mortal Wkly Rep. 1998;
47(27);565–567.
10. Yoshida H, Matsuo M, Miyoshi T, et al. An outbreak
of cryptosporidiosis suspected to be related to contami-
nated food, October 2006, Sakai City. Jpn J Infect Dis.
2007;60(6);405–407.
11. Vojdani J, Beuchat L, Tauxe R. Juice-associated
outbreaks of human illness in the United States, 1995
through 2005. J Food Prot. 2008;71(2);356–364.
12. Frost F, Muller T, Calderon R, Craun G. Analysis of
serological responses to Cryptosporidium antigen among
NHANES III participants. Ann Epidemiol. 2004;14(7);
473–478.
13. Chen X-M, Keithly J, Paya C, LaRusso N. Crypto-
sporidiosis. N Engl J Med. 2002;346(22);1723–1731.
14. Frost F, Muller T, Gunther F, Lockwood W, Calderon
R. Serological evidence of endemic waterborne Crypto-
sporidium infections. Ann Epidemiol. 2002;12(4);222–
227.
15. Hlavsa MC, Watson JC, Beach MJ. Cryptosporidiosis
surveillance—United States 1999–2002. MMWR Sur-
veill Summ. 2005;54(1);1–8.
16. Centers for Disease Control and Prevention. Cryp-
tosporidiosisassessment of chemotherapy of males with
acquired immune deficiency syndrome(AIDS). MMWR
Morb Mortal Wkly Rep. 1982;31:589–592.
17. Jokipii L, Pohjola S, Jokipii AM. Cryptosporidium: a
frequent finding in patients with gastrointestinal symp-
toms. Lancet. 1983;2:358–361.
18. Current W, Reese N, Ernst J, Bailey WS, Heyman M,
Weinstein W. Human cryptosporidiosis in immunocom-
petent and immunodeficient persons. Studies of an out-
break and experimental transmission. N Engl J Med.
1983;308(21);1252–1257.
19. Forgacs P, Tarshis A, Ma P, et al. Intestinal and
bronchial cryptosporidiosis in an immunodeficient ho-
mosexual man. Ann Intern Med. 1983;99(6);793–794.
20. Soave R, Danner R, Honig C, et al. Cryptosporidiosis
in homosexual men. Ann Intern Med. 1984;100(4);504–
511.
21. Casemore D, Sands R, Curry A. Cryptosporidium
species a ‘‘new’’ human pathogen. J Clin Pathol. 1985;
38(12);1321–1336.
22. Brandonisio O, Maggi P, Panaro M, Bramante L, Di
Coste A, Angarano G. Prevalence of cryptosporidiosis in
HIV-infected patients with diarrhoeal illness. Eur J Epi-
demiol. 1993;9(2);190–194.
23. Sandhu S, Priest J, Lammie P, et al. The natural
history of antibody responses to Cryptosporidium para-
sites in men at high risk of HIV infection. J Infect Dis.
2006;194(10);1428–1437.
24. Raccurt C, Brasseur P, Verdier R, et al. Human
cryptosporidiosis and Cryptosporidium spp. in Haiti. Trop
Med Int Health. 2006;11(6);929–934.
25. de Oliveira-Silva M, de Oliveira L, Resende J, et al.
Seasonal profile and level of CD4+ lymphocytes in the
occurrence of cryptosporidiosis and cystoisosporidiosis in
HIV/AIDS patients in the Triaˆngulo Mineiro region
Brazil. Rev Soc Bras Med Trop Scielo. 2007;40:512–515.
26. Rao Ajjampur SS, Asirvatham JR, Muthusamy D,
et al. Clinical features and risk factors associated with
cryptosporidiosis in HIV infected adults in India. Indian J
Med Res. 2007;126:553–557.
27. Gatei W, Barrett D, Lindo J, Eldemire-Shearer D,
Cama V, Xiao L. Unique Cryptosporidium population in
HIV-infected persons, Jamaica. Emerg Infect Dis. 2008;
14(5);841–843.
28. Manabe Y, Clark D, Moore R, et al. Cryptosporidiosis
in patients with AIDS: correlates of disease and survival.
Clin Infect Dis. 1998;27(3);536–542.
29. Hunter PR, Nichols G. Epidemiology and clinical
features of Cryptosporidium infection in immunocompro-
mised patients. Clin Microbiol Rev. 2002;15(1);145–154.
TABLE 3—Study Participants’ Frequency of Participating in Recreational Water Activities, by
Location: Baltimore, MD, 2007
Activity Patapsco River Baltimore Harbor Gunpowder River Back River
Fishing, times/mo
1–4 21 8 11 7
5–8 4 0 0 0
‡9 1 1 0 0
Missing 5 1 0 1
Not applicablea
44 65 64 67
Total 75 75 75 75
Crabbing
1–4 15 9 6 4
5–8 2 0 0 0
‡9 1 1 0 0
Missing 3 1 0 1
Not applicablea
54 64 69 70
Total 75 75 75 75
Boating
1–4 7 26 4 2
5–8 2 0 0 0
‡9 0 1 0 0
Missing 0 5 0 0
Not applicablea
66 43 71 73
Total 75 75 75 75
Swimming
1–4 5 6 14 2
5–8 1 1 0 0
‡9 0 0 0 0
Missing 1 1 2 0
Not applicablea
68 67 59 63
Total 75 75 75 65
Note. These 4 sites were the most frequently used by the 75 patients reporting recreational water contact.
a
Participant did not engage in this activity at this site.
RESEARCH AND PRACTICE
June 2009, Vol 99, No. 6 | American Journal of Public Health McOliver et al. | Peer Reviewed | Research and Practice | 1121
30. Lumadue J, Manabe Y, Moore R, Belitsos P, Sears C,
Clark D. A clinicopathologic analysis of AIDS-related
cryptosporidiosis. AIDS. 1998;12(18):2459–2466.
31. Walker-Smith J. Post-infective diarrhea. Curr Opin
Infect Dis. 2001;14(5):567–571.
32. Forbes A, Blanshard C, Gazzard B. Natural history of
AIDS related sclerosing cholangitis: a study of 20 cases.
Gut. 1993;34:116–121.
33. Lo´pez-Ve´lez R, Tarazona R, Garcia C, et al. Intestinal
and extraintestinal cryptosporidiosis in AIDS patients.
Eur J Clin Microbiol Infect Dis. 1995;14(8):677–681.
34. Vakil N, Schwartz S, Buggy B, et al. Biliary crypto-
sporidiosis in HIV-infected people after the waterborne
outbreak of cryptosporidiosis in Milwaukee. N Engl J Med.
1996;334(1):19–23.
35. Muthusamy D, Rao S, Ramani S, et al. Multilocus
genotyping of Cryptosporidium sp. isolates from human
immunodeficiency virus-infected individuals in South
India. J Clin Microbiol. 2006;44(2):632–634.
36. Smith H. Diagnostics. In:Fayer R, Xiao L eds. Cryp-
tosporidium and Cryptosporidiosis. 2nd ed. Boca Raton,
FL: CRC Press; 2008:173–207.
37. Xiao L, Ryan UM. Molecular epidemiology. Fayer R,
Xiao L, eds. Cryptosporidium and Cryptosporidiosis. 2nd
ed. Boca Raton, FL: CRC Press; 2008:119–164.
38. Fayer R. General biology. In: Fayer R, Xiao L, eds.
Cryptosporidium and Cryptosporidiosis. Boca Raton, FL:
CRC Press; 2008:1–43.
39. States S, Stadterman K, Ammon L, et al. Protozoa in
river water: sources, occurrence, and treatment. J Am
Water Works Assoc. 1997;89(9):74–83.
40. Casemore D. Human cryptosporidiosis. In: Reeves
DS, Geddes AM, eds. Recent Advances in Infection.
Edinburgh, Scotland: Churchill Livingstone:1998:209–
236.
41. Fayer R, Morgan U, Upton S. Epidemiology of
Cryptosporidium: transmission, detection and identifica-
tion. Int J Parasitol. 2000;30(12–13):1305–1322.
42. Caccio` S. Molecular epidemiology of human cryp-
tosporidiosis. Parassitologia. 2005;47(2):185–192.
43. Caputo C, Forbes A, Frost F, et al. Determinants of
antibodies to Cryptosporidium infection among gay and
bisexual men with HIV infection. Epidemiol Infect.
1999;122(2):291–297.
44. Centers for Disease Control and Prevention. Cryp-
tosporidiosis outbreaks associated with recreational wa-
ter use—five states, 2006. MMWR Morb Mortal Wkly
Rep. 2007;56(29):729–732.
45. Inungu J, Morse A, Gordon C. Risk factors, season-
ality, and trends of cryptosporidiosis among patients
infected with human immunodeficiency virus. Am J Trop
Med Hyg. 2000;62(3):384–387.
46. Causer LM, Handzel T, Welch P, et al. An outbreak
of Cryptosporidium hominis infection at an Illinois recre-
ational waterpark. Epidemiol Infect. 2006;134:147–156.
47. US Department of the Interior, Fish and Wildlife
Service and US Department of Commerce, US Census
Bureau. 2001 National survey of fishing, hunting, and
wildlife-associated recreation. Available at: http://
www.census.gov/prod/2002pubs/FHW01.pdf.
Accessed October 14, 2008.
48. Centers for Disease Control and Prevention. Notice
to Readers: National Recreational Water Illness Pre-
vention Week—May 19–25, 2008. MMWR. 2008;
57(19):528–529. Available at: http://www.cdc.gov/
mmwr/preview/mmwrhtml/mm5719a8.htm?s_cid=
mm5719a8_e Accessed January 16, 2009.
49. Dziuban EJ, Liang JL, Craun GF, et al. Surveillance
for waterborne disease and outbreaks associated with
recreational water—United States, 2003–2004. MMWR
Surveill Summ. 2006;55(12):1–20.
50. Curriero F, Patz J, Rose J, Lele S. The association
between extreme precipitation and waterborne disease
outbreaks in the United States, 1948–1994. Am J Public
Health. 2001;91(8):1194–1199.
51. Naumova E, Jagai JS, Matyas B, DeMaria A Jr,
MacNeill IB, Griffiths JK. Seasonality in six enterically
transmitted diseases and ambient temperature. Epidemiol
Infect. 2007;135(2):281–292.
52. Peng M, Xiao L, Freeman A, et al. Genetic poly-
morphism among Cryptosporidium parvum isolates: evi-
dence of two distinct human transmission cycles. Emerg
Infect Dis. 1997;3(4):567–573.
53. Sorvillo F, Fujioka K, Nahlen B, Tormey M,
Kebabjian R, Mascola L. Swimming-associated crypto-
sporidiosis. Am J Public Health. 1992;82(5):742–744.
54. Craun G, Calderon R, Craun M. Outbreaks associ-
ated with recreational water in the United States. Int J
Environ Health Res. 2005;15(4):243–262.
55. Roy S, DeLong S, Stenzel S, et al. Risk factors for
sporadic Cryptosporidiosis among immunocompetent
persons in the United States from 1999 to 2001. J Clin
Microbiol. 2004;42(7):2944–2951.
56. Bergsson G, Agerberth B, Jo¨rnvall H, Gudmundsson
GH. Isolation and identification of antimicrobial compo-
nents from the epidermal mucus of Atlantic cod (Gadus
morhua). FEBS J. 2005;272(19):4960–4969.
57. Wade T, Calderon R, Sams E, et al. Rapidly mea-
sured indicators of recreational water quality are pre-
dictive of swimming-associated gastrointestinal illness.
Environ Health Perspect. 2006;114(1):24–28.
58. Why are river recreationalists most at risk for
development of waterborne infectious diseases: how can
clinicians improve surveillance? A national problem. J
Occup Environ Med. 2007;49(1):104–105.
59. Anne Arundel County, MD, Department of Health.
Water quality and swimming or fishing in Anne Arundel
County rivers and creeks. 2008. Available at: http://
www.aahealth.org/a2z.asp?id=110. Accessed October
14, 2008.
60. Anne Arundel County, MD, Department of Health.
Mycobacterium marinum. 2006. Available at: http://
www.aahealth.org/a2z.asp?id=191. Accessed October
14, 2008.
61. Graczyk T, Schwab K. Foodborne infections vec-
tored by molluscan shellfish. Curr Gastroenterol Rep.
2000;2(4):305–309.
62. Su Y-C, Liu C. Vibrio parahaemolyticus: a concern of
seafood safety. Food Microbiol. 2007;24(6):549–558.
63. Davison SG, Merwin JG, Capper J, Power G, Shivers
F. Chesapeake (Bay) Waters: Four Centuries of Controversy,
Concern, and Legislation. 2nd ed. Centreville, MD: Tide-
water Publishers; 1997.
64. Gibson JC, McClafferty JA. Chesapeake Bay Angler
Interviews: Identifying Populations at Risk for Consuming
Contaminated Fish in Three Regions of Concern. Blacks-
burg, VA: Virginia Polytechnic Institute and State Uni-
versity; 2005. Final Report CMI-HDD-05-01. Available
at: http://www.nbii.gov/images/uploaded/155729_
1170437308921_2004_ConsumptionAdvisories_
AnglerSurvey.pdf. Accessed January 21, 2009.
65. Graczyk T, Cranfield M, Fayer R. Recovery of
waterborne oocysts of Cryptosporidium from water sam-
ples by the membrane-filter dissolution method. Parasitol
Res. 1997;83(2):121–125.
66. Graczyk T, Fayer R, Trout J, et al. Susceptibility of
the Chesapeake Bay to environmental contamination
with Cryptosporidium parvum. Environ Res. 2000b;
82(2):106–112.
67. Maryland Department of Health and Mental Hy-
giene, AIDS Administration. Maryland HIV/AIDS fourth
quarter 2007—data reported through December 31,
2007. Available at: http://www.dhmh.state.md.us/AIDS/
Data&Statistics/NewMDQtrEpi.pdf. Accessed October
14, 2008.
68. Graczyk T, McOliver C, Silbergeld EK, Tamang L,
Roberts JD. Risk of handling as a route of exposure to
infectious waterborne Cryptosporidium parvum oocysts
via Atlantic blue crabs (Callinectes sapidus). Appl Environ
Microbiol. 2007;73(12):4069–4070.
69. McOliver C, Graczyk TK, Silbergeld EK. Assessing
the risks of exposure to Cryptosporidium from recrea-
tional water activities in Baltimore, Maryland. 2008. In:
Eades RT, Neal JW, Lang TJ, Hunt KM, Pajak P, eds.
Urban and Community Fisheries Programs: Development,
Management, and Evaluation. Symposium 67. Bethesda,
MD: American Fisheries Society; 2008:165–174.
70. Microsoft Office Excel 2003 [computer program].
Redmond, WA: Microsoft Corp; 2003.
71. Intercooled STATA Statistical Software. 9th ed. Col-
lege Station, TX: STATA Corp; 2006.
72. Baltimore County Environmental Protection and
Resource Management Watershed Management Pro-
gram. Map of Baltimore County watershed. 2007.
Available at: http://www.baltimorecountymd.gov/
agencies/environment/watersheds/index.html. Accessed
October 14, 2008.
73. Sunderland D, Graczyk T, Tamang L, Breysse P.
Impact of bathers on levels of Cryptosporidium parvum
oocysts and Giardia lamblia cysts in recreational beach
waters. Water Res. 2007;41(15):3483–3489.
RESEARCH AND PRACTICE
1122 | Research and Practice | Peer Reviewed | McOliver et al. American Journal of Public Health | June 2009, Vol 99, No. 6

More Related Content

Viewers also liked

윈스바카라あ÷『JATA7.COM』÷あ카지노사이트
윈스바카라あ÷『JATA7.COM』÷あ카지노사이트윈스바카라あ÷『JATA7.COM』÷あ카지노사이트
윈스바카라あ÷『JATA7.COM』÷あ카지노사이트zkagcda264
 
강원도바카라ト㉿『JATA7.COM』㉿ト라이브카지노
강원도바카라ト㉿『JATA7.COM』㉿ト라이브카지노강원도바카라ト㉿『JATA7.COM』㉿ト라이브카지노
강원도바카라ト㉿『JATA7.COM』㉿ト라이브카지노zkagcda264
 
Explorador de windows (1)
Explorador de windows (1)Explorador de windows (1)
Explorador de windows (1)nilda2019
 
UCI Hipotecas - Inmocionate 2015 (Cóctel)
UCI Hipotecas - Inmocionate 2015 (Cóctel)UCI Hipotecas - Inmocionate 2015 (Cóctel)
UCI Hipotecas - Inmocionate 2015 (Cóctel)UCI España
 
11 ways for_local_businesses_to_get_links
11 ways for_local_businesses_to_get_links11 ways for_local_businesses_to_get_links
11 ways for_local_businesses_to_get_linksContent Amplified
 
Protección, explotación y valoración de la marca en el deporte
Protección, explotación y valoración de la marca en el deporteProtección, explotación y valoración de la marca en el deporte
Protección, explotación y valoración de la marca en el deportePons Deporte y Entretenimiento
 
Plataforma google ppt
Plataforma google pptPlataforma google ppt
Plataforma google pptnilda2019
 
BallSamples3of3
BallSamples3of3BallSamples3of3
BallSamples3of3F.C. Ball
 
MANUAL BÁSICO DE INTRODUCCIÓN A LA CUSTODIA DEL TERRITORIO
MANUAL BÁSICO DE INTRODUCCIÓN A LA CUSTODIA DEL TERRITORIO MANUAL BÁSICO DE INTRODUCCIÓN A LA CUSTODIA DEL TERRITORIO
MANUAL BÁSICO DE INTRODUCCIÓN A LA CUSTODIA DEL TERRITORIO ESDI MAESTRAZGO
 

Viewers also liked (13)

윈스바카라あ÷『JATA7.COM』÷あ카지노사이트
윈스바카라あ÷『JATA7.COM』÷あ카지노사이트윈스바카라あ÷『JATA7.COM』÷あ카지노사이트
윈스바카라あ÷『JATA7.COM』÷あ카지노사이트
 
강원도바카라ト㉿『JATA7.COM』㉿ト라이브카지노
강원도바카라ト㉿『JATA7.COM』㉿ト라이브카지노강원도바카라ト㉿『JATA7.COM』㉿ト라이브카지노
강원도바카라ト㉿『JATA7.COM』㉿ト라이브카지노
 
Explorador de windows (1)
Explorador de windows (1)Explorador de windows (1)
Explorador de windows (1)
 
UCI Hipotecas - Inmocionate 2015 (Cóctel)
UCI Hipotecas - Inmocionate 2015 (Cóctel)UCI Hipotecas - Inmocionate 2015 (Cóctel)
UCI Hipotecas - Inmocionate 2015 (Cóctel)
 
11 ways for_local_businesses_to_get_links
11 ways for_local_businesses_to_get_links11 ways for_local_businesses_to_get_links
11 ways for_local_businesses_to_get_links
 
Telefonia IP
Telefonia IPTelefonia IP
Telefonia IP
 
Protección, explotación y valoración de la marca en el deporte
Protección, explotación y valoración de la marca en el deporteProtección, explotación y valoración de la marca en el deporte
Protección, explotación y valoración de la marca en el deporte
 
Journey-Escape
Journey-EscapeJourney-Escape
Journey-Escape
 
Plataforma google ppt
Plataforma google pptPlataforma google ppt
Plataforma google ppt
 
BallSamples3of3
BallSamples3of3BallSamples3of3
BallSamples3of3
 
MANUAL BÁSICO DE INTRODUCCIÓN A LA CUSTODIA DEL TERRITORIO
MANUAL BÁSICO DE INTRODUCCIÓN A LA CUSTODIA DEL TERRITORIO MANUAL BÁSICO DE INTRODUCCIÓN A LA CUSTODIA DEL TERRITORIO
MANUAL BÁSICO DE INTRODUCCIÓN A LA CUSTODIA DEL TERRITORIO
 
Practica n0
Practica n0Practica n0
Practica n0
 
Herramienta web2
Herramienta web2Herramienta web2
Herramienta web2
 

Similar to McOliver et al AJPH.2008

fact sheet human herpes virus mod 7 updated.docx
fact sheet human herpes virus mod 7  updated.docxfact sheet human herpes virus mod 7  updated.docx
fact sheet human herpes virus mod 7 updated.docxSoniaShandil
 
Water borne microorganisms
Water borne microorganismsWater borne microorganisms
Water borne microorganismsTamanna Syeda
 
Microbial source tracking markers for detection of fecal contamination
Microbial source tracking markers for detection of fecal contaminationMicrobial source tracking markers for detection of fecal contamination
Microbial source tracking markers for detection of fecal contaminationFatima Batool
 
GLOBAL ISSUES IN WATER QUALITY: IMPLICATIONS FOR ONE HEALTH
GLOBAL ISSUES IN WATER QUALITY: IMPLICATIONS FOR ONE HEALTHGLOBAL ISSUES IN WATER QUALITY: IMPLICATIONS FOR ONE HEALTH
GLOBAL ISSUES IN WATER QUALITY: IMPLICATIONS FOR ONE HEALTHGlobal Risk Forum GRFDavos
 
Awarenes of aids amongst hs students in bonaire with amended list of authors
Awarenes of aids amongst hs students in bonaire with amended list of authorsAwarenes of aids amongst hs students in bonaire with amended list of authors
Awarenes of aids amongst hs students in bonaire with amended list of authorsAleksandar Dusic, MD, MSc
 
UC Nursing CESDEV Deworming
UC Nursing CESDEV DewormingUC Nursing CESDEV Deworming
UC Nursing CESDEV Dewormingucnursingcesdev
 
Foodborne diseases
Foodborne diseasesFoodborne diseases
Foodborne diseasesS A Tabish
 
Parasites in food chains
Parasites in food chainsParasites in food chains
Parasites in food chainsILRI
 
morbillivirus2014
morbillivirus2014morbillivirus2014
morbillivirus2014Kat Gilmore
 
Prevalence Of Urinary Schistosomiasis Among Pupils Attending Primary Schools ...
Prevalence Of Urinary Schistosomiasis Among Pupils Attending Primary Schools ...Prevalence Of Urinary Schistosomiasis Among Pupils Attending Primary Schools ...
Prevalence Of Urinary Schistosomiasis Among Pupils Attending Primary Schools ...IJRES Journal
 
Emerging and Reemerging Viruses
 Emerging and Reemerging Viruses Emerging and Reemerging Viruses
Emerging and Reemerging VirusesBASITZESHAN
 
Zoonotics and vector borne diseases
Zoonotics and vector borne diseases Zoonotics and vector borne diseases
Zoonotics and vector borne diseases DR HARDEV SINGH
 
Traditional Medicine &amp; Healthcare in Ghana
Traditional Medicine &amp; Healthcare in GhanaTraditional Medicine &amp; Healthcare in Ghana
Traditional Medicine &amp; Healthcare in Ghanalisambriggs
 
Role of life events in the presence of colon polyps among African Americans
Role of life events in the presence of colon polyps among African AmericansRole of life events in the presence of colon polyps among African Americans
Role of life events in the presence of colon polyps among African AmericansEnrique Moreno Gonzalez
 
Views of Postgraduate Students about Staph Infection
Views of Postgraduate Students about Staph InfectionViews of Postgraduate Students about Staph Infection
Views of Postgraduate Students about Staph InfectionBRNSSPublicationHubI
 
HIV/ AIDS Fact Sheet
HIV/ AIDS Fact SheetHIV/ AIDS Fact Sheet
HIV/ AIDS Fact Sheetadroits
 

Similar to McOliver et al AJPH.2008 (20)

crypto
cryptocrypto
crypto
 
fact sheet human herpes virus mod 7 updated.docx
fact sheet human herpes virus mod 7  updated.docxfact sheet human herpes virus mod 7  updated.docx
fact sheet human herpes virus mod 7 updated.docx
 
Water borne microorganisms
Water borne microorganismsWater borne microorganisms
Water borne microorganisms
 
Microbial source tracking markers for detection of fecal contamination
Microbial source tracking markers for detection of fecal contaminationMicrobial source tracking markers for detection of fecal contamination
Microbial source tracking markers for detection of fecal contamination
 
GLOBAL ISSUES IN WATER QUALITY: IMPLICATIONS FOR ONE HEALTH
GLOBAL ISSUES IN WATER QUALITY: IMPLICATIONS FOR ONE HEALTHGLOBAL ISSUES IN WATER QUALITY: IMPLICATIONS FOR ONE HEALTH
GLOBAL ISSUES IN WATER QUALITY: IMPLICATIONS FOR ONE HEALTH
 
Awarenes of aids amongst hs students in bonaire with amended list of authors
Awarenes of aids amongst hs students in bonaire with amended list of authorsAwarenes of aids amongst hs students in bonaire with amended list of authors
Awarenes of aids amongst hs students in bonaire with amended list of authors
 
UC Nursing CESDEV Deworming
UC Nursing CESDEV DewormingUC Nursing CESDEV Deworming
UC Nursing CESDEV Deworming
 
Foodborne diseases
Foodborne diseasesFoodborne diseases
Foodborne diseases
 
Parasites in food chains
Parasites in food chainsParasites in food chains
Parasites in food chains
 
Campylobacter fetus
Campylobacter fetusCampylobacter fetus
Campylobacter fetus
 
morbillivirus2014
morbillivirus2014morbillivirus2014
morbillivirus2014
 
Prevalence Of Urinary Schistosomiasis Among Pupils Attending Primary Schools ...
Prevalence Of Urinary Schistosomiasis Among Pupils Attending Primary Schools ...Prevalence Of Urinary Schistosomiasis Among Pupils Attending Primary Schools ...
Prevalence Of Urinary Schistosomiasis Among Pupils Attending Primary Schools ...
 
Emerging and Reemerging Viruses
 Emerging and Reemerging Viruses Emerging and Reemerging Viruses
Emerging and Reemerging Viruses
 
Zoonotics and vector borne diseases
Zoonotics and vector borne diseases Zoonotics and vector borne diseases
Zoonotics and vector borne diseases
 
Traditional Medicine &amp; Healthcare in Ghana
Traditional Medicine &amp; Healthcare in GhanaTraditional Medicine &amp; Healthcare in Ghana
Traditional Medicine &amp; Healthcare in Ghana
 
Role of life events in the presence of colon polyps among African Americans
Role of life events in the presence of colon polyps among African AmericansRole of life events in the presence of colon polyps among African Americans
Role of life events in the presence of colon polyps among African Americans
 
rucker_final
rucker_finalrucker_final
rucker_final
 
Views of Postgraduate Students about Staph Infection
Views of Postgraduate Students about Staph InfectionViews of Postgraduate Students about Staph Infection
Views of Postgraduate Students about Staph Infection
 
REPORT ON PEER EDUCATOR TRAINING
REPORT ON PEER EDUCATOR TRAININGREPORT ON PEER EDUCATOR TRAINING
REPORT ON PEER EDUCATOR TRAINING
 
HIV/ AIDS Fact Sheet
HIV/ AIDS Fact SheetHIV/ AIDS Fact Sheet
HIV/ AIDS Fact Sheet
 

McOliver et al AJPH.2008

  • 1. Risks of Recreational Exposure to Waterborne Pathogens Among Persons With HIV/AIDS in Baltimore, Maryland Cynthia C. McOliver, MPH, Hanna B. Lemerman, MPH, Ellen K. Silbergeld, PhD, Richard D. Moore, MD, and Thaddeus K. Graczyk, PhD Persons with HIV/AIDS are at high risk for increased morbidity and mortality associated with a range of opportunistic infections, some of which are caused by Cryptosporidium. Cryp- tosporidium species are of particular public health and medical importance because they are prevalent in surface waters of the United States,1–7 are efficiently transmitted via water,8 and can be consumed in foods contaminated by fecal matter.9–11 Exposures to Cryptosporidium are common in the US population,12 and past studies have demonstrated that Cryptosporidium infections significantly contribute to illness and mortality in persons with HIV/AIDS.13–15 In the 1980s, Cryptosporidium was identified as a major opportunistic pathogen.16–21 Infection continues to be frequently diagnosed in persons with HIV/ AIDS.22–27 Before the advent of highly active antiretroviral therapy, Cryptosporidium was a relatively common opportunistic infection even in developed countries.28,29 Cryptosporidiosis manifests as an acute gas- troenteritis, accompanied by cramps, anorexia, vomiting, abdominal pains, fever, and chills29 and by histological presentation of gastrointesti- nal mucosal injury.30,31 Persons with AIDS who become infected with this parasite are at in- creased risk of developing chronic and often life- threatening diarrhea, biliary tract diseases, pan- creatitis, colitis, and chronic asymptomatic infec- tion and recurrence. These developments are especially likely in those who are severely immunosuppressed (CD4 counts<150 cells/ mL).29,32–35 Infection is diagnosed by the pres- ence of oocysts in unpreserved or preserved stools.36 Histological and ultrastructural exami- nation of biopsy material for different Crypto- sporidium life stages, detection of Cryptosporid- ium DNA and antigens, and identification of species through molecular techniques can also aid in diagnosis.36–38 Cryptosporidium species are enteric proto- zoan organisms and are prevalent in US watersheds, especially in urban waters.1,6,39 These parasites have natural hosts in domestic and wild animals such as cattle (especially new- born calves), horses, fish, and birds.5,40–42 These parasites cause cryptosporidiosis by infecting and damaging the cells of the small intestine and other organs.13,41 For persons with HIV/AIDS, increased risk for infection by Cryptosporidium has been related to sexual practices such as engaging in sexual intercourse within the past 2 years, having multiple partners during that time, and engaging in anal intercourse.43 Use of spas and saunas has also been identified as a risk factor.43 In the United States, Cryptosporidium is the most commonly identified pathogen in cases of recreationally acquired gastroenteritis44 ; the majority of those affected are children. In- creased risk of cryptosporidiosis in persons with HIV/AIDS has been associated with swim- ming.45,46 US residents make an estimated 360 million annual visits to recreational water venues such as swimming pools, spas, and lakes; swim- ming is the second most popular physical activity in the country and the most popular among children.47 Recreational swimming, even in highly chlorinated water, carries a high risk of expo- sure to enteric pathogens, including Crypto- sporidium, Norovirus, Shigella, Escherichia coli, and Giardia.48 Cryptosporidiosis and some other enteric illnesses are seasonal, with spikes in occurrence in the summer months from contact with recreational water venues.49 Extreme pre- cipitation50 and high ambient temperatures51 can also affect patterns of disease outbreaks. Because not all infections with Cryptosporidium lead to apparent illness or symptoms, infected persons may unknowingly transmit these pathogens to others, such as household members and other recreationists.12,52 Cryptosporidiosis from swim- ming, wading, and splashing is prevalent in the United States.44,46,53,54 Risks from the presence of pathogens in waterways include (1) waterborne gastroenter- itis and other recreational water illnesses in anglers and other recreationists44,55–59 ; (2) transmission of pathogens to humans from Objectives. We assessed the prevalence of recreational activities in the waterways of Baltimore, MD, and the risk of exposure to Cryptosporidium among persons with HIV/AIDS. Methods. We studied patients at the Johns Hopkins Moore Outpatient AIDS Clinic. We conducted oral interviews with a convenience sample of 157 HIV/AIDS patients to ascertain the sites used for recreational water contact within Baltimore waters and assess risk behaviors. Results. Approximately 48% of respondents reported participating in recrea- tional water activities (fishing, crabbing, boating, and swimming). Men and women were almost equally likely to engage in recreational water activities (53.3% versus 51.3%). Approximately 67% (105 of 157) ate their own catch or that of friends or family members, and a majority (61%, or 46 of 75) of respondents who reported recreational water contact reported consumption of their own catch. Conclusions. Baltimoreans with HIV/AIDS are engaging in recreational water activities in urban waters that may expose them to waterborne pathogens and recreational water illnesses. Susceptible persons, such as patients with HIV/AIDS, should be cautioned regarding potential microbial risks from recrea- tional water contact with surface waters. (Am J Public Health. 2009;99: 1116–1122. doi:10.2105/AJPH.2008.151654) RESEARCH AND PRACTICE 1116 | Research and Practice | Peer Reviewed | McOliver et al. American Journal of Public Health | June 2009, Vol 99, No. 6
  • 2. caught seafood acting as fomites, or surface carriers60 ; (3) food-borne gastroenteritis from consumption of raw or improperly cooked fish and shellfish61,62 ; and (4) hand-to-mouth trans- mission of pathogens while eating, drinking, or smoking during activities such as fishing and crabbing.7 Recreational water activities in the Balti- more, Maryland, area take place in Jones Falls and Baltimore Harbor. These and other waterways are used for angling, crabbing, swimming, kayaking, and boating (including paddle boating).7,63 In addition, Baltimore-area residents often catch and consume fish and crabs from the Baltimore Harbor and local waterways, many of which are already highly contaminated by persistent chemicals such as mercury and polychlorinated biphenyls.64 These activities are known to increase risks of exposure to water- borne pathogens through direct contact with contaminated waters or through contact with or handling and consumption of caught seafood (fish, crabs, oysters).7,65,66 To investigate the potential contribution of recreational water contact to Cryptosporidium exposures among persons with HIV/AIDS, we carried out a cross-sectional study at the Johns Hopkins Moore Outpatient AIDS Clinic. The Baltimore metropolitan area has a high preva- lence rate of HIV/AIDS among both men and women,67 and its population makes intensive recreational use of a contaminated watershed. In addition, laboratory experiments have indicated that crabs can become superficially contami- nated by Cryptosporidium and transfer the path- ogen to hands.68 Local anglers are at risk from Cryptosporidium on wild-caught fish.7 Our objective was to address the risks of exposure to Cryptosporidium for an urban subpopulation, persons with HIV/AIDS, as a result of recreational contact with Baltimore waterways. We also assessed the patterns and locations of recreational water activities in Baltimore waters. METHODS The Hopkins AIDS Care Program and Moore Outpatient AIDS Clinic serve persons from the entire Baltimore metropolitan region; as of December 2008, approximately 3000 patients were being actively followed. Of these 31.3% were women, 78.2% were African American, 20.1% were non-Hispanic White, and 1.6% were Hispanic. Fifty percent of these patients were intravenous drug users, 22% were men who have sex with men, and 25% were heterosexual. These demographics are reflective of the AIDS epidemic in Baltimore and central Maryland. Study Design We identified a convenience sampling of patients that represented the typical clientele of the Moore clinic; our overall sample target was 150 patients. Our study was conducted between July 10 and September 17, 2007. Consent was obtained from respondents. The study was facilitated by R.D.M., the director of the clinic, as well as Vivian Zhao, the clinic administrator. Patients were ineligible if they worked with farm animals, had contact with animals from a petting zoo, or had previously completed the survey. No personal identifiers were collected during the course of the study. In total, 157 patients con- sented and fulfilled the criteria to participate in the study. We used an oral interview format validated in a pilot project.69 The survey was adminis- tered in the lobby of the clinic and in a down- stairs office between 9 AM and 2 PM. Participants were asked to respond to questions about their place of residence, age, gender, ethnicity, loca- tions of recreational water activities (specifically crabbing), patterns of activity, consumption of wild-caught fish and crabs from Baltimore waterways, and hand-washing habits during recreational water activities. A Batimore County watershed map was used to facilitate location of sites used for recretional water activities (Figure 1). They also reported current and recent recre- ational water activity by month and frequency and responded to questions about potential risk factors for Cryptosporidium transmission such as contact with diapered children, consumption of untreated water, travel overseas, pet ownership, and wild-animal contact. Most responses were qualitative (yes, no, not applicable). We used a categorical frequency scale to quantify monthly recreational activity (e.g., 0–4 times/mo). The term recent referred to any event occurring with the previous month. Respondents were compensated with a $10 store gift card upon completion of the survey. Responses to survey questions were checked off or handwritten on the survey by C.C.M. and 2 other survey administrators. Respondents were also encouraged to comment on the survey and to ask any questions they thought were relevant. Statistical Analyses Data were entered into Microsoft Excel 200370 and analyzed with STATA version 9.2.71 We made statistical comparisons with the Fisher exact test and c2 test. Statistical signifi- cance was set at .05. We used the 2-sided t test for means to assess difference in age by cate- gories. We assessed group differences with the binomial test of proportions and used nonmiss- ing data for estimations. RESULTS Participants were predominantly African American and evenly distributed between men and women (Table1). The participation rate was more than 90% among clinic patients who were approached. Demographic characteristics and risk exposure behaviors of the study population are presented in Table1and Table 2. Because of small numbers, racial/ethnic groups other than African American and non-Hispanic White TABLE 1—Race/Ethnicity and Gender Comparisons Between Study Participants (n=157) and Clinic Patients (n=1830) of the Johns Hopkins Moore Outpatient AIDS Clinic: Baltimore, MD, 2007 Participants Clinic Patientsa Race/ethnicity, % African American 86.6 74 Non-Hispanic White 7 23 Biracial 3.2 . . . Hispanic 1.3 2 Other 0.6 1 Missing 1.3 . . . Gender, % Men 51.3 65 Women 48 35 Transgender 0.7 . . . Age, y, median (range) 47 (27–75) 41 (19–88) Note. Ellipses indicate data were not available or not collected. a Data were from 2003 to 2007. RESEARCH AND PRACTICE June 2009, Vol 99, No. 6 | American Journal of Public Health McOliver et al. | Peer Reviewed | Research and Practice | 1117
  • 3. were collapsed into 1 category, other (Hispanic, Asian, biracial, and African). There were 75 women, 80 men, and 1 transgendered per- son. One respondent did not provide gender information. The mean age of the 152 participants whose age was reported was 47.2 68.4 years (range=27–75 years). The median age was 47 years, with the age distribution slightly posi- tively skewed (0.35). There was no difference in age between respondents who engaged in recreational water activities and those who did not (P=.32). Ninety-five percent of the re- spondents were 61 years or younger. Almost half of the respondents (47.8%, or 75 persons) TABLE 2—Participant Characteristics and Risk Behaviors, by Gender and Race/Ethnicity: Baltimore, MD, 2007 Gender Race/Ethnicity Men (n=80) Women (n=75) African American (n=136) Non-Hispanic White (n=11) Other (n=8) Age, y, mean 6SD (95% CI) 48.267.7 (46.5, 49.9) 46.168.9 (43.9, 48.1) 47.167.8 (45.8, 48.5) 4468.3 (37.6, 50.9) 51614.9 (38.5, 63.5) Age, y, median (range) 49 (27–68) 45 (27–75) 47 (27–75) 48 (30–53) 50 (27–68) Recreational water contact, No. (%) Yes 41 (51.3) 40 (53.3) 71 (52.2) 5 (45.5) 5 (62.5) No 39 (48.7) 35 (46.7) 65 (47.8) 6 (54.5) 3 (37.5) Consumption of self-caught fish and crabs, No. (%) Yes 24 (30) 22 (29.3) 41 (30.1) 3 (27.3) 2 (25) No 3 (3.8) 3 (4) 4 (2.9) 2 (18.2) 0 (0) Not applicablea 52 (65) 50 (66.7) 91 (66.9) 6 (54.5) 6 (75) Missing 1 (1.25) 0 (0) 0 (0) 0 (0) 0 (0) Consumption of others’ wild-caught fish and crabs Yes 46 (57.5) 52 (69.3) 88 (64.7) 6 (54.5) 4 (50) No 32 (40) 22 (29.3) 46 (33.8) 5 (45.5) 4 (50) Missing 2 (2.5) 1 (1.4) 2 (1.5) 0 (0) 0 (0) Handwashing during recreational activity, No. (%) Yes 31 (38.8) 25 (33.3) 50 (36.8) 4 (36.4) 2 (25) No 6 (7.5) 6 (8) 10 (7.4) 2 (18.2) 0 (0) Not applicablea 41 (51.3) 40 (53.3) 72 (52.9) 5 (45.5) 5 (62.5) Missing 2 (2.5) 4 (5.3) 4 (2.9) 0 (0) 1 (12.5) Pets in home, No. (%) Yes 29 (36.3) 29 (38.7) 51 (37.5) 5 (45.5) 2 (25) No 49 (61.3) 44 (58.7) 84 (61.8) 4 (36.4) 6 (75) Missing 2 (2.4) 2 (2.6) 1 (0.7) 2 (18.1) 0 (0) Consumption of well water, No. (%) Yes 4 (5) 4 (5.3) 7 (5.2) 1 (9.1) 0 (0) No 74 (92.5) 70 (93.3) 128 (94.1) 9 (81.8) 8 (100) Missing 2 (2.5) 1 (1.33) 1 (0.7) 1 (9.1) 0 (0) Travel outside United States, No. (%) Yes 1 (0.8) 1 (1.3) 1 (0.7) 0 (0) 1 (12.5) No 77 (96.3) 73 (97.3) 134 (98.5) 10 (90.9) 7 (87.5) Missing 2 (2.5) 1 (1.33) 1 (0.7) 1 (9.1) 0 (0) Changing of baby diapers, No. (%) Yes 13 (16.3) 26 (34.7) 34 (25) 2 (18.2) 3 (37.5) No 65 (81.3) 47 (62.7) 101 (74.3) 7 (63.6) 5 (62.5) Missing 2 (2.4) 2 (2.6) 1 (0.7) 2 (18.2) 0 (0) Contact with wild animals, No. (%) Yes 4 (5) 3 (4) 6 (4.4) 1 (9.1) 0 (0) No 73 (91.3) 70 (93.3) 128 (94.1) 8 (72.7) 8 (100) Missing 3 (3.7) 2 (2.7) 2 (1.5) 2 (18.2) 0 (0) Note. CI=confidence interval. Totals across categories may not sum to total study population because of missing data. a Participant did not engage in this activity. RESEARCH AND PRACTICE 1118 | Research and Practice | Peer Reviewed | McOliver et al. American Journal of Public Health | June 2009, Vol 99, No. 6
  • 4. reportedsomeform of recreational wateractivity, and 82 participants (52.2%) reported none. Similar numbers of men and women engaged in recreational water activity (39 and 35, respec- tively), and similar numbers did not (41and 40). The most common locations for reported recreational water activity were the Baltimore Harbor (Canton, Fells Point), Patapsco River (Middle Branch Park, Harbor Hospital), and Gunpowder River (Figure 2). These sites are centrally located within the Baltimore County watershed (Figure 1).72 Respondents gave mul- tiple reasons for engaging in fishing and crab- bing. The majority (n=75) reported that they fished or crabbed for fun, recreation, and relax- ation (68%) as well as for food or to supplement diets (58.9%). Other reported reasons were sharing caught fish and crabs (45%) and spend- ing time with family or children (2.7%). Among risk factors associated with Crypto- sporidium infection and transmission, the most commonly reported were changing baby dia- pers (39 respondents, or 24.8%) and pets in the home (58, or 36.9%). Eight respondents (5.1%) reported well water consumption, 2 (1.3%) reported travel outside the United States, and 7 (4.5%) reported contact with wild animals (wild birds, raccoons, or deer). The distribution of these risk factors by race/eth- nicity and gender are shown in Table 2. We estimated contact with wild-caught fish and crabs by asking about consumption of fish and crabs caught by others. Approximately 67% of participants (105 of 157) reported con- sumption of their own catch or wild-caught fish and crabs from friends or family members. A majority (46 of 75, or 61%) of respondents who reported recreational water contact ate their own catch. Consumption of fish and crabs caught in the wild by either friends or family members was reported by approximately 80% (59 of 74) of those who engaged in recreational water activity and only 48% (38 of 79) of those who did not. Respondents also provided data on their frequency of recreational water activities (Ta- ble 3), with the majority reporting taking part in activities 1 to 4 times a month. DISCUSSION We found a high level of self-reported par- ticipation in recreational water activity among HIV/AIDS patients at an urban Baltimore outpatient clinic. Respondents reported activi- ties such as fishing, crabbing, boating, and swimming, as well as consumption of their own catch and wild-caught fish and crabs supplied by friends or family members. Our study sam- ple was representative of the larger clinic pop- ulation; therefore, our findings could be gen- eralized to the larger Moore Clinic patient population, despite our small sample size. These findings are relevant to public health in light of recent findings of viable Cryptosporid- ium in many of the waters commonly used by our respondents and others in the region for recreational water activities.7,67,73 To our knowledge, ours is the first study to describe recreational water contact among persons with HIV/AIDS. Another strength of our study was an excellent participation rate of more than 90% of clinic patients who were approached for participation. Limitations Our study had several limitations. Respon- dents were asked to recall recreational activi- ties, including locations, activities, frequency, and specific months of participation, a method of data collection with a potential for recall bias. Some participants could not describe or iden- tify the specific sites they used for recreational activities. Efforts were made to fill in these data gaps with a Baltimore County watershed map during the interview process. Interviews took place in a clinical setting where participants often had limited time to complete surveys. Patients were free to leave at any point during the interview to go to their appointments; most returned to complete their surveys. Some incomplete data collection and nonresponses resulted from time restraints on both patients and interviewers (who could not always review all questions or double-check responses). Language barriers may have prevented en- rollment and participation of patients in the study. However, fewer than 5 patients were identified as having a language barrier. Some respondents may have completed multiple surveys during the course of the study period, because no personal identifiers were collected. However, efforts were made to limit participa- tion to persons who reported not previously completing our survey, and we used an ex- emption form to exclude these persons. Source. Baltimore County Environmental Protection and Resource Management Watershed Management Program.73 FIGURE 1—Map of Baltimore County watershed used during survey to identify sites of recreational water activity: 2007. RESEARCH AND PRACTICE June 2009, Vol 99, No. 6 | American Journal of Public Health McOliver et al. | Peer Reviewed | Research and Practice | 1119
  • 5. Conclusions We found that persons with HIV/AIDS, a subset of the urban population, frequently take part in recreational water activities in the Baltimore area. Unfortunately, this watershed is contaminated by Cryptosporidium and other enteric pathogens of concern for both healthy and immunocompromised individuals. This population is engaging in fishing and crabbing not only for fun, sport, or recreation but also for diet supplementation and subsis- tence. Contact with fish and crabs during preparation and handling may expose individ- uals to Cryptosporidium via contamination of hands, preparation and cooking surfaces, and equipment. In addition, exposure may occur from consumption of improperly cooked fish and crabs. These recreational sites lack hand- washing facilities, a concern because food and beverages are commonly consumed there. Pathogens such as Cryptosporidium are not routinely monitored in surface waters and are not included in existing fish advisories. As a result, the general public, including immuno- compromised and other highly susceptible persons, are not aware of the risks of exposure and infection posed by pathogens. This lack of communication is a major public health failure, not limited to but of particular concern for persons who are immunocompromised. Regu- latory agencies, watershed associations, and others involved in recreational water programs should inform themselves about the effect of infectious pathogens in recreational waters and develop routine surveillance, monitoring, and notification systems to ensure the safety of urban waters. Physicians and other caregivers for per- sons with HIV/AIDS should incorporate questions about recreational water activities, foreign travel, and other activities with po- tential for pathogen exposure during routine intake procedures and follow-up of patients with acute or chronic gastroenteritis. In addition, patients who are at high risk for noncompliance with antiretroviral therapy regimens or who are not receiving these therapies should be counseled on the risk factors for exposure and infection by Cryp- tosporidium. Future national health surveys should in- clude questions about potential sources of exposure to Cryptosporidium, as well as about residence, foreign travel, and recrea- tional water activities (including chlorinated water venues such as swimming pools) to accurately characterize the populations at risk. j About the Authors At the time of the study, Cynthia C. McOliver, Ellen K. Silbergeld, and Thaddeus K. Graczyk were with the Bloomberg School of Public Health, Johns Hopkins Uni- versity, Baltimore, MD. Hanna B. Lemerman was a student at the School of Medicine, Johns Hopkins University, Baltimore. Richard D. Moore is with the HIV Clinic, Johns Hopkins University, Baltimore. Request for reprints should be sent to Cynthia C. McOliver, 615 N Wolfe St, Room W6005, Johns Hopkins Bloomberg School of Public Health, Baltimore, MD 21205 (e-mail: cmcolive@jhsph.edu). This article was accepted December 11, 2008. Contributors C.C. McOliver conducted the research, analyzed the data, and drafted the article. H. B. Lemerman admin- istered surveys, performed quality control of the sur- vey data, checked references for the article, modified tables, and edited drafts of the article. E. K. Silbergeld and T. K. Graczyk designed the study and assisted with the revision of the article. E. Silbergeld also reviewed the study materials and helped develop the questions for the survey. R. D. Moore facilitated participant re- cruitment and clinic staff assistance and reviewed the article. Acknowledgments This research was supported by a Johns Hopkins Center for a Livable Future Faculty and Student Innovation Grant (no. 1602030055). The authors thank the staff and patients of the Moore Clinic for participating in this research. We are especially thankful for the advice and support of Cynthia Sears of the Divisions of Infectious Diseases and Gastroenterology at Johns Hopkins School of Medicine. Special thanks to Preety Gadhoke and Carol Resnick for their assistance with developing the surveys, Sean Evans for assistance with administering the surveys, Ruth Quinn and Ellen Wells for beta testing the surveys, and Marisa Caliri for her untiring assistance with data entry and quality assurance. Human Participant Protection All study protocols and materials received approval from the Johns Hopkins School of Public Health committee on human research. Note. The number reporting activities includes multiple sites and activities. FIGURE 2—Recreational water sites used by patients surveyed at the Johns Hopkins Moore Outpatient AIDS Clinic, Baltimore, MD: 2007. RESEARCH AND PRACTICE 1120 | Research and Practice | Peer Reviewed | McOliver et al. American Journal of Public Health | June 2009, Vol 99, No. 6
  • 6. References 1. LeChevallier MW, Norton WD, Lee RG. Occurrence of Giardia and Cryptosporidium spp. in surface water supplies. Appl Environ Microbiol. 1991;57(9);2610– 2616. 2. Lisle JT, Rose JB. Cryptosporidium contamination of water in the USA and UK: a mini-review. Aqua. 1995; 44(3);103–117. 3. Rose J, Lisle J, LeChevallier M. Waterborne crypto- sporidiosis: incidence, outbreaks. treatment strategies. Fayer R, ed. Cryptosporidium and Cryptosporidiosis. New York, NY: CRC Press:1997:251. 4. Todd S, Phillips M, Marchin G, Upton S. Cryptospo- ridium Giardia in surface waters in and around Manhat- tan, Kansas. Trans Kans Acad Sci. 1991;94(3/4); 101–106. 5. Xiao L, Singh A, Limor J, Graczyk T, Gradus S, Lal A. Molecular characterization of Cryptosporidium oocysts in samples of raw surface water and wastewater. Appl Environ Microbiol. 2001;67(3);1097–1101. 6. Arnone R, Walling J. Waterborne pathogens in urban watersheds. J Water Health. 2007;5(1);149–162. 7. Roberts J, Silbergeld E, Graczyk T. A probabilistic risk assessment of Cryptosporidium exposure among baltimore urban anglers. J Toxicol Environ Health A. 2007;70(18);1568–1576. 8. Fayer R. Cryptosporidium: a water-borne zoonotic parasite. Vet Parasitol. 2004;126(1-2);37–56. 9. Centers for Disease Control and Prevention. Food- borne outbreak of cryptosporidiosis—Spokane, Wash- ington, 1997. MMWR Morb Mortal Wkly Rep. 1998; 47(27);565–567. 10. Yoshida H, Matsuo M, Miyoshi T, et al. An outbreak of cryptosporidiosis suspected to be related to contami- nated food, October 2006, Sakai City. Jpn J Infect Dis. 2007;60(6);405–407. 11. Vojdani J, Beuchat L, Tauxe R. Juice-associated outbreaks of human illness in the United States, 1995 through 2005. J Food Prot. 2008;71(2);356–364. 12. Frost F, Muller T, Calderon R, Craun G. Analysis of serological responses to Cryptosporidium antigen among NHANES III participants. Ann Epidemiol. 2004;14(7); 473–478. 13. Chen X-M, Keithly J, Paya C, LaRusso N. Crypto- sporidiosis. N Engl J Med. 2002;346(22);1723–1731. 14. Frost F, Muller T, Gunther F, Lockwood W, Calderon R. Serological evidence of endemic waterborne Crypto- sporidium infections. Ann Epidemiol. 2002;12(4);222– 227. 15. Hlavsa MC, Watson JC, Beach MJ. Cryptosporidiosis surveillance—United States 1999–2002. MMWR Sur- veill Summ. 2005;54(1);1–8. 16. Centers for Disease Control and Prevention. Cryp- tosporidiosisassessment of chemotherapy of males with acquired immune deficiency syndrome(AIDS). MMWR Morb Mortal Wkly Rep. 1982;31:589–592. 17. Jokipii L, Pohjola S, Jokipii AM. Cryptosporidium: a frequent finding in patients with gastrointestinal symp- toms. Lancet. 1983;2:358–361. 18. Current W, Reese N, Ernst J, Bailey WS, Heyman M, Weinstein W. Human cryptosporidiosis in immunocom- petent and immunodeficient persons. Studies of an out- break and experimental transmission. N Engl J Med. 1983;308(21);1252–1257. 19. Forgacs P, Tarshis A, Ma P, et al. Intestinal and bronchial cryptosporidiosis in an immunodeficient ho- mosexual man. Ann Intern Med. 1983;99(6);793–794. 20. Soave R, Danner R, Honig C, et al. Cryptosporidiosis in homosexual men. Ann Intern Med. 1984;100(4);504– 511. 21. Casemore D, Sands R, Curry A. Cryptosporidium species a ‘‘new’’ human pathogen. J Clin Pathol. 1985; 38(12);1321–1336. 22. Brandonisio O, Maggi P, Panaro M, Bramante L, Di Coste A, Angarano G. Prevalence of cryptosporidiosis in HIV-infected patients with diarrhoeal illness. Eur J Epi- demiol. 1993;9(2);190–194. 23. Sandhu S, Priest J, Lammie P, et al. The natural history of antibody responses to Cryptosporidium para- sites in men at high risk of HIV infection. J Infect Dis. 2006;194(10);1428–1437. 24. Raccurt C, Brasseur P, Verdier R, et al. Human cryptosporidiosis and Cryptosporidium spp. in Haiti. Trop Med Int Health. 2006;11(6);929–934. 25. de Oliveira-Silva M, de Oliveira L, Resende J, et al. Seasonal profile and level of CD4+ lymphocytes in the occurrence of cryptosporidiosis and cystoisosporidiosis in HIV/AIDS patients in the Triaˆngulo Mineiro region Brazil. Rev Soc Bras Med Trop Scielo. 2007;40:512–515. 26. Rao Ajjampur SS, Asirvatham JR, Muthusamy D, et al. Clinical features and risk factors associated with cryptosporidiosis in HIV infected adults in India. Indian J Med Res. 2007;126:553–557. 27. Gatei W, Barrett D, Lindo J, Eldemire-Shearer D, Cama V, Xiao L. Unique Cryptosporidium population in HIV-infected persons, Jamaica. Emerg Infect Dis. 2008; 14(5);841–843. 28. Manabe Y, Clark D, Moore R, et al. Cryptosporidiosis in patients with AIDS: correlates of disease and survival. Clin Infect Dis. 1998;27(3);536–542. 29. Hunter PR, Nichols G. Epidemiology and clinical features of Cryptosporidium infection in immunocompro- mised patients. Clin Microbiol Rev. 2002;15(1);145–154. TABLE 3—Study Participants’ Frequency of Participating in Recreational Water Activities, by Location: Baltimore, MD, 2007 Activity Patapsco River Baltimore Harbor Gunpowder River Back River Fishing, times/mo 1–4 21 8 11 7 5–8 4 0 0 0 ‡9 1 1 0 0 Missing 5 1 0 1 Not applicablea 44 65 64 67 Total 75 75 75 75 Crabbing 1–4 15 9 6 4 5–8 2 0 0 0 ‡9 1 1 0 0 Missing 3 1 0 1 Not applicablea 54 64 69 70 Total 75 75 75 75 Boating 1–4 7 26 4 2 5–8 2 0 0 0 ‡9 0 1 0 0 Missing 0 5 0 0 Not applicablea 66 43 71 73 Total 75 75 75 75 Swimming 1–4 5 6 14 2 5–8 1 1 0 0 ‡9 0 0 0 0 Missing 1 1 2 0 Not applicablea 68 67 59 63 Total 75 75 75 65 Note. These 4 sites were the most frequently used by the 75 patients reporting recreational water contact. a Participant did not engage in this activity at this site. RESEARCH AND PRACTICE June 2009, Vol 99, No. 6 | American Journal of Public Health McOliver et al. | Peer Reviewed | Research and Practice | 1121
  • 7. 30. Lumadue J, Manabe Y, Moore R, Belitsos P, Sears C, Clark D. A clinicopathologic analysis of AIDS-related cryptosporidiosis. AIDS. 1998;12(18):2459–2466. 31. Walker-Smith J. Post-infective diarrhea. Curr Opin Infect Dis. 2001;14(5):567–571. 32. Forbes A, Blanshard C, Gazzard B. Natural history of AIDS related sclerosing cholangitis: a study of 20 cases. Gut. 1993;34:116–121. 33. Lo´pez-Ve´lez R, Tarazona R, Garcia C, et al. Intestinal and extraintestinal cryptosporidiosis in AIDS patients. Eur J Clin Microbiol Infect Dis. 1995;14(8):677–681. 34. Vakil N, Schwartz S, Buggy B, et al. Biliary crypto- sporidiosis in HIV-infected people after the waterborne outbreak of cryptosporidiosis in Milwaukee. N Engl J Med. 1996;334(1):19–23. 35. Muthusamy D, Rao S, Ramani S, et al. Multilocus genotyping of Cryptosporidium sp. isolates from human immunodeficiency virus-infected individuals in South India. J Clin Microbiol. 2006;44(2):632–634. 36. Smith H. Diagnostics. In:Fayer R, Xiao L eds. Cryp- tosporidium and Cryptosporidiosis. 2nd ed. Boca Raton, FL: CRC Press; 2008:173–207. 37. Xiao L, Ryan UM. Molecular epidemiology. Fayer R, Xiao L, eds. Cryptosporidium and Cryptosporidiosis. 2nd ed. Boca Raton, FL: CRC Press; 2008:119–164. 38. Fayer R. General biology. In: Fayer R, Xiao L, eds. Cryptosporidium and Cryptosporidiosis. Boca Raton, FL: CRC Press; 2008:1–43. 39. States S, Stadterman K, Ammon L, et al. Protozoa in river water: sources, occurrence, and treatment. J Am Water Works Assoc. 1997;89(9):74–83. 40. Casemore D. Human cryptosporidiosis. In: Reeves DS, Geddes AM, eds. Recent Advances in Infection. Edinburgh, Scotland: Churchill Livingstone:1998:209– 236. 41. Fayer R, Morgan U, Upton S. Epidemiology of Cryptosporidium: transmission, detection and identifica- tion. Int J Parasitol. 2000;30(12–13):1305–1322. 42. Caccio` S. Molecular epidemiology of human cryp- tosporidiosis. Parassitologia. 2005;47(2):185–192. 43. Caputo C, Forbes A, Frost F, et al. Determinants of antibodies to Cryptosporidium infection among gay and bisexual men with HIV infection. Epidemiol Infect. 1999;122(2):291–297. 44. Centers for Disease Control and Prevention. Cryp- tosporidiosis outbreaks associated with recreational wa- ter use—five states, 2006. MMWR Morb Mortal Wkly Rep. 2007;56(29):729–732. 45. Inungu J, Morse A, Gordon C. Risk factors, season- ality, and trends of cryptosporidiosis among patients infected with human immunodeficiency virus. Am J Trop Med Hyg. 2000;62(3):384–387. 46. Causer LM, Handzel T, Welch P, et al. An outbreak of Cryptosporidium hominis infection at an Illinois recre- ational waterpark. Epidemiol Infect. 2006;134:147–156. 47. US Department of the Interior, Fish and Wildlife Service and US Department of Commerce, US Census Bureau. 2001 National survey of fishing, hunting, and wildlife-associated recreation. Available at: http:// www.census.gov/prod/2002pubs/FHW01.pdf. Accessed October 14, 2008. 48. Centers for Disease Control and Prevention. Notice to Readers: National Recreational Water Illness Pre- vention Week—May 19–25, 2008. MMWR. 2008; 57(19):528–529. Available at: http://www.cdc.gov/ mmwr/preview/mmwrhtml/mm5719a8.htm?s_cid= mm5719a8_e Accessed January 16, 2009. 49. Dziuban EJ, Liang JL, Craun GF, et al. Surveillance for waterborne disease and outbreaks associated with recreational water—United States, 2003–2004. MMWR Surveill Summ. 2006;55(12):1–20. 50. Curriero F, Patz J, Rose J, Lele S. The association between extreme precipitation and waterborne disease outbreaks in the United States, 1948–1994. Am J Public Health. 2001;91(8):1194–1199. 51. Naumova E, Jagai JS, Matyas B, DeMaria A Jr, MacNeill IB, Griffiths JK. Seasonality in six enterically transmitted diseases and ambient temperature. Epidemiol Infect. 2007;135(2):281–292. 52. Peng M, Xiao L, Freeman A, et al. Genetic poly- morphism among Cryptosporidium parvum isolates: evi- dence of two distinct human transmission cycles. Emerg Infect Dis. 1997;3(4):567–573. 53. Sorvillo F, Fujioka K, Nahlen B, Tormey M, Kebabjian R, Mascola L. Swimming-associated crypto- sporidiosis. Am J Public Health. 1992;82(5):742–744. 54. Craun G, Calderon R, Craun M. Outbreaks associ- ated with recreational water in the United States. Int J Environ Health Res. 2005;15(4):243–262. 55. Roy S, DeLong S, Stenzel S, et al. Risk factors for sporadic Cryptosporidiosis among immunocompetent persons in the United States from 1999 to 2001. J Clin Microbiol. 2004;42(7):2944–2951. 56. Bergsson G, Agerberth B, Jo¨rnvall H, Gudmundsson GH. Isolation and identification of antimicrobial compo- nents from the epidermal mucus of Atlantic cod (Gadus morhua). FEBS J. 2005;272(19):4960–4969. 57. Wade T, Calderon R, Sams E, et al. Rapidly mea- sured indicators of recreational water quality are pre- dictive of swimming-associated gastrointestinal illness. Environ Health Perspect. 2006;114(1):24–28. 58. Why are river recreationalists most at risk for development of waterborne infectious diseases: how can clinicians improve surveillance? A national problem. J Occup Environ Med. 2007;49(1):104–105. 59. Anne Arundel County, MD, Department of Health. Water quality and swimming or fishing in Anne Arundel County rivers and creeks. 2008. Available at: http:// www.aahealth.org/a2z.asp?id=110. Accessed October 14, 2008. 60. Anne Arundel County, MD, Department of Health. Mycobacterium marinum. 2006. Available at: http:// www.aahealth.org/a2z.asp?id=191. Accessed October 14, 2008. 61. Graczyk T, Schwab K. Foodborne infections vec- tored by molluscan shellfish. Curr Gastroenterol Rep. 2000;2(4):305–309. 62. Su Y-C, Liu C. Vibrio parahaemolyticus: a concern of seafood safety. Food Microbiol. 2007;24(6):549–558. 63. Davison SG, Merwin JG, Capper J, Power G, Shivers F. Chesapeake (Bay) Waters: Four Centuries of Controversy, Concern, and Legislation. 2nd ed. Centreville, MD: Tide- water Publishers; 1997. 64. Gibson JC, McClafferty JA. Chesapeake Bay Angler Interviews: Identifying Populations at Risk for Consuming Contaminated Fish in Three Regions of Concern. Blacks- burg, VA: Virginia Polytechnic Institute and State Uni- versity; 2005. Final Report CMI-HDD-05-01. Available at: http://www.nbii.gov/images/uploaded/155729_ 1170437308921_2004_ConsumptionAdvisories_ AnglerSurvey.pdf. Accessed January 21, 2009. 65. Graczyk T, Cranfield M, Fayer R. Recovery of waterborne oocysts of Cryptosporidium from water sam- ples by the membrane-filter dissolution method. Parasitol Res. 1997;83(2):121–125. 66. Graczyk T, Fayer R, Trout J, et al. Susceptibility of the Chesapeake Bay to environmental contamination with Cryptosporidium parvum. Environ Res. 2000b; 82(2):106–112. 67. Maryland Department of Health and Mental Hy- giene, AIDS Administration. Maryland HIV/AIDS fourth quarter 2007—data reported through December 31, 2007. Available at: http://www.dhmh.state.md.us/AIDS/ Data&Statistics/NewMDQtrEpi.pdf. Accessed October 14, 2008. 68. Graczyk T, McOliver C, Silbergeld EK, Tamang L, Roberts JD. Risk of handling as a route of exposure to infectious waterborne Cryptosporidium parvum oocysts via Atlantic blue crabs (Callinectes sapidus). Appl Environ Microbiol. 2007;73(12):4069–4070. 69. McOliver C, Graczyk TK, Silbergeld EK. Assessing the risks of exposure to Cryptosporidium from recrea- tional water activities in Baltimore, Maryland. 2008. In: Eades RT, Neal JW, Lang TJ, Hunt KM, Pajak P, eds. Urban and Community Fisheries Programs: Development, Management, and Evaluation. Symposium 67. Bethesda, MD: American Fisheries Society; 2008:165–174. 70. Microsoft Office Excel 2003 [computer program]. Redmond, WA: Microsoft Corp; 2003. 71. Intercooled STATA Statistical Software. 9th ed. Col- lege Station, TX: STATA Corp; 2006. 72. Baltimore County Environmental Protection and Resource Management Watershed Management Pro- gram. Map of Baltimore County watershed. 2007. Available at: http://www.baltimorecountymd.gov/ agencies/environment/watersheds/index.html. Accessed October 14, 2008. 73. Sunderland D, Graczyk T, Tamang L, Breysse P. Impact of bathers on levels of Cryptosporidium parvum oocysts and Giardia lamblia cysts in recreational beach waters. Water Res. 2007;41(15):3483–3489. RESEARCH AND PRACTICE 1122 | Research and Practice | Peer Reviewed | McOliver et al. American Journal of Public Health | June 2009, Vol 99, No. 6