1) Approximately 48% of respondents reported participating in recreational water activities like fishing, crabbing, boating, and swimming in Baltimore waterways.
2) Men and women were almost equally likely to engage in these activities.
3) A majority (61%) of those who reported recreational water contact also reported consuming fish and crabs caught from these waterways.
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)
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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.
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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.
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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.
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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.
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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.
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