Protective Practices and Respiratory Illness Among US Travelers to

163
Protective Practices and Respiratory Illness Among US Travelers
to the 2009 Hajj
Victor Balaban, PhD,∗ William M. Stauffer, MD,∗† Adnan Hammad, PhD,‡ Mohamud Afgarshe,
MD,§ Mohamed Abd-Alla, MD, Qanta Ahmed, MD,¶ Ziad A. Memish, MD,# Janan Saba,
MPH,‡ Elizabeth Harton, MPH,∗ Gabriel Palumbo, MPH,∗ and Nina Marano, DVM∗
∗
Division of Global Migration and Quarantine, Centers for Disease Control and Prevention, Atlanta, GA, USA; † Division of
Infectious Diseases and International Medicine, University of Minnesota, Minneapolis, MN, USA; ‡ Arab Community Center for
Economic and Social Services (ACCESS), Dearborn, MI, USA; § Gargar Urgent Care and Clinic, Minneapolis, MN, USA;
Division of Infectious Disease, Internal Medicine, Medical College of Wisconsin, Milwaukee, WI, USA; ¶ Department of
Medicine, Division of Pulmonary and Critical Care Medicine, State University of New York at Stony Brook, Winthrop
University Hospital, Mineola, NY, USA; # Ministry of Health, Riyadh, Kingdom of Saudi Arabia
DOI: 10.1111/j.1708-8305.2012.00602.x
Background. All mass gatherings can place travelers at risk for infectious diseases, but the size and density of the annual Hajj
pilgrimage to the Kingdom of Saudi Arabia (KSA) present important public health and infection control challenges. This survey of
protective practices and respiratory illness among US travelers to the 2009 Hajj was designed to evaluate whether recommended
behavioral interventions (hand hygiene, wearing a face mask, cough etiquette, social distancing, and contact avoidance) were
effective at mitigating illness among travelers during the 2009 Hajj.
Methods. US residents from Minnesota and Michigan completed anonymous surveys prior to and following travel to the 2009
Hajj. Surveys assessed demographics, knowledge, attitudes, and practices (KAP) related to influenza A(H1N1), vaccination,
health-seeking behaviors, sources of health information, protective behaviors during the Hajj, and respiratory illness during and
immediately after the Hajj.
Results. Pre- and post-travel surveys were completed by 186 participants. Respiratory illness was reported by 76 (41.3%)
respondents; 144 (77.4%) reported engaging in recommended protective behaviors during the Hajj. Reduced risk of respiratory
illness was associated with practicing social distancing, hand hygiene, and contact avoidance. Pilgrims who reported practicing
more recommended protective measures during the Hajj reported either less occurrence or shorter duration of respiratory illness.
Noticing influenza A(H1N1) health messages during the Hajj was associated with more protective measures and with shorter
duration of respiratory illness.
Conclusions. Recommended protective behaviors were associated with less respiratory illness among US travelers to the 2009 Hajj.
Influenza A(H1N1) communication and education in KSA during the Hajj may also have been an effective component of efforts
to mitigate illness. Evaluations of communication efforts and preventive measures are important in developing evidence-based
public health plans to prevent and mitigate disease outbreaks at the Hajj and other mass gatherings.
E
very year, millions of Muslims, including thousands
in the United States, make a pilgrimage called the
Hajj to the cities of Mecca and Medina in the Kingdom
of Saudi Arabia (KSA). An estimated 2,521,000
pilgrims attended the 2009 Hajj during November
25–29; of these, 1,613,000 were international pilgrims
from 163 countries, including 11,066 US Hajj
travelers.1,2
Corresponding Author: Victor Balaban, PhD, Field Services
and Evaluation Branch, Division of Tuberculosis Elimination,
Centers for Disease Control and Prevention, 1600 Clifton
Road, MS E-10, Atlanta, GA 30333, USA. E-mail:
[email protected]
While all mass gatherings have the potential to place
travelers at risk for infectious and noninfectious hazards,
the Hajj presents some of the world’s most important
public health and infection control challenges.3 A variety
of risk factors makes the Hajj an environment where
emerging infectious diseases can quickly spread and
even evolve into epidemics, including extended stays at
Hajj sites, crowded accommodations with other Hajj
pilgrims, many of whom are from developing nations,
and long periods of time spent in densely packed crowds
(crowd densities at Hajj have been estimated to be as
high as seven people per square meter).4 Any disease
outbreak at the Hajj could potentially be spread globally
by returning travelers though major airline hubs, which
Published 2012. This article is a U.S. Government work and is in the public domain in the USA. 1195-1982
Journal of Travel Medicine 2012; Volume 19 (Issue 3): 163–168
164
could become the settings for further dissemination of
disease.5
The 2009 Hajj took place during the influenza
A(H1N1) pandemic, which led to increased emphasis on
understanding ways to mitigate the potential spread of
respiratory disease.6 In order to address these concerns
KSA, with guidance from national and international
public health agencies such as the US Centers for Disease Control and Prevention (CDC), and the World
Health Organization (WHO), issued recommendations on measures to mitigate the impact of influenza
A(H1N1) among pilgrims performing the Hajj. The
recommended behaviors included washing hands often
(hand hygiene), use of hand sanitizers, wearing a face
mask, covering one’s cough or sneeze (cough etiquette),
staying away from sick people (social distancing), and
not touching objects touched by sick people (contact
avoidance).7,8 At the time the survey was developed,
CDC recommendations for high-risk people in crowded
settings where influenza A(H1N1) was circulating were
to avoid the setting, but if that was not possible, to consider wearing a face mask.9 The 2009 Hajj presented
an opportunity to evaluate behavioral interventions for
community mitigation of respiratory disease in the context of an extremely large and crowded mass gathering.
Our survey collected self-report data on protective
practices and respiratory illness among US travelers
to the 2009 Hajj. We hypothesized that travelers
who engaged in the recommended protective behaviors
would be more likely to have lower rates of respiratory
illness, as well as less severe illness and shorter duration
of illness, compared with pilgrims who did not engage
in protective behaviors.
Methods
Study Population
The sample in our survey represents approximately
2.0% of US pilgrims to the 2009 Hajj. US Hajj pilgrims in Michigan and Minnesota were administered
pre-travel surveys from October 21 to November 18,
2009; post-Hajj surveys were administered within 14
days of pilgrims’ return, from December 3, 2009,
to February 8, 2010. Participants in Minnesota were
recruited at a weekly clinic for Hajj travelers conducted
by HealthPartners, a Minnesota-based not-for-profit
health maintenance organization (HMO). Participants
in Michigan were recruited by the Arab Community
Center for Economic and Social Services (ACCESS)
at multiple settings, including mosques, community
health clinics, and the Detroit Wayne County International Airport, and telephone surveys were conducted
by health care workers in the language the participant
requested (English, Arabic, or Somali). All pre-Hajj surveys and 129 of the post-Hajj surveys were conducted
in person by health educators; the remaining 35 postHajj surveys were conducted by telephone by health
educators when in-person interviews could not be
J Travel Med 2012; 19: 163–168
Balaban et al.
arranged. All interviews were conducted whenever possible by medically trained persons from the same culture.
To ensure anonymity, no identifying information was
included on survey forms. Surveys were coded with a
survey identification number to allow pre- and posttravel surveys to be linked. This study was reviewed and
approved by the ethics review boards of all participating
institutions.
Survey Questionnaires
Surveys were developed and piloted by investigators at
the Travelers’ Health Branch of CDC, in conjunction
with investigators at the participating institutions. They
were vetted by health professionals from multiple
cultures and nationalities, including Somali, Egyptian,
Saudi, Palestinian, Lebanese, and Pakistani. The pretravel survey consisted of 60 items that assessed
demographics, travel itinerary and activities, previous
international travel, perceived health risks, health status,
sources of health information, seasonal and influenza
A(H1N1) immunization status, and knowledge of
influenza A(H1N1) symptoms, transmission and
prevention. The post-travel survey consisted of 36
items that assessed the (1) occurrence, (2) severity,
and (3) duration of any respiratory illness experienced
during Hajj and/or during the first 7 days after return
home from travel; protective behaviors during Hajj; and
exposure to health messages in KSA during Hajj.
An expanded definition of respiratory illness was
used for this study. Respiratory illness was defined as an
illness with the presence of one or more of the following
localizing signs or symptoms: cough, congestion, sore
throat, sneezing, or breathing problems. Two travelers
who reported ‘‘bronchitis’’ as a symptom were also
included. Severity of respiratory illness was calculated
by using a Likert scale from 0 (‘‘did not need to see a
doctor or nurse’’), to 1 (‘‘ill enough to see a doctor or
nurse’’), to 2 (‘‘needed to be hospitalized’’).
The protective behaviors assessed were five of the
community mitigation practices recommended by CDC
and WHO: hand hygiene, wearing a face mask, cough
etiquette, social distancing, and contact avoidance.7 – 9
Protective behaviors during Hajj were analyzed both as
categorical variables (whether the respondent reported
engaging in the behavior) and as continuous variables
(the number of behaviors reported by the respondent).
Analysis
Data were recorded by interviewers and then entered
in an Excel spreadsheet. Pearson correlation coefficients, ANOVAs, and chi-square tests were used to
assess variables and determine associations and correlations. Univariate factors with p values <0.2 were entered
into multivariable regression analyses. Two-tailed p values <0.05 were considered statistically significant in
multivariable models.
To analyze the effects of protective behaviors during
Hajj on respiratory illness, additional factors that have
been shown to influence compliance with relevant
165
Evaluation of Practices to Prevent Hajj Illness
health behaviors were also included in multivariable
models.10 The variables included in multivariable
models were (1) demographic and health factors: age,
gender, education, whether respondent was US-born,
health risk factors, seasonal influenza vaccination in the
previous 12 months, influenza A(H1N1) vaccination
prior to Hajj, and taking medication for respiratory
illness during or post-Hajj; (2) travel-related factors:
length of trip, international travel in the previous
12 months, and whether respondent had made a
previous Hajj; and (3) influenza A(H1N1) knowledge
and attitudes: if respondent received pre-travel health
information, level of influenza A(H1N1) knowledge,
perceived severity of influenza A(H1N1), and noticing
influenza A(H1N1)-related health messages during
the Hajj.
Influenza A(H1N1) knowledge was calculated as
the number of correct influenza A(H1N1) symptoms,
modes of transmission, and methods of prevention that
the respondent provided when asked. Perceived severity
of influenza A(H1N1) was calculated by asking respondents how serious a disease they felt influenza A(H1N1)
was on a Likert scale from ‘‘not serious’’ (defined as ‘‘like
a cold’’) to ‘‘very serious’’ (defined as ‘‘it can kill you’’).
Table 1 Demographic characteristics of 2009 Hajj pilgrims
from Michigan and Minnesota
Factor
n (%)
Age
Mean = 48.9 y (range 16–89)
Gender (female)
94 (50.5)
Country of birth
Lebanon
Iraq
Somalia
Pakistan
USA
Yemen
Egypt
Bangladesh
Palestine
Jordan
India
Kuwait
Ghana
Iran
Morocco,
United Arab Emirates
Years lived in US (if foreign-born)
64 (34.6)
40 (21.6)
21 (11.4)
17 (9.2)
13 (7.0)
6 (3.2)
5 (2.7)
4 (2.2)
4 (2.2)
3 (1.6)
2 (1.1)
2 (1.1)
1 (0.5)
1 (0.5)
1 (0.5)
1 (0.5)
Mean = 16.3 y (range 0.5–44)
Results
Pre-travel surveys were completed by 221 participants;
186 (84.2%) completed the post-Hajj survey after their
return (Table 1). Reasons for not completing post-Hajj
surveys included travelers not receiving a visa for Hajj
(which forced trip cancellation), travelers receiving a
visa but choosing not to go to Hajj, travelers making
extended visits to other countries lasting past the timeframe for the survey, and being lost to follow-up.
Analyses were conducted among the 186 participants
who completed both pre- and post-travel surveys.
The mean length of stay at Hajj was 24.1 days.
Protective behaviors during the Hajj were reported by
144 (77.4%) of the 186 respondents. Hand hygiene
was reported by 125 (67.2%), wearing a face mask by
91 (48.9%), cough etiquette by 86 (46.2%), social distancing by 64 (34.4%), and contact avoidance by 45
(24.2%). Seasonal influenza vaccination in the previous
12 months was reported by 138 (63.0%) respondents.
Influenza A(H1N1) vaccinations were reported by 72
(38.7%) respondents.
Respiratory illness during the Hajj and/or in the first
7 days post-Hajj was reported by 76 (41.3%) respondents (respiratory illness during Hajj = 32 (17.3%)
respondents and post-Hajj =53 (29.0%) respondents).
Among the 76 respondents who reported respiratory
symptoms, coughing was reported by 56 (73.7%), sneezing by 48 (63.2%), sore throat by 29 (38.2%), fever by
25 (31.1%), congestion by 16 (32.9%), breathing problems by 4 (5.3%), and ‘‘bronchitis’’ by 2 (2.6%). Of
the 76 respondents who reported respiratory illness,
18 (23.7%) met criteria for self-reported influenza-like
Education
Elementary or less
High school
University
Graduate or professional
Health risk factors
Low risk (age < 65 and no chronic
condition) (Chronic conditions
in the pilgrim population were:
diabetes, hypertension, and
asthma)
Age > 65, no chronic condition
Chronic condition, age < 65
Age > 65 and chronic condition
44 (23.8)
62 (33.5)
35 (18.9)
44 (23.8)
153 (82.3)
20 (10.8)
13 (7.0)
18 (9.7)
illness (ILI), defined as fever plus sore throat and/or
coughing.11
Three protective behaviors were associated with
reduced risk of respiratory illness: social distancing,
hand hygiene, and contact avoidance (Table 2). When
the number of protective practices was analyzed as a continuous variable, reduced risk of respiratory illness was
associated with engaging in more protective behaviors
during the Hajj (F = 3.13, p = 0.03) (Figure 1). Engaging in more protective measures was associated with
noticing influenza A(H1N1) health messages during the
Hajj (F = 6.93, p = 0.01).
Respiratory illness mild enough that the respondents
did not need to see a doctor or nurse was reported by 47
(65.3%) respondents, 23 (31.9%) were ill enough to see a
doctor or nurse, and 2 (2.8%) needed to be hospitalized.
No protective behaviors during Hajj were associated
with less severe respiratory illness. Reduced severity of
respiratory illness during Hajj was associated with fewer
years lived in the United States (F = 4.72, p = 0.01).
J Travel Med 2012; 19: 163–168
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Balaban et al.
Table 2 Protective behaviors and occurrence of respiratory
illness among 2009 Hajj pilgrims from Michigan and
Minnesota
Respiratory illness
Protective
behavior
Contact avoidance
Practiced
% reporting
illness
27.9% (12/43)
Not practiced
Cough etiquette
Practiced
43.0% (43/100)
Not practiced
Face mask
Practiced
39.7% (23/58)
Not practiced
Hand hygiene
Practiced
37.6% (32/85)
41.6% (37/89)
Odds ratio
(OR), 95% CI
p
OR = 0.51, 95%
CI = 0.24–1.11
0.06
OR = 0.92, 95%
CI = 0.46–1.82
0.47
OR = 1.42, 95%
CI = 0.70–2.88
0.21
OR = 0.36, 95%
CI = 0.14–0.94
0.03
OR = 0.44, 95%
CI = 0.22–0.90
0.02
33.3% (18/54)
35.0% (43/123)
Not practiced
Social distancing
Practiced
60.0% (12/20)
28.1% (18/64)
Not practiced
46.8% (37/79)
Figure 2 Protective behaviors reported during Hajj and
duration of respiratory illness.
factors also explained a significant proportion of variance in the duration of respiratory illness (r 2 =
0.13, F6,45 = 2.29, p = 0.05). When the number of protective practices was analyzed as a continuous variable,
engaging in more protective measures during Hajj was
correlated with shorter duration of respiratory illness
(r 2 = −0.307, p = 0.02 ) (Figure 2).
Discussion
Figure 1 Protective behaviors reported during Hajj and
occurrence of respiratory illness.
The mean duration of respiratory illness reported
during Hajj was 7 days (range = 1–21d). Practicing contact avoidance during Hajj was associated with shorter
duration of respiratory illness (F = 3.54, p = 0.06).
Shorter duration of respiratory illness during Hajj
was also associated with younger age (r 2 = 0.361, p =
0.002), fewer health risks (F = 3.99, p = 0.02), and
higher levels of perceived influenza A(H1N1) severity (F = 8.02, p < 0.001). A multivariable model contained two significant predictors of reduced duration
of respiratory illness: practicing contact avoidance
(β = −0.38, p = 0.01) and noticing influenza A(H1N1)
health messages during Hajj (β = 0.25, p = 0.06). These
J Travel Med 2012; 19: 163–168
Engaging in CDC- and WHO-recommended protective behaviors during the Hajj was a predictor of reduced
occurrence and duration of respiratory illness during
and after the Hajj. Pilgrims who practiced contact avoidance, social distancing, and hand hygiene during the
Hajj reported less respiratory illness. Practicing contact
avoidance was also associated with shorter duration of
respiratory illness.
The number of protective practices carried out by
pilgrims was also a predictor of Hajj-related respiratory
illness. Pilgrims who reported carrying out more protective practices during Hajj reported less illness and
shorter duration of illness (Figures 1 and 2). Although
engaging in multiple protective behaviors may have
a cumulative protective effect, it is likely that travelers who engaged in more behaviors might have been
better informed before and/or during travel and thus
more conscientious in practicing recommended behaviors. This hypothesis is consistent with the finding that
noticing influenza A(H1N1) health messages during the
Hajj was a predictor of the number of protective behaviors engaged in by pilgrims, and was also associated with
reduced occurrence and duration of respiratory illness.
These findings suggest that the influenza A(H1N1)
communications and education carried out by the KSA
during the 2009 Hajj may have been an important
component of efforts to mitigate illness among travelers to this mass gathering. Future evaluations of health
communications conducted during Hajj, combined with
objective observations of protective behaviors and confirmation of respiratory disease would help to delineate
the role played by health messages during the Hajj.
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Evaluation of Practices to Prevent Hajj Illness
Compared with other protective behaviors, wearing
face masks during Hajj seemed to have little protective
effect. Wearing a face mask was actually associated with
greater likelihood of respiratory illness. This finding is
consistent with previous findings that face masks either
offered no significant protection or were associated with
sore throat and with longer duration of sore throat and
fever symptoms among Hajj pilgrims,12 – 15 but in contrast to other studies that have found protective effects
of face masks at Hajj.16 Evidence for the efficacy of
face masks for preventing the transmission of influenza
is limited.17 In addition, a recent study of influenza
transmission suggests that poor face mask compliance
decreases their utility in mitigating the spread of disease,
and there is anecdotal evidence that many pilgrims at
the 2009 Hajj may not have worn masks correctly (eg,
mistakenly positioning the top of the mask below the
nose)18 (S. Ebrahim, personal communication). Since
our survey asked only if respondents had worn face
masks during Hajj, but did not ask whether masks had
been worn correctly or consistently, or what types of
masks were worn, it is not possible to determine the
effectiveness of face masks from our data.
The occurrence, symptoms, and severity of illness in
this population are consistent with previous studies of
Hajj travelers.3,12,13,19 – 22 The rates of ILI are consistent
with a study of French Hajj pilgrims and with previous
studies that have found 8.0–9.8% of Hajj pilgrims
with acute respiratory infection to have influenza.13,14,22
Pilgrims who reported respiratory illness during the
Hajj and those who reported post-Hajj illness were
not the same travelers: only 17% of travelers with
respiratory illness reported illness both during and after
the Hajj. This finding suggests that surveys that only
assess respiratory illness during or after mass gatherings
might risk underreporting the burden of respiratory
disease associated with mass gatherings.
The present study has several limitations. The study
population might not be representative of the Muslim population in the United States. Compared with
the US-Arab population, the study population had a
higher proportion of people of Iraqi (32 vs 4%) ancestry
and a lower proportion of Egyptian (3 vs 11%), and
Syrian ancestry (0 vs 10%).23 Nor could we systematically evaluate the effects of pre-Hajj health information,
since there was no consistent communication or education outreach for Hajj travelers. Many respondents
were contacted during pre-Hajj clinic visits, leading
to confusion over whether the visit itself was also
a source of pre-Hajj health information. Finally, all
health information was collected by self-report and so
could not be independently corroborated, although selfreported symptoms of respiratory illnesses have shown
close congruence with physician documentation.11 It is
also unclear whether self-reported duration of illness
corresponds to actual severity of respiratory infection
(ie, greater viral load). This association likely represents
a subjective measure of respondents’ perceived severity
of their illness.
Our findings highlight the role that both protective behaviors and health communications can play in
mitigating respiratory illness, even during extremely
large and densely crowded mass gatherings such as the
Hajj. Our study also demonstrates the value of conducting enhanced surveillance of international travelers
both during and immediately after large mass gatherings. The fact that more than 40% of pilgrims reported
respiratory illness during or after the Hajj illustrates the
potential for Hajj pilgrims to be a major contributor
in the international transmission of respiratory disease.
The possible role of mass gatherings in the worldwide spread of respiratory disease is highlighted by a
recent study speculating that a large Easter mass gathering of two million people in Iztapalapa, Mexico City
may have been a key contributing factor in the rapid
spread of influenza A(H1N1) throughout Mexico at the
beginning of the 2009 pandemic.24
Mass gatherings such as the Hajj pilgrimage provide
an opportunity to conduct large trials to evaluate the role
of communication campaigns and protective behaviors
in mitigating respiratory illness. Future research should
focus on prospective studies of predictors of protective
behaviors that also include objective confirmation of
respiratory disease. If KAP were assessed using reliable,
consistent instruments prior to and after travel to mass
gatherings, and observational and behavioral studies
of actual protective behaviors were conducted during
gatherings, it would be possible to better determine the
effectiveness of protective behaviors, and which factors
predict protective behaviors during travel. The results
from these types of studies could then be used to develop
evidence-based interventions to help prepare for future
pandemics.
Declaration of Interests
The authors state they have no conflicts of interest to
declare.
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