key: cord-0994008-0nrejsgr
authors: Alqahtani, Amani S.; Wiley, Kerrie E.; Tashani, Mohamed; Willaby, Harold W.; Heywood, Anita E.; BinDhim, Nasser F.; Booy, Robert; Rashid, Harunor
title: Exploring barriers to and facilitators of preventive measures against infectious diseases among Australian Hajj pilgrims: cross-sectional studies before and after Hajj
date: 2016-02-10
journal: Int J Infect Dis
DOI: 10.1016/j.ijid.2016.02.005
sha: cd05be991e31e44acba14989bdfe61c4a2ceb860
doc_id: 994008
cord_uid: 0nrejsgr

OBJECTIVE: For reasons that have yet to be elucidated, the uptake of preventive measures against infectious diseases by Hajj pilgrims is variable. The aim of this study was to identify the preventive advice and interventions received by Australian pilgrims before Hajj, and the barriers to and facilitators of their use during Hajj. METHODS: Two cross-sectional surveys of Australians pilgrims aged ≥18 years were undertaken, one before and one after the Hajj 2014. RESULTS: Of 356 pilgrims who completed the survey (response rate 94%), 80% had the influenza vaccine, 30% the pneumococcal vaccine, and 30% the pertussis vaccine. Concern about contracting disease at Hajj was the most cited reason for vaccination (73.4%), and not being aware of vaccine availability was the main reason for non-receipt (56%). Those who obtained pre-travel advice were twice as likely to be vaccinated as those who did not seek advice. Of 150 pilgrims surveyed upon return, 94% reported practicing hand hygiene during Hajj, citing ease of use (67%) and belief in its effectiveness (62.4%) as the main reasons for compliance; university education was a significant predictor of hand hygiene adherence. Fifty-three percent used facemasks, with breathing discomfort (76%) and a feeling of suffocation (40%) being the main obstacles to compliance. CONCLUSION: This study indicates that there are significant opportunities to improve awareness among Australian Hajj pilgrims about the importance of using preventive health measures.

The transmission of infectious diseases is high at mass gatherings such as the annual Hajj pilgrimage in Makkah, Saudi Arabia. 1 Hajj is the largest annual mass gathering on the planet, with around two to three million people attending from over 180 countries. Intense congestion, shared accommodation, air pollution, and compromised hygiene all contribute to the transmission of infections at Hajj, most notably acute respiratory infections (ARIs). 1, 2 Hajj presents a public health challenge for Saudi Arabia, as the authorities need to cater for an increasing number of pilgrims and respond to emerging infections such as the Middle East respiratory syndrome coronavirus (MERS-CoV). 3, 4 It is also challenging for the countries sending pilgrims, since these pilgrims can import epidemic diseases to their home countries upon return. In an effort to reduce the risk of infectious diseases at Hajj, an array of preventive measures have been recommended by the Saudi Arabian Ministry of Health (MoH), which include vaccination and hygiene measures (Table 1) . 5 However, studies have demonstrated that vaccine uptake and compliance with hygiene and protective measures are highly variable among pilgrims, 6, 7 and the reasons behind this variability remain unclear.

To date few studies have assessed the knowledge, attitudes, and beliefs in relation to preventive measures among Hajj pilgrims. A recent qualitative study of Australian pilgrims found that considerable misconceptions about preventive measures and the risk of respiratory infections prevail among Hajj pilgrims. 8 A French study demonstrated that less than half of pilgrims were aware of social distancing and facemask use as precautions against respiratory infections, 9 but no study has explored the barriers to and facilitators of the uptake of preventive measures. To address these questions, two cross-sectional surveys were conducted among Australian pilgrims, one before and one after the Hajj 2014, to identify what preventive advice and interventions pilgrims received before travel, and what factors influenced their compliance with these measures while they were there.

Two cross-sectional self-administered questionnaires were distributed among Australian Hajj pilgrims aged !18 years in 2014. The first survey was conducted on a group of departing pilgrims approximately 1 month before Hajj (pre-Hajj study). The second survey was conducted on a second, separate group of pilgrims immediately after their return to Australia (post-Hajj study).

The pre-Hajj survey collected data on socio-demographic characteristics, Hajj itinerary details, and the receipt of pre-travel advice, including vaccinations. The questionnaire also assessed the pilgrims' knowledge of and attitudes towards preventive measures, and their risk perception of diseases occurring at Hajj, including influenza, pneumonia, and blood-borne diseases.

The post-Hajj questionnaire assessed the actual compliance with infection control measures (such as the use of facemasks, hand disinfectants, and handkerchiefs) during Hajj, and the barriers to and facilitators of the use of those preventive measures while at Hajj. The surveys were primarily in English, with Arabic translations available for those who preferred to complete the survey in Arabic.

Muslims residing in the Greater Sydney area, New South Wales (NSW) were the target population for the study. NSW has the largest Muslim population (50%) of any state in Australia with the majority living in Greater Sydney. 10 Australian Hajj pilgrims aged 18 years and over who were planning to attend the Hajj 2014 were eligible for recruitment. Potential participants were approached through Hajj tour operators. The list of accredited Hajj travel agents in Australia, including their location/address, was obtained from the Saudi Arabian Embassy in Canberra, Australia. The selection of participants was based on the number of Hajj visas allocated for a given travel agent: travel agents with the highest quota of Hajj visas were approached first, and the travel agents who dealt with diverse ethnic groups, including Arabs, Africans, Indians, and Malays, were prioritized to ensure a diverse sample.

For the pre-Hajj survey, departing pilgrims were approached at weekly pre-Hajj seminars run by travel agents between August 1 and mid-September 2014. All pilgrims attending the seminars were invited to take part in the study.

For the post-Hajj survey, a second group of pilgrims (separate to the first) were approached in person at community gatherings and events within weeks of returning home from Hajj (between mid-October and the end of December 2014). The study was promoted using a number of methods, including the distribution of brochures at mosques and community centres and by word of mouth.

A consecutive sampling plan was used to ensure a sample that was representative of pilgrims residing in NSW. Assuming that at least 70% of respondents will have a general knowledge of infection control measures, and considering an error margin of 5% to be acceptable for this anonymous survey, a sample of 323 was considered to be sufficient for this study; assuming a noncompletion rate of the survey of 15-20%, a total of 380 participants were targeted. The sample size of this study represents approximately 10% of Australian pilgrims to Hajj 2014 (which is approximately 3500). Previous works studying the uptake of vaccinations among Australian Hajj pilgrims showed that a convenience sample of 10% of the target population is sufficient.

The data collected were entered into an Excel spreadsheet. The statistical analysis was performed using IBM SPSS Statistics version 19.0 (IBM Corp., Armonk, NY, USA). Pearson correlation coefficients and Chi-square tests were used to assess variables and determine associations and correlations. Univariate factors with p-values of <0.25 were entered into multivariable regression analyses. Twotailed p-values of 0.05 were considered statistically significant in the multivariable models.

This study was reviewed and approved by the Human Research Ethics Committee (HREC) at The University of Sydney (Project No. 2014/599).

A total of 380 respondents agreed to participate in the study, of whom 356 (94%) completed the survey questionnaires. Their demographic details are presented in Table 2 . Eighty-two percent of pilgrims (291/356) were attending Hajj for the first time, and the median duration of their stay in Saudi Arabia was 27 (range 7-40) days.

All respondents reported receiving meningococcal vaccine; the majority (83%, 297/356) also received one or more other recommended vaccines (Table 3) . Factors influencing vaccine uptake are listed in Table 3 . Being aged >40 years was significantly associated with the uptake of recommended vaccines (odds ratio (OR) 2.5, 95% confidence interval (CI) 1.2-4.9, p = 0.01), as was having a university education (OR 3.4, 95% CI 1.7-6.7, p = 0.01).

Approximately two thirds (236/356) obtained 'professional travel health advice' from one or more sources before Hajj, including 57% (182/236) from general practitioners (GPs), 24% (55/ 236) from a specialist travel clinic, 12% (27/236) from a specific Hajj website (e.g., MoH website 11 ), and 11% (25/236) from the 'Smartraveller' website. 12 Of those who received professional pretravel advice, 81% (191/236) reported a positive experience with the advice, while the rest described a negative experience.

One third (120/356) did not seek any 'professional travel health advice' before Hajj. Reasons for not seeking pre-travel advice included not recognizing the need to seek such advice (47%, 56/ 120), preference for other sources, i.e., friends, family members, and travel agents (32%, 39/120), reliance on previous experience/ knowledge (14%, 17/120), and previous negative experience of seeking pre-travel advice (7%, 8/120). Being within the age band of 34 to 49 years was the only factor associated with receiving professional pre-travel advice (OR 2.5, 95% CI 1.5-4, p = 0.01).

Additional pre-travel health advice sources were also reported, including Hajj travel leaders (66%, 235/356), family members and friends who had previous experience of performing Hajj (45%, 161/ 356), and 'general websites' on the Internet (17%, 59/356). Fortysix percent (164/356) were aware of the annual Hajj health recommendations issued by the Saudi MoH.

Additionally, pilgrims who sought pre-travel advice from GPs (OR 1.9, 95% CI 1-3.5, p = 0.03) or tour group leaders (OR 2.1, 95% CI 1.1-3.8, p = 0.01) before travelling to Hajj were twice as likely to be vaccinated as those who did not.

Pilgrims were reportedly concerned about food poisoning (61%, 217/356), diarrhoea (59%, 210/356), influenza (58%, 206/356), blood-borne diseases (49%, 173/356), skin diseases (45%, 160/356), and pneumonia (33%, 117/356). However, there was no association between the level of concern about influenza, pneumonia, and blood-borne diseases and the uptake of the influenza, pneumococcal, and hepatitis B vaccines, respectively (all p-values >0.2).

A total of 150 returned pilgrims were surveyed. Their demographic characteristics are presented in Table 2 . A large proportion of pilgrims (79%, 118/150) had performed Hajj for the first time. They had stayed for a median duration of 25 (range 7-35) days.

The majority of participants, 71% (107/150), believed hand washing (with water only) to be the most effective measure to protect oneself from respiratory infections, while the uses of alcoholic hand rubs (37%, 56/150) and facemasks (35%, 52/150) were considered to be less effective. Only beliefs about the effectiveness of facemasks and hand washing with water and soap were significantly associated with their actual use (p < 0.01) ( Table 4 ).

Half of the pilgrims (53%, 80/150) used facemasks to protect themselves from infectious diseases during Hajj at least three times a day. Participants described three major reasons for facemask use: protection from disease (76%, 61/80), protection from air pollution (58%, 46/80), and belief that facemasks are effective in preventing ARIs (41%, 33/80). Less than half (47%, 70/ 150) did not use a facemask. The reasons for non-compliance were breathing discomfort (76%, 53/70), feeling of suffocation (40%, 28/ 70), and thinking it was not necessary (31%, 22/70). In addition, none of the demographic characteristics were associated with facemask compliance (all p-values >0.25) and therefore these were not entered into multivariable regression analyses.

A subgroup of women (n = 76) answered questions on their use of the niqab (traditional face veil); of those who responded, 49% (37/76) used only facemasks, 34% (26/76) used only the niqab, and 20% (15/76) used both a facemask and the niqab. Of those who used the niqab (either alone or with a facemask), 51% (21/41) reported that they did so because it is 'airy' and easier to breathe and 39% (16/41) felt that it was comfortable to use.

Almost all (94%, 141/150) practised some kind of hand hygiene during Hajj. This included hand washing with soap (73%, 110/150), hand washing with water only (55%, 82/150), and alcoholic hand disinfectant (31%, 46/150). Reasons influencing the pilgrims' decision to use these methods included belief in the effectiveness of hand hygiene in preventing infectious diseases (67%, 94/141) and convenience and ease of use (62.4%, 88/141). Additionally, those with a university education were more likely to use hand hygiene measures than those without (OR 7.9, 95% CI 1.4-42.9, p = 0.01).

Respondents reported using other preventive measures including disposable handkerchiefs (53%, 79/150), avoiding dense crowding (29%, 43/150), avoiding contact with symptomatic people (39%, 58/150), and practicing hand washing after touching the ill (30%, 45/150).

This appears to be the first in-depth quantitative study comparing the health knowledge attitudes, beliefs, and practices of departing and returning Hajj pilgrims regarding preventive measures against infectious diseases. This study found that 14 and France where the vaccination rate for 2014 was zero due to vaccine non-availability, 15 and compares well with the overall vaccination rates among international pilgrims over recent decades, which range between 0.7% and 100%. 6, 16 Influenza vaccine aside, the uptake of other recommended vaccines was low. For instance, the uptake of pneumococcal vaccine was only 30%. Previous Australian and international surveys have reported coverage rates ranging from 2.5% to 36%. 6, 17 This is concerning because pneumonia is the leading cause of hospital admission and an important cause of mortality at Hajj. [18] [19] [20] Furthermore, surveys have shown that many pilgrims were not aware that pneumonia is transmissible 21 and preventable by vaccination. 22 There is currently no formal guidance from the Saudi MoH on the use of pneumococcal vaccine for Hajj pilgrims, which may partly explain this apparent lack of awareness (Table 1) . 23 The uptake of pertussis vaccine was 30%, compared with 10.6% among French Hajj pilgrims in 2005. 24 Additionally, the coverage for hepatitis A and B vaccines were each 17%, which is higher than the 11.5% uptake for hepatitis A reported among French pilgrims in 2005, 24 and the 6% each for hepatitis A and B among Saudi pilgrims in 2010. 25 While a large proportion of Hajj pilgrims are from countries with intermediate to high hepatitis B virus (HBV) prevalence, the risk of contracting HBV at Hajj is not well studied. 26, 27 It is known that a significant proportion of pilgrims engage in high-risk behaviours; for example it was found that about 43% of male pilgrims shaved their heads with reused razors, 28 or had their heads shaved by non-professional (unlicensed) barbers. 25 Other studies have also reported high-risk behaviours that increase the risk of hepatitis A, including buying and eating food from street vendors. 29 Despite this, hepatitis A and B vaccines are not listed in the Saudi MoH recommendations for Hajj pilgrims (Table 1) . 23 In this study, polio vaccine uptake was 8%, which is low compared with the uptake among French pilgrims in 2006 (15%), 30 and the uptake among pilgrims from other non-endemic countries in 2013 (43%). 31 Typhoid vaccine coverage was 13% in this study, which compares well with the uptake rate of 9% among international pilgrims in 2002. 32 The present study appears to report MMR (measles, mumps, and rubella) vaccine uptake (10%) for the first time.

The participants cited several reasons for not receiving the recommended vaccines, the most common being that they were unaware that the vaccines were recommended. These results are consistent with the findings of Memish et al., who reported a lack of knowledge to be a significant factor for poor uptake of the seasonal influenza vaccine among pilgrims. 33 Conversely, previous Australian studies have reported reliance on natural immunity as the main reason for not being vaccinated against influenza in 2011, while low risk perception of contracting influenza was the main reason in 2012. 13 A unique finding of this study is that pilgrims who received pretravel advice from GPs and Hajj tour group leaders were twice as likely to be vaccinated as those who did not receive such advice. Barasheed et al. found that receiving advice from Hajj group leaders was the main motivator for the uptake of influenza vaccine among Australian Hajj pilgrims in 2012. 13 This survey also revealed that older pilgrims (aged >40 years) were more likely to take up the recommended vaccines. Similarly, Gautret et al. demonstrated that influenza vaccine coverage increased with age in French pilgrims. 24 This could be due to the fact that older people are more aware of their health, or it could be due to an increasing number of pre-existing illnesses as people age. Another study among French pilgrims found that 'at risk' pilgrims were significantly more likely to be advised to receive pneumococcal vaccine than those who were not 'at risk'. 22 This may explain why vaccine uptake has been found to increase with age in some studies. 24, 34 Although respiratory infections are the most common diseases during Hajj, 1 the participants in this study were more concerned about food-borne illness than ARIs. Limited knowledge and perception of diseases among pilgrims has been found in other studies; an Australian study found that 42% of pilgrims in 2014 were not aware that pneumonia can be transmissible. 21 Similarly, French pilgrims in 2014 did not perceive pneumonia as a severe condition, and were not aware of the existence of a vaccine against it. 22 No association was found between the disease risk perception for influenza, pneumonia, and hepatitis B and the uptake of the respective vaccines. This contradicts other data, which demonstrated that an increased risk perception of pandemic influenza A (H1N1) was significantly associated with influenza vaccine uptake among US pilgrims in 2009. 35 Almost all of the participants in the present study used some kind of hand hygiene; this was higher compared with French pilgrims in 2013 (50%). 36 More than half of the pilgrims used facemasks in this study, similar to French pilgrims in 2013. 36 Nevertheless, previous studies have reported that only half of the participants were aware of the availability of non-pharmaceutical preventive measures against respiratory infections. 9, 33 Belief that hand hygiene is easy to use and effective in preventing infections were the main reasons for uptake among the present sample. Conversely, facemasks were less accepted. Among non-users, discomfort and difficulty in breathing were barriers to their use. Those who used facemasks believed that they were effective in preventing infectious diseases. Similar quantitative findings have been reported among members of the general Singaporean community, 37 but not previously among Hajj pilgrims. Another important factor identified as a driver for the use of facemasks was protection from air pollution. A recent study found that the air pollution level in Makkah during the Hajj consistently exceeds internationally acceptable standards, 38 and therefore this perception is probably justified and could inform health promotion policy.

Thirty-four percent of female pilgrims in the present sample preferred to use a traditional face cover (niqab) to a facemask during Hajj. In contrast, other studies found that higher proportions (over 70%) of Saudi women preferred the niqab over facemasks at Hajj 2002 and 2003. 39, 40 In the exploration of why some women prefer using the niqab, it was found that comfort and breathability were contributing factors.

In this study, two thirds of pilgrims sought pre-travel advice from health professionals; this is similar to the results of a survey that found that 65% of Arab pilgrims received health advice before departing to Hajj. 41 GPs were the most cited sources, followed by specialist travel clinics. This result is supported by a study that found GPs to be the most trusted sources of health advice among Australian pilgrims in 2014. 21 Interestingly, only 12% of the present sample sought advice from the Saudi MoH website. This is different to the findings of a study that showed the Saudi MoH to be the main source of health information among pilgrims from Arab countries (69%). 41 This difference may be due to language barriers.

Not recognizing the need to seek pre-travel health advice and the preference for other information sources (i.e., friends, family members, and travel agents) were the main barriers to seeking professional pre-travel advice. These results support the findings of a recent Australian study, which also demonstrated a high level of confidence in advice from non-health professional sources such as family, friends, and travel agents. 8 The present study identified that being aged between 34 and 49 years was the only factor significantly associated with seeking pre-travel health advice. Therefore, enhancing awareness among other groups of Hajj pilgrims, especially elderly adults and those with pre-existing illnesses, about the importance of seeking professional pre-travel advice could be an important strategy to improve the uptake of preventive measures. Moreover, providing GPs with culturally appropriate health information on Hajj and the preventive measures recommended by the Saudi MoH could also facilitate uptake. 42 This study has some limitations. Two different groups were surveyed and the groups showed significant differences in demographic characteristics, particularly in sex, education level, and country of birth. Also, the sample size of the post-Hajj group was smaller than intended. These could limit the generalizability of the findings of one group to the other. These limitations are being addressed by a second, larger cohort study among Australian pilgrims during Hajj 2015, and a qualitative study among GPs and tour group leaders is underway. Despite these limitations this study has uniquely identified the barriers to and facilitators of the uptake of preventive measures among Australian Hajj pilgrims, providing important preliminary data upon which to build.

This study shows that there are significant opportunities to improve awareness among Hajj pilgrims about the importance of using preventive health measures and indicates the need for better communication of official health information from the Saudi MoH to a broader international audience.

Conflict of interest: Professor Robert Booy has received funding from Baxter, CSL, GSK, Merck, Novartis, Pfizer, Roche, Romark, and Sanofi Pasteur for the conduct of sponsored research, travel to present at conferences, or consultancy work; all funding received is directed to research accounts at The Children's Hospital at Westmead. Dr Anita E. Heywood has received grant funding for investigator driven research from GSK and Sanofi Pasteur. Dr Harunor Rashid received fees from Pfizer and Novartis for consulting or serving on an advisory board. The other authors have no competing interests to declare.

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