Australian Chinese Travellers Visiting Friends and Relatives: New Approaches to Understanding and Reducing Infectious Disease Risks

Australian Chinese travellers visiting friends and relatives: new approaches to understanding and reducing infectious disease risks

Tara Elaina Chun Hin Ma

Submitted for the degree of Doctor of Philosophy

School of Public Health and Community Medicine Faculty of Medicine University of New South Wales, Sydney, Australia

April 2016

PLEASE TYPE THE UNIVERSITY OF NEW SOUTH WALES Thesis/Dissertation Sheet

Surname or Family name: Ma

First name: Tara Other name/s: Elaina Chun Hin

Abbreviation for degree as given in the University calendar: PhD

School: School of Public Health and Community Medicine Faculty: Medicine

Title: Australian Chinese travellers visiting friends and relatives: new approaches to understanding and reducing infectious disease risks

Abstract 350 words maximum: (PLEASE TYPE)

Travellers are an important vector in the global spread of infections. China has been the source of multiple pandemics over the past century, spread globally via travel. Travellers visiting friends and relatives (VFR) are at an increased risk of ma ny infectious diseases compared to other travellers. Therefore, returned Chinese VFR travellers are a potentially important source of importation of emerging infectious diseases to countries with large Chinese migrant populations, including Australia. This thesis aimed to understand the knowledge, attitudes and practices (KAP) of Australian Chinese VFR travellers around internationa l travel, and to study travel health-related behaviours both before and during travel, to identify areas for intervention.

The thesis has three components. The first study consists of five focus groups with Chinese-Aust ra lian VFR travellers from t he general community. The second study consists of two focus groups involving Chinese international students. The third study focuses on KAP of infectious disease outbreaks through integrating an in-depth literature review of outbreak risks in China with data from all seven focus groups, and exploring the implications of the combined findings. In each focus group, topics relating to pre-travel health preparations, actual and intended health-related behaviour during travel and during outbreaks, and general health-related KAP were explored.

The research identified low risk-perception and sub-optimal travel health behaviours, both pre-travel and during travel, among Austra lian Chinese VFR travellers, and identified important cultural and belief system reasons for this. They often undertook activities and consumed commercially prepared meals with family and friends in China, who were also their most important source of t ravel advice. Simi lar findings were identified amongst international students, with additional unique findings including common use of social media for healt h information. Chinese VFR travellers and international stud ents were inadequately prepared for disease outbreaks experienced during past travel, and likely to be underprepared for future travel. China has been and will likely continue to be an important source of pandemics. This research highlights the importance of Chinese VFR travellers as potential vectors. Overall, this research provides new insights into Chinese VFR travellers, which can be used to tailor prevention programs for this group of at-ri sk travellers.

Declaration relating to disposition of project thesis/dissertation

I hereby grant to the University of New South Wales or its agents the right to archive and to make available my thesis or dissertation in whole or in part in the University libraries in all forms of media, now or here after known, subject to the provisions of the Copyright Act 1968. I retain all property rights, such as patent rights. I also retain the right to use in future works (s uch as articles or books) all or part of th is thesis or dissertation.

I also authorise University Microfilms to use the 350 word abstract of my thesis in Dissertation Abstracts International (this is applicable to doctoral theses onlv). l

The University recognises that there may be exceptional circumstances requiring restrictions on copying or conditions on use Requests for restriction for a period of up to 2 years must be made in writing. Requests for a longer period of restriction may be considered in exceptional circumstances and req uire the approval of the Dean of Graduate Research.

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I hereby declare that this submission is my own work and to the best of my knowledge it contains no materials previously published or written by another person, or substantial proportions of material which have been accepted for the award of any other degree or diploma at UNSW or any other educational institution, except where due acknowledgment is made in the thesis. Any contribution made to the research by others, with whom I have worked at UNSW or elsewhere, is explicitly acknowledged in the thesis. I also declare that the intellectual content of this thesis is the product of my own work, except to the extent that assistance from others in the project’s design and conception or in style, presentation and linguistic expression is acknowledged.

Tara Ma 15 April 2016

‘I hereby grant the University of New South Wales or its agents the right to archive and to make available my thesis or dissertation in whole or part in the University libraries in all forms of media, now or here after known, subject to the provisions of the Copyright Act 1968. I retain all proprietary rights, such as patent rights. I also retain the right to use in future works (such as articles or books) all or part of this thesis or dissertation. I also authorise University Microfilms to use the 350 word abstract of my thesis in Dissertation Abstract International (this is applicable to doctoral theses only). I have either used no substantial portions of copyright material in my thesis or I have obtained permission to use copyright material; where permission has not been granted I have applied/will apply for a partial restriction of the digital copy of my thesis or dissertation.'

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‘I certify that the Library deposit digital copy is a direct equivalent of the final officially approved version of my thesis. No emendation of content has occurred and if there are any minor variations in formatting, they are the result of the conversion to digital format.’

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Date ……………………………………………...... This thesis is dedicated to my mother and father.

iv Acknowledgements

I would like to thank my supervisors Dr Anita Heywood and Professor Raina MacIntyre for their continued supervision and assistance over the course of conducting this research and writing this thesis. Your ongoing comments and critiques and the discussions we had during our regular meetings were very helpful. I have learnt so much from both of you, and for this I am very grateful.

I would like to thank the wonderful staff at the School of Public Health and Community Medicine, UNSW Australia. Your assistance was of great help in photocopying materials for the focus groups, and arranging various administrative matters with the School.

I would like to thank the UNSW library and its dedicated librarians for the help they provided me during the literature reviews, and for their assistance in locating several books I had wanted to borrow over the years but could not find on the shelf.

I would also like to thank Willoughby City Council and Ashfield City Council for providing the venues for the community focus groups. Having access to convenient venues located in suburbs with substantial Chinese-speaking populations was vital to the success of recruiting participants for the focus groups.

Professional editor, Donna Armstrong, provided copyediting and proofreading services, according to the guidelines laid out in the university-endorsed national Guidelines for editing research theses.

Finally, I would like to thank my family for their continued emotional support and encouragement throughout the course of writing this thesis.

v Ethics clearance

Approval for conducting the focus groups was granted by the Medical and Community Human Research Ethics Advisory Panel of UNSW Australia, in November 2012 (Reference number: 2012- 7-40). The approval was granted for 12 months, covering the period in which all focus groups were conducted.

vi Publication arising from this thesis

Ma T, Heywood A, MacIntyre CR. Chinese travellers visiting friends and relatives: a review of infectious risks. Travel Medicine and Infectious Disease 2015;13(4):285-94.

This article is provided in Appendix 3.

vii Contents

Acknowledgements ...... v Ethics clearance ...... vi Publication arising from this thesis ...... vii Abbreviations ...... x Abstract ...... xi Guide to the thesis ...... xiii Chapter 1 Literature review ...... 1 1.1 Introduction ...... 2 1.2 Travellers visiting friends and relatives ...... 3 1.3 Travel health issues in ethnic Chinese travellers ...... 16 1.4 Infectious risks in China relevant to VFR travellers ...... 20 1.5 Health beliefs in Chinese culture ...... 28 1.6 Conclusions ...... 36 Chapter 2 Focus groups with Australian Chinese VFR travellers ...... 37 2.1 Abstract...... 38 2.2 Introduction ...... 40 2.3 Methodology ...... 41 2.4 Results ...... 46 2.5 Discussion ...... 62 2.6 Conclusions ...... 72 Chapter 3 Focus groups with Chinese international students ...... 74 3.1 Abstract...... 75 3.2 Introduction ...... 77 3.3 Methodology ...... 79 3.4 Results ...... 80 3.5 Discussion ...... 91 3.6 Conclusions ...... 100 Chapter 4 Outbreaks of infectious disease in China – literature review and focus group analysis . 102 4.1 Abstract...... 103 4.2 Introduction ...... 105 4.3 Methodology ...... 106

viii 4.4 Results ...... 108 4.5 Discussion ...... 122 4.6 Conclusions ...... 129 Chapter 5 Conclusions ...... 130 5.1 Introduction ...... 131 5.2 Key findings from this research ...... 132 5.3 Implications and future recommendations ...... 137 5.4 Strengths and limitations of this research ...... 150 5.5 Conclusions ...... 153 Appendix 1 Literature review search strategy ...... 154 Appendix 2 Focus group guide, demographic survey form, and participant information and consent form ...... 155 Appendix 3 Publication arising from this thesis ...... 163 References ...... 165

ix Abbreviations

CDC Centers for Disease Control and Prevention (USA) CoxA16 Coxsackievirus A16 EV71 Enterovirus 71 GP General practitioner HBM Health Belief Model HPV Human papillomavirus HPAI highly pathogenic avian influenza MDR-TB Multidrug-resistant tuberculosis PBS Pharmaceutical Benefits Scheme SARS Severe acute respiratory syndrome UNSW University of New South Wales VFR Visiting friends and relatives WHO World Health Organization XDR-TB Extensively drug-resistant tuberculosis

x Abstract

Travellers are an important vector in the global spread of infections and importations of infectious diseases with outbreak potential by travellers is a challenge to national disease control efforts. Travellers should be made aware of the infectious risks surrounding their travel and adequate preventive behaviour should be encouraged to prevent infections while travelling, and to protect contacts back in their country of residence. Travellers who visit friends and relatives (VFR) in their country of origin are at an increased risk of many infectious diseases compared to other travellers. Because China has been the source of multiple pandemics over the past century, and will likely continue to be an important source of infectious diseases with pandemic potential, Chinese VFR travellers are an important at-risk population group and a potential source of imported infectious diseases to the many countries around the world with sizeable Chinese migrant populations, including Australia. The overarching aim of this thesis is to explore the knowledge, attitudes and practices of Australian Chinese VFR travellers around international travel, including travel health preparations and travel health-related behaviours both before and during travel, to identify areas for intervention.

This thesis comprises three components. Focus groups with migrant Chinese Australians from the general community explored topics relating to pre-travel health preparations, actual and intended health-related behaviour during travel, and general health-related knowledge, attitudes and practices relevant to travel health. Focus groups with Chinese international students explored similar issues, but in the unique context of this population. An in-depth literature review of outbreak risks in China was then integrated with the focus group data specific to attitudes and travel behaviour during outbreaks of infectious diseases.

The research identified low risk perception and suboptimal travel health preparation and behaviours among Australian Chinese VFR travellers. Reasons for this included factors related to culture and belief systems, undertaking activities and consuming commercially prepared meals with family and friends in China, and the strong influence of family and friends in both pre-travel preparations and behaviour during travel. Similar findings were identified among international students, with additional unique findings including a view of VFR travel as ‘returning home’ and the common use of social media for accessing health information. Chinese VFR travellers had sometimes taken inadequate precautions regarding disease outbreaks in the past, including refusal to cancel non- essential travel as per WHO advice and not using face masks in public, and often expressed the intention to do the same regarding hypothetical future outbreaks.

xi Findings from this thesis provide new insights into Chinese VFR travellers and highlight the importance of educational interventions to raise risk awareness and encourage adequate preventive behaviour regarding VFR travel, especially during outbreaks. These findings can inform the development of health promotion and health education tailored to this group of at-risk travellers.

xii Guide to the thesis

International travel has long been associated with the emergence of infectious diseases and the spread of pandemics (1). Acquiring an infectious disease during travel not only places the individual traveller at risk but may also result in the importation, and possibly local spread, of the disease when they return to their country of residence. Preventing infectious diseases in travellers is therefore an important national disease control issue for countries like Australia with comparatively low disease incidence. Moreover, in modern times, international air travellers are an important potential vector in the rapid international spread of major pandemics (2, 3), which can have a major economic and social impact on affected countries (4-10). China has been the source of multiple pandemics over the past century, including the SARS outbreak in 2003 (2, 3, 11). SARS was introduced into many other countries via travellers, including into Canada via a returning VFR traveller (12). There is therefore the potential for emerging infectious diseases to be imported into countries like Australia by travellers to and from China.

Travellers whose main purpose of travel is for visiting friends and relatives constitute a substantial proportion of all outbound travellers from Australia (13). This proportion is rising due to both increasing immigration and a decline in the cost of air travel (14). VFR travellers are at an increased risk of contracting certain infectious diseases, including malaria, hepatitis and tuberculosis (15-18), during travel. There are several identified factors that contribute to this increased risk, including the circumstances of their travel and the activities they undertake during travel which place them at similar infectious disease risk to the local population compared to other travellers (14, 19). Comprehensive pre-travel consultations with health providers includes provision of a range of recommendations for vaccinations, prophylaxis and other precautionary health behaviours that aim to reduce the risk of infectious diseases and other health problems during travel (20, 21). However, VFR travellers are less likely to seek pre-travel health advice compared to other travellers and subsequently may be under-vaccinated and under-prepared for travel, have lower risk perceptions and important knowledge gaps regarding infectious risks present in their travel destination, and fail to undertake adequate precautionary and preventive behaviours during travel (14, 16, 18, 19, 22- 24). VFR travellers are therefore an important group of travellers to address in efforts to promote adequate preventive travel health behaviours, and the adequate uptake of pre-travel medical consultations. Chinese VFR travellers, a currently under-researched population, are especially important in this regard due to the pandemic risks China poses. If we are to develop effective interventions aimed at improving Australian Chinese VFR travellers’ uptake of pre-travel health

xiii advice and preventive health behaviours, we first need to understand why and how Australian Chinese VFR travellers practice travel health. However, such knowledge is currently lacking in the published literature.

This thesis is organised as follows:

Chapter 1 contains a review of the literature covering four major topics relevant to the aims of this thesis. Section 1.1 describes the importance of travel medicine in public health and explains why VFR travellers deserve particular study. Section 1.2 reviews general VFR travel-related health issues. It defines VFR travellers and summarises the literature that provides evidence supporting their increased risk of certain infectious diseases and the reasons for this increased risk. Section 1.3 reviews the public health literature surrounding ethnic Chinese and international travel. It explores published data regarding the knowledge, attitudes and practices of Chinese travellers, and highlights issues that may be specifically relevant to Chinese travellers, including Australian Chinese VFR travellers. Section 1.4 reviews important infectious disease risks in China including hand, foot and mouth disease, hepatitis A, B, C and E, tuberculosis, Streptococcus suis, dengue fever, chikungunya, Japanese encephalitis, plague and some parasitic infections. Section 1.5 reviews general health beliefs and behaviours among ethnic Chinese that may impact VFR travel outcomes, including attitudes and behaviours regarding infectious diseases and vaccination in general, and beliefs and behaviours surrounding Western medicine, Chinese medicine and self-medication. The methodology of this literature review is described in Appendix 1.

Three research chapters follow the literature review, and present, in detail, the findings of this doctoral work. The study presented in this thesis contained three components, which addressed the aims of the thesis. The first component (Chapter 2) was a series of focus groups conducted at two sites in Sydney, Australia, involving Australian Chinese VFR travellers from the general community. The second component (Chapter 3) was a series of focus groups conducted at the University of New South Wales (UNSW Australia) with Chinese international students. Conducting focus groups comprised solely of international students allowed an international student-specific perspective in the exploration of travel health issues. This is important, as Chinese international students have a very different context of travel to other Chinese VFR travellers, and thus may have different needs and views. The third component (Chapter 4) focused on infectious disease outbreaks, integrating an in-depth literature review of outbreak risks in China with qualitative data from the focus groups on issues related to outbreaks and exploring the implications of these issues.

xiv

The conclusions arising from this thesis are presented in Chapter 5. The chapter summarises the main findings of this thesis, positioning the research contained in this thesis in the context of current studies. It also reviews the strengths and limitations of the studies contained in this thesis, and discusses the implications of the findings, provides recommendations arising from the findings, and potential future research directions. Appendix 2 contains the focus group participant information and consent form, the demographic survey form, and a copy of the focus group guide used across all focus groups. Appendix 3 contains a copy of a publication arising from this thesis.

Chapter 1: Literature review

Chapter 1 Literature review

1 Chapter 1: Literature review

This chapter comprises a review of the literature surrounding the topic of ethnic Chinese travellers visiting friends and relatives (‘VFR travellers’). There are currently no published studies specifically focusing on this population. However, this review will focus on VFR travellers in general, ethnic Chinese persons as travellers, the infectious disease risks present in China, and aspects of health beliefs and practices in ethnic Chinese that may be relevant to travel health, all topics of potential relevance to Chinese VFR travellers. The methodology for this literature review is described in Appendix 1.

1.1 Introduction

1.1.1 The importance of travel medicine in public health

International travel is an important vector for the spread of infectious diseases, especially with the high and increasing volume of international air travel (25). The spread of recent pandemics via international travellers has highlighted the importance of travel health as a public health priority for countries around the world (2, 3). Travel medicine is the branch of medicine which aims to improve travel health outcomes in travellers, and thus also reduce the international transmission of infectious diseases via travellers (26-29). One important function of travel medicine is to provide pre-travel health consultations for travellers (26, 27, 29). In such consultations, a detailed medical history is taken, and a detailed description of the proposed itinerary for travel is also discussed, so that an individualised assessment of travel-related health risks can be made (29). The patient is then provided with advice on the infectious risks present in their travel destination(s) and preventive measures that are recommended for these infectious risks (21, 29-31). The administration of vaccines and prescription of prophylactic medication, as indicated according to the infectious risks in the travel destination(s) and the immunization profile of the patient, is also an important part of the consultation (21, 26, 29). The World Health Organization (WHO) recommends that travellers to developing countries in particular should obtain pre-travel medical consultation (27).

Whilst pre-travel consultations have been found to be effective in reducing a variety of infectious risks (20), travellers have been found to generally have a low rate of uptake of such consultations, and therefore are sub-optimally prepared for their travel from a medical point of view (22, 26, 32). In light of the increasing frequency of international travel and associated potential for spread of emerging and re-emerging infections, it is more important than ever before that efforts are made to improve the travel health-related practices of international travellers, including the utilization of pre-travel health consultations (25). To develop effective interventions to this aim, we must first

2 Chapter 1: Literature review

understand any common deficiencies in their current practices, including the reasons for not seeking professional pre-travel health consultation (33).

1.1.2 The particular case of the traveller visiting friends and relatives

Travellers travelling from developed countries, such as Australia, to developing countries to visit friends and relatives are significantly contributing to the ongoing rise in international travel (14). But current literature shows that they have even lower rates of undertaking adequate pre-travel preparations than other travellers (22, 24, 33). They are also known to be at greater risk of travel- related infectious diseases and poor health outcomes, compared to other travellers (34, 35). Travel medicine has traditionally focussed on tourist and business travellers (36), and VFR travellers are currently not a well-studied population.

VFR travel is also important because it accounts for a substantial proportion of all travel. Globally, international travel for the purpose of visiting friends and relatives (including, but not limited to, VFR travellers as defined in the next section) accounted for a quarter of international tourist arrivals in 2012 (37), particularly originating from Western countries (13, 38). In 2011, 46% of outbound international travel by US residents was to visit friends and relatives (38), while the main purpose of travel for 23% of Australian resident departures in 2012 was for visiting friends and relatives (13). The proportion of travel for VFR purposes is also increasing, due to both an increase in global migration, especially from sources where there are no political or safety barriers for VFR travel, and the increased affordability of travel, reducing the economic barriers for frequent VFR travel (14).

1.2 Travellers visiting friends and relatives

1.2.1 Defining travellers who visit friends and relatives

The term ‘VFR traveller’ is often defined differently in different publications. Although is it most commonly understood in travel medicine that the term refers to immigrants who return to their country of origin to visit friends and relatives, travelling from high-income to lower-income countries (34) where their risk of infectious disease is greater (15-17), there is no one standard definition. Some authors have recommended that a broad definition be taken, including all “those whose primary purpose of travel is to visit friends or relatives and for whom there is a gradient of epidemiologic risk between home and destination, regardless of race, ethnicity, or administrative/legal status (e.g. immigrant)” (34). This definition would be broad enough to encompass children and spouses of immigrants not born in developing countries and hence do not

3 Chapter 1: Literature review

fit the classical immigrant picture of VFR travellers, but who may still experience the travel conditions commonly associated with immigrant VFR travel, and hence an increased risk of certain infections. This population would be excluded by narrower definitions, such as those including only first generation immigrants (34). However, this definition would also include some travellers travelling between developed countries, as well as some domestic travel within developed countries, extending it much further beyond the commonly accepted definition. This broad definition also introduces into the VFR category travellers with very different cultural, economic and attitudinal characteristics, compared with the classic VFR traveller definition (35, 39). To avoid this confusion, and to be consistent with the current literature, this broad definition will not be used for this study.

The US Centers for Disease Control and Prevention (CDC) defines VFR travellers in the following way (39):

A traveler categorized as a VFR is an immigrant, ethnically and racially distinct from the majority population of the country of residence (a higher-income country), who returns to his or her home country (lower-income country) to visit friends or relatives. Included in the VFR category are family members such as the spouse or children, who were born in the country of residence.

The CDC definition retains the common understanding that VFR travellers include only those travelling to lower-income countries, while specifically including non-immigrant family members who may also experience VFR travel-associated risks. It is the definition which will be used in this study.

1.2.2 The unique infectious risk profile of VFR travel

Travellers in general are at risk of acquiring and transmitting infectious diseases, both in the country to which they travel and upon their return. As VFR travellers are by definition travelling to lower- income countries, they are often at increased risk of certain infectious diseases not present in their country of residence and may introduce or re-introduce infections uncommon in their country of residence, upon their return (40-42). VFR travellers also have a different profile in terms of the risks of acquiring travel-related infectious diseases. They are at particular risk of acquiring certain diseases during their travel, and hence also at particular risk of importing these diseases back to their country of residence. A study of patients presenting for treatment for travel-related illnesses at the University Hospital of Zurich (part of the global GeoSentinel Surveillance Network collecting data from travel health and tropical medicine clinics) during a 17-month period, including 121 VFR

4 Chapter 1: Literature review

travellers and 217 other travellers, found that VFR travellers were more likely to be diagnosed with malaria and viral hepatitis, but less likely to present with acute diarrhoea, compared to other travellers (18). Furthermore, an analysis of data from the entire GeoSentinel database from November 1997 to December 2004, found that systemic febrile illnesses (including malaria), non- diarrhoeal intestinal parasitic infections, respiratory syndromes, tuberculosis and sexually transmitted diseases were more commonly diagnosed among ‘immigrant VFRs’ than among tourist travellers, but acute diarrhoea was less common (16). This study included data from multiple clinics treating travel-related illnesses around the world and including a total of 1813 ‘immigrant VFRs’ (VFR travellers who were born in other countries) and 10,021 tourist travellers. Other studies have also found VFR travellers to be at particularly high risk of acquiring hepatitis A (43-45), enteric fever (17, 45, 46), dengue fever (46) and malaria (15, 45, 46) and other potentially preventable infectious diseases.

There are several reasons for this special risk profile. VFR travellers commonly stay in local family homes during their stay overseas (36). A Greek study of VFR and other travellers seeking pre-travel health advice from travel clinics found that most VFR travellers stayed at local people’s homes (87% of VFR travellers compared with 15.5% of other travellers) (23). Furthermore, VFR travellers often undertake a longer duration of travel, which increases the length of time that they are exposed to infections present in their environment (19, 23, 24, 36, 47). This prolonged contact with the local population increases the risk of acquiring diseases where prolonged close contact increases the likelihood of transmission, for example, tuberculosis (36). Where VFR travellers visit or stay in rural places or in close proximity with animals, they can also be at increased risk of zoonoses (e.g. leishmaniasis or leptospirosis) (36). VFR travellers often consume food that tourist travellers do not, due to living with and spending time with family and friends, and social pressure to eat the food provided by their hosts. This increases the risk of food poisoning, food-borne hepatitis and toxin ingestion (19, 36). VFR travellers may elect to undertake medical and dental procedures during travel, due to these procedures often being more affordable than in Western countries (19). In settings where infection control practices are substandard, some medical procedures (e.g. dental procedures) put them at risk of blood-borne infections (36). Also importantly, incomplete childhood immunisation coverage is more common in immigrants, due to lower vaccine coverage rates in developing countries for first generation immigrants who grew up there (48, 49), and also due to barriers to healthcare access in their new homelands (48, 50). This means that VFR travellers are at particular risk for some vaccine-preventable illnesses, including measles, tuberculosis, hepatitis A and B and enteric fever (14, 19). Moreover, in the case of malaria, VFR travellers often do not

5 Chapter 1: Literature review

undertake adequate prophylaxis, due to the misconception that one possesses life-long immunity (24, 51) and are less likely to follow the complete course of malaria prophlaxis (52).

1.2.3 VFR travellers and pre-travel health advice

Studies have shown that travellers aware of travel risks in the destination country are more likely to seek professional travel health advice (25, 33). VFR travellers often underestimate the risk of acquiring diseases during their travel (36), and multiple studies have shown that, as expected from this, VFR travellers have lower rates of seeking professional travel health advice than non-VFR travellers (16, 18, 22-24). Surveys of departing passengers at airports in both Europe (22) and the USA (33) found that VFR travellers were less likely to have obtained pre-travel health advice compared with other travellers, although in the aforementioned US study the trend was not statistically significant (OR 2.04; 95% CI 0.94–4.42). The European study involved 5067 passengers (25.4% of whom were VFR travellers) at nine airports, and the US study involved 1254 passengers (including 98 VFRs) all surveyed at Boston Logan International Airport. Taken together, these studies represent a sizeable sample, and as they included random passengers departing multiple international airports, they provide a representative cross-sectional sample. An airport survey of 1302 US residents travelling to India, of which 76% were VFR travellers, found that only 29.8% of VFR travellers had sought pre-travel health advice, compared with 48.4% of non-VFR travellers (p<0.001) (52). A Canadian airport survey of 307 travellers to India (87% of whom were “visiting relatives”), conducted at Toronto Pearson International Airport, found that only 54% of respondents sought pre-travel advice (including professional and non-professional) (24). There was no comparison between VFR and non-VFR travellers in this study, however, this is further evidence of VFR travellers having sub-optimal rates of seeking pre-travel health advice. Furthermore, an airport survey of 729 passengers departing Sydney international airport and 114 passengers departing Bangkok international airport found that migrant Australian travellers, who were more likely to undertake VFR travel, were half as likely as Australian-born travellers to have sought professional pre-travel health advice (53). The aforementioned airport studies are summarised in Table 1.1.

Studies conducted in other contexts, also provide further evidence of VFR travellers having lower rates of seeking pre-travel health advice. The previously mentioned study at the University Hospital of Zurich found that only 20% of returning VFR travellers with travel-associated illnesses had sought pre-travel health advice, compared with 67% of other travellers (p=0.0001) (18). Furthermore, the previously mentioned analysis of the entire GeoSentinel database from November

6 Chapter 1: Literature review

1997 to December 2004 found that only 16% of the 1813 ‘immigrant VFRs’ had sought pre-travel health advice, compared with 62% of the 10,021 tourists travellers (16). Among ‘traveller VFRs’ (VFR travellers who were born in high-income countries, e.g. second generation immigrants), 47% of 670 had sought pre-travel advice. It is important to point out that both aforementioned studies were conducted on unwell returned travellers, rather than samples representative of travellers in general, as with the airport studies. However, they contribute to the extensive evidence of VFR travellers commonly not seeking pre-travel health advice. Furthermore, a study conducted in Greek government-operated travel clinics, which provide almost all travel health services in Greece, estimated that only 1 out of 700 VFR travellers to Africa and Asia sought pre-travel health advice (23).

Various studies have shed light on the reasons why VFR travellers do not seek pre-travel health advice, and multiple studies have reported similar results. The most common reasons given by VFR travellers were that they did not think it was necessary to seek advice (25, 52), they were not concerned enough by the possible health problems of their travel (24, 25, 33), they believed they already knew enough to protect themselves (24), or in some cases, they had never even considered seeking advice and/or were unaware of the need to do so (24, 33, 52). Another commonly stated reason was time constraints (24, 33, 52, 54). This is especially relevant to VFR travellers, who are more likely to seek pre-travel consultations closer to departure, on average, than other travellers (47). VFR travel may also occur at the last minute in cases of family emergencies (19), which has implications for pre-travel vaccination, even in patients who manage to obtain a pre-travel consultation. There may be inadequate time to administer the recommended vaccine schedule for vaccines requiring multiple doses, and the ability to give multiple vaccinations at the same time is limited by the increased likelihood of experiencing side effects with the number of vaccinations given simultaneously (31). Financial considerations were not commonly stated as a reason for not seeking pre-travel advice (25, 33, 52), but as quantitative studies typically only allow respondents’ answers to be classified into several limited options, they may have underestimated cost factors. A qualitative study of US Nigerian VFR travellers reported cost to be an important barrier to seeking pre-travel health care, regarding both pre-travel consultations and purchasing prophylactic medications including for malaria (54).

Sources of pre-travel health advice

Professional pre-travel health advice can be provided by a general practitioner (GP), or by travel medicine specialists. The previously mentioned Boston airport survey found that only 1 out of the

7 Chapter 1: Literature review

35 VFR travellers who sought pre-travel advice visited a travel medicine specialist, and VFR travellers were significantly more likely than non-VFR travellers to have sought their advice from GPs (33). This is further supported by the previously mentioned Canadian airport study where, among the 167 participants who had sought pre-travel advice, 70% had done so from their family physician, while only 11% had visited a travel clinic (24). Although this study did not exclude non- VFR travellers, 87% of participants were VFR travellers. Whilst Australian GPs are regularly consulted for pre-travel health advice (55, 56), a 2000 survey of 208 Australian GPs found that only 47.1% reported having had any formal training in travel medicine (57). A recent survey of Sydney GPs also found that the majority did not recognise VFR travellers as a particularly high-risk group compared to holiday travellers (58). Studies from other countries have also found knowledge deficits regarding travel medicine in GPs. A survey of 300 Swiss and German GPs, published in 1997, found that the majority could not correctly state the recommendations for vaccinations and malaria prophylaxis regarding travel to Kenya and Thailand, according to the national guidelines of their country of practice (59). A study of Canadian South-Asian VFR travellers also found that in 76% of cases their GPs prescribed inappropriate malaria chemoprophylaxis regimens (24). Furthermore, a survey of 76 GPs in Qatar published in 2011 also showed that many GPs could not correctly answer a significant number of questions regarding travel health, and relied mainly on the internet and books for travel health information (78.9% of respondents relied on the internet as their main source of travel health knowledge) (60). As VFR travellers have been shown to prefer seeking pre-travel advice from GPs, and it would also be impractical for all of them to use professional travel health clinics, it has been recommended that GPs serving VFR communities should be trained about issues surrounding travel health, including appropriate immunisations for common and low- risk travel destinations of their patients, and about the need to refer high-risk cases to travel health professionals (21).

A telephone survey of 309 Australians who had travelled to East or Southeast Asia in the previous 3 years found that VFR travellers (16% of the sample) were more likely than other travellers to seek travel health advice from family and friends, and travel agents were also common sources of advice (61). This provides evidence that VFR travellers also commonly seek non-professional advice in lieu of professional advice.

1.2.4 Vaccination and other prophylactic measures

Besides having a lower rate of seeking pre-travel health advice, VFR travellers also have low rates of taking appropriate prophylactic measures, including vaccination for travel and malaria

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chemoprophylaxis. This has been shown in a number of studies. The previously mentioned airport survey of US residents travelling to India found that VFR travellers were significantly less likely than other travellers to be protected against hepatitis A (from a past history of infection or having received vaccination or immunoglobulin), to have received an up-to-date typhoid vaccine, or to be taking appropriate malaria chemoprophylaxis (52). The previously mentioned Canadian airport survey found that only 31% of respondents intended to use malaria chemoprophylaxis (24). A post- travel survey of 106 VFR travellers of African ethnicity living in Paris found that only 29% of respondents took adequate chemoprophylaxis with complete adherence, although 75% had taken some form of chemoprophylaxis (62). In this study, 64 participants were recruited at travel health clinics, and 42 were recruited at travel agencies and had no intention to visit a travel health clinic. Among the latter group, only 12% practised adequate chemoprophylaxis, and, even among those who had visited a travel health clinic, only 41% practised adequate chemoprophylaxis. A random telephone survey of 263 Australians who had travelled overseas in the past 2 years found that those staying with friends or relatives during their trip (i.e. likely to be VFR travellers) were less likely to be vaccinated against hepatitis A compared with those staying in hotels or budget accommodation (63). Furthermore, the previously mentioned European airport survey also found that VFR travellers were less likely to be protected against hepatitis A than tourists or business travellers (22). A study of 3707 VFR travellers and 17,507 non-VFR travellers presenting for pre-travel consultation at various sites in the USA also found that being a VFR traveller was an independent predictor of declining to receive a recommended vaccine (47). All these results illustrate the fact that VFR travellers commonly undertake inadequate medical prophylaxis against potential infectious risks.

Lack of awareness, knowledge deficits and misconceptions are likely to be important causes of the common perception among VFR travellers that seeking pre-travel advice is not required or that accepting recommendations regarding vaccination and other prophylaxis is not essential. The Canadian airport survey found that among respondents not intending to use malaria chemoprophylaxis, a majority either were unaware that precautions were needed, believed that they were not at risk, or thought they were immune (24). Four participants also stated that they were ‘vaccinated’ against malaria, indicative of a poor understanding of their travel health preparations. A pre-travel survey that was part of the previously mentioned French African VFR study showed that less than half of the 191 participants considered malaria a health concern, and many were not knowledgeable about common malaria prevention measures, despite travelling to malaria endemic regions (62). Furthermore, the aforementioned qualitative study of US Nigerian VFR travellers found that participants’ general knowledge was poor and misconceptions were common regarding

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the three diseases studied (malaria, typhoid and hepatitis A) (54). Misconceptions reported included a belief that taking a single curative dose of antimalarials can provide months of protection, that hepatitis A can be spread by mosquitoes, and that immunity can be improved with high frequency of travel.

Table 1.1: Summary of selected airport surveys of departing travellers comparing pre-travel health seeking practices of VFR and other travellers

Van Herck et al. (2004) – Knowledge, attitudes and practices in travel-related infectious diseases: the European airport survey

• European airport survey, included nine international airports in Europe • 5067 participants, 25.4% VFRs • 31.4% of VFRs sought pre-travel health advice, compared with 60.9% of tourists • VFRs were also more likely to be unprotected against hepatitis A (51.6%) compared with tourists (42.1%) or business travellers (42.3%)

LaRocque et al. (2010) – Pre-travel health advice-seeking behavior among US international travelers departing from Boston Logan International Airport

• 1254 participants, all recruited at Boston Logan International Airport, including 98 VFRs • VFRs were less likely to have sought pre-travel health advice, but this finding was not statistically significant (OR 2.04; 95% CI 0.94–4.42) • Main reasons for not seeking advice among VFR travellers included “not concerned about health problems related to this trip”, “didn’t think of it” and “not enough time” • VFR travellers were significantly more likely than non-VFR travellers to have sought advice from GPs; only 1 in 35 who sought advice visited a travel health specialist

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dos Santos et al. (1999) – Survey of use of malaria prevention measures by Canadians visiting India

• Canadian airport survey, specifically re ethnic Canadian South-Asian residents travelling to India, and focusing on malaria • 307 participants, all recruited at Toronto Pearson International Airport, 87% “visiting relatives” • 167 participants (54%) sought pre-travel health advice, 70% of those from GPs and 11% from travel clinics • The most common reasons participants did not seek advice included a belief that they knew about malaria enough to protect themselves, being unaware of the need for precautions against malaria, being unaware that they were at risk, and insufficient time • 31% intended to use chemoprophylaxis. Of those who did not, the majority were unaware of the need to.

Baggett et al. (2009) – Pretravel health preparation among US residents traveling to India to VFRs: importance of ethnicity in defining VFRs

• US airport survey, specifically re travellers to India • 1302 participants, recruited at three airports, 76% VFRs • 29.8% of VFR travellers sought pre-travel health advice, compared with 48.4% of non-VFR travellers (p<0.001) • Main reasons for not seeking advice among VFR travellers included “did not think needed/never considered” and “time limitations” • VFR travellers were significantly less likely than other travellers to be protected against hepatitis A, typhoid and malaria

Heywood et al. (2012) – A cross-sectional study of pre-travel health-seeking practices among travelers departing Sydney and Bangkok airports

• Airport survey of 729 passengers departing Sydney international airport and 114 passengers departing Bangkok international airport • No significant association between VFR travel and seeking professional pre-travel health advice • However, migrant Australian travellers, who were more likely to undertake VFR travel, were half as likely as Australian-born travellers to have sought professional pre-travel health advice

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Table 1.2: Summary of other selected studies describing VFR travellers’ pre-travel health seeking behaviours

LaRocque et al. (2013) – Pre-travel health care of immigrants returning home to visit friends and relatives

• Evaluation of patients presenting for pre-travel consultations at various Global TravEpiNet centres, sponsored by the CDC • 3707 VFR travellers and 17,507 non-VFR travellers • VFR status was an independent predictor of declining to accept a recommended vaccine

Pistone et al. (2007) – Malaria risk perception, knowledge and prophylaxis practices among travellers of African ethnicity living in Paris and visiting their country of origin in sub- Saharan Africa

• 191 participants in pre-travel survey, including 122 from travel clinics and 69 from travel agencies • Less than half considered themselves at risk of malaria, and knowledge deficiencies regarding prevention were common • 106 participants in post-travel survey, including 64 from travel clinics and 42 from travel agencies • 75% of participants took some form of chemoprophylaxis, but only 29% of participants took adequate chemoprophylaxis • 41% of the travel clinic cohort took adequate chemoprophylaxis, compared with 12% of the travel agency cohort

Fenner et al. (2007) – Imported infectious disease and purpose of travel, Switzerland

• Analysis of patients presenting for treatment for travel-related illness at University Hospital of Zurich clinic • 121 VFR travellers and 217 other travellers • 20% of VFR travellers sought pre-travel health advice, compared with 67% of others (p=0.0001) • VFR travellers were more likely than other travellers to be diagnosed with malaria and viral hepatitis, but less likely to present with acute diarrhoea

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Leder et al. (2006) – Illness in travelers visiting friends and relatives: a review of the GeoSentinel Surveillance Network

• Analysis of GeoSentinel (a global network collecting data from travel health and tropical medicine clinics) database from November 1997 to December 2004 • 1813 immigrant VFRs, 670 traveller VFRs, and 10,021 tourist travellers • 16% of VFR immigrants sought pre-travel health advice, compared with 47% of VFR travellers and 62% of tourist travellers • Immigrant VFRs were more likely than tourist travellers to be diagnosed with systemic febrile illnesses (including malaria), non-diarrhoeal intestinal parasitic infections, respiratory syndromes, tuberculosis and sexually transmitted diseases, but less likely to present with acute diarrhoea

Leonard and VanLandingham (2001) – Adherence to travel health guidelines: the experience of Nigerian immigrants in Houston, Texas

• Qualitative study including focus groups and interviews with VFR travellers and physicians and pharmacists serving the Nigerian population • Low risk perception and knowledge deficits and misconceptions were common for malaria, typhoid and hepatitis A • Low rates of typhoid and hepatitis A vaccination and malaria chemoprophylaxis • Financial, time and other barriers, e.g. vaccine shortages, were important barriers to both pre- travel consultation and vaccination and chemoprophylaxis • More likely to seek pre-travel advice if travelling with children

1.2.5 Special subgroups of VFR travellers

Children as VFR travellers

It is common for VFR travellers who have children to take them on trips to visit friends and relatives (47). Childhood VFR travellers account for a higher proportion of total international travel in their age group, compared to adult VFR travellers in relation to total international travel for all adults (23, 64). Parents who may not seek pre-travel health advice for themselves may nevertheless specifically seek advice regarding their children (54, 65).

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Many of the issues relating to adult VFR travellers also apply to childhood VFR travellers, including an increased risk of acquiring certain infectious diseases while travelling, and systematic barriers to accessing health care. However, there are also specific issues for childhood VFR travellers. For example, while adult migrants who grew up in developing countries may be immune to hepatitis A, their children born in developed countries may not be and would require hepatitis A vaccination. Some parents may not be aware of this (64).

Like adult VFR travellers, childhood VFR travellers also risk the introduction of infectious diseases on their return, and this can have particular important implications for health outcomes for the larger paediatric population. For example, in the USA there are concerns that childhood VFR travellers to Mexico, who are at risk of acquiring hepatitis A during their travel, often asymptomatically, may transmit the infection to other children after they return to the USA. This was one of the reasons there were calls for universal paediatric hepatitis A vaccination for US children (41), which has since been part of the national recommendations (66).

International students as VFR travellers

International students are a sizeable population in Australia, with 589,860 total enrolments in 2014 (67). International students from developing countries studying in developed countries, who travel back home during semester breaks to visit friends and family, constitute another important group of VFR travellers with unique issues (68). A survey of international students at UNSW Australia (University of New South Wales) found that, of 829 participants including 185 international students who had travelled internationally in the past 12 months, 52.2% of international students had travelled for VFR purposes on their last trip, compared with 30.3% of domestic students (p<0.001).

Previous studies have shown that university-aged travellers are at increased risk of travel-related illness compared to older travellers (69, 70). Such travellers also have a lot of issues in common with VFR travellers, including low risk perception (71), inadequate travel preparation (71), exposure to more health risks (72, 73), and lower compliance with preventive measures (72). Hence, in international student VFR travellers, risks due to age and VFR travel are potentially compounded. The aforementioned survey of students at UNSW Australia found that, compared with domestic students, international students were less likely to have undertaken adequate travel health preparations, including obtaining travel health insurance, bringing medication for use while travelling, and bringing a first aid kit and insect repellent, and were also less likely to take

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precautions while travelling, such as avoiding certain foods and drinking tap water (all p<0.001) (71).

Compared to other VFR travellers, returned international student VFR travellers potentially pose an additional public health threat, due to studying, and often living, in a university campus. In such a setting, a large population with varying immunisation status is in frequent close contact with each other, providing an optimal environment for the spread of infectious diseases (74-76). Multiple outbreaks of influenza with high attack rates have been previously associated with university campuses (74, 77, 78). More serious infections, including those already eliminated in Australia, may also be introduced by returned international students. For example, the diagnosis of polio in a returned Pakistani international student in Melbourne in 2007 highlighted this risk (79, 80).

1.2.6 Australian Chinese VFR travellers

Ethnic Chinese are one of the largest cultural groups in Australia. As of 30 June 2013, 1.8% of the total population in Australia was born in China, making it the third largest foreign country of birth, after the UK and New Zealand (81). This figure has increased from 1.0% in 2003 (81). China also continues to be one of the largest sources of immigration to Australia each year. In the year from July 2012 to June 2013, China was the third biggest source of migrants into Australia. There were 18,041 new settler arrivals from mainland China, accounting for 11.8% of all new settler arrivals in Australia during that year (82).

Travel to mainland China and Hong Kong accounts for a significant proportion of all overseas travel by Australian residents. Of resident Australian departures in 2010, 4.7% were to mainland China and 3.0% were to Hong Kong (83), and, of those, 28.9% were for the purpose of visiting friends and relatives (84). Therefore, VFR travel among Australian Chinese has the potential to affect health outcomes in Australia. Although there have been a limited number of published studies that have explored VFR travel health behaviour, either specifically or as part of a wider study of travellers, none have specifically studied ethnic Chinese VFR travellers.

The following sections of the literature review explore published literature on ethnic Chinese and travel health in various contexts, health beliefs of ethnic Chinese that may be relevant to travel health, and specific infection risks regarding travel to China. Together with research identifying risk characteristics of VFR travellers in general, as described above, they provide information regarding issues of potential concern in Chinese VFR travellers.

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In summary

VFR travellers have been shown to be at especially high risk of acquiring a range of infectious diseases, including systemic febrile illnesses (including malaria), viral hepatitis, some parasitic infections, respiratory syndromes, tuberculosis, sexually transmitted diseases, enteric fever and dengue fever (15-18, 43, 44, 46).

This is due to a variety of factors, including duration of travel (23, 24), accommodation circumstances, dietary habits and other activities undertaken during travel (14, 19, 36), as well as knowledge deficits and low awareness regarding a range of infectious risks (24, 54, 62), and suboptimal preventive behaviour, including lower rates of vaccination (47, 63).

VFR travellers have also been found to seek professional pre-travel health advice at a lower rate than other travellers (16, 18, 22-24, 33, 52). The most common reasons given relate to a lack of awareness of the need to or benefit of seeking such advice, while time and financial factors are also important barriers (24, 25, 33, 52, 54). Where VFR travellers do seek medical consultation, they are much more likely to consult their GP than to consult a travel health specialist (24, 33).

Although there have been a limited number of published studies that have explored VFR travel health behaviour, either specifically or as part of a wider study of travellers, none have specifically studied ethnic Chinese VFR travellers. This study of Australian Chinese VFR travellers will aim to fill this gap.

1.3 Travel health issues in ethnic Chinese travellers

Although data specific to ethnic Chinese VFR travellers living in Western countries is lacking, there have been studies in other ethnic Chinese travellers which have explored issues that are likely to be relevant to Chinese VFR travellers. As ethnic Chinese around the world share a similar culture, attitudes and cultural issues identified in studies regarding ethnic Chinese travellers in other contexts are likely to be of some relevance to Chinese VFR travellers. This section will explore such studies and their findings.

1.3.1 Use of travel health services

The specialty of travel medicine was first developed in Western countries, and many Asian travellers remain unfamiliar with it (85). There are also fewer travel health clinics per capita in Asia than in the West (85). Several large-scale studies have found that the proportion of Asian travellers

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seeking pre-travel health information is lower than that among Western travellers (53, 86, 87). A traveller survey study conducted at five airports in Asia and Australia, involving 2101 participants (82% Asian, 17% Western), found that travellers of Asian origin were significantly less likely than Western travellers to have sought pre-travel health advice (86). A cross-sectional survey conducted in a Singaporean travel clinic involving 495 patients seeking pre-travel consultation (including 357 ethnic Chinese) also identified that Caucasians and Eurasians were more likely than ethnic Chinese (as well as Malays and Indians) to have previously sought professional pre-travel health advice. (comparing Caucasians and Eurasians to Chinese, OR=3.8 by univariate analysis, 95% CI 2.1-7.0; OR=6.6 by multivariate analysis, 95% CI 2.3-19.4) (87). Another airport study conducted at Sydney and Bangkok airports involving 843 participants also found that travellers from Asian countries were significantly less likely to have visited a doctor for travel advice before their trip, and were significantly more likely to have not sought any travel health advice at all, compared to travellers from Western countries (53). The Singaporean study also found that travel outside Asia, and particularly to Africa and South America, was associated with a higher likelihood of travellers seeking health advice (87), while the Sydney and Bangkok study found that travel to Southeast Asia was significantly associated with seeking pre-travel health advice among travellers from Western countries other than Australia (53). All this suggests that the travel destination may be important in determining whether a person seeks travel advice, and Asians may be less likely to seek travel health advice for travel within the Asian continent.

An airport survey of 2495 departing passengers across five international airports in mainland China found that 78.2% of respondents had sought some form of travel health information, but only 40% had sought a pre-travel medical consultation (88). The most common sources of pre-travel health information were the internet, travel agencies, and family and friends. The study also found that, among travellers to malaria-prone destinations, less than a quarter were carrying a mosquito net, insecticide, mosquito repellent or malaria chemoprophylaxis. Only 42.5% of travellers to malaria- prone destinations had received information about malaria, and most either did not know the level of malaria risk in their destination or underestimated the risk. Substantially more respondents knew that mosquito nets and mosquito repellents were effective in malaria prevention than the proportion that actually carried these items. The most common reason given by travellers for not carrying antimalarials was that they did not know of the need to do so, suggesting that risk awareness regarding their destination was a major barrier to adequate pre-travel preparation. Furthermore, none of the respondents visiting malaria-prone destinations were correctly taking chemoprophylaxis before departure. An airport survey conducted at Hong Kong International Airport among 770

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travellers, 76.9% of whom were ethnic Chinese, found that the internet was the most common source of pre-travel health information. Only 14.9% sought medical advice from a health professional, and, of those, only 18.8% consulted a travel health specialist (89). Only 9.1% had received appropriate vaccinations for their travel. Most participants thought that pre-travel health preparations were effective for the prevention of adverse health outcomes at the travel destination. However, most participants also believed that adequate pre-travel preparation did not have to include a medical consultation, and 66.9% stated they believed that their preparations were adequate. The study also found that Chinese ethnicity was negatively associated with medical consultation prior to travel, compared with Caucasian ethnicity (on univariate analysis only). Participants travelling to malaria-prone destinations (n=403, 75.6% ethnic Chinese) also answered extra questions regarding malaria prevention (90). It was found that only 27.1% had undertaken adequate pre-travel prevention measures, and Caucasians were significantly more likely than Chinese travellers to use bed nets and chemoprophylaxis. Participants generally had a low risk perception regarding malaria, and the level of pre-travel preparation was significantly associated with participants’ perceived likelihood of developing illness while travelling. Over a quarter (26.7%) of respondents felt that pre-travel preparations were time-consuming, and 25.6% were concerned about side effects of vaccinations and prophylactic medications. A survey of 501 travellers travelling by sea between Xiamen (in mainland China) and Kinmen, Taiwan, conducted in 2006–2007, found that 94% of respondents were aware that increased travel between the two destinations would increase the risk of transmission of infectious diseases, 72.3% would accept vaccination for influenza, and 70.9% would visit places where there is live poultry (91). A majority (60.5%) of respondents would actively seek travel health information, and television, newspapers and the internet were the major sources of information. Taken together, these studies suggest that Chinese travellers commonly seek pre-travel health information, but do not commonly seek a medical consultation as part of this process. They have generally low awareness of infectious risks associated with their travel, and often undertake inadequate precautions.

There have also been some studies conducted in other contexts (i.e. not conducted with participants during their travel) regarding the use of travel health services among ethnic Chinese populations. The majority of such studies that have been published in English were conducted in Hong Kong. In Hong Kong, the utilisation of travel-related health services had previously been found to be low. In a 1998 cross-sectional telephone survey of 369 Hong Kong residents with a history of travel in the past 12 months, only 8% received health advice before travel, despite 59% taking health precautions while travelling (70). These health precautions commonly included measures to prevent food

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poisoning (e.g. boiling water, washing fruit and vegetables, and avoiding certain foods) and measures to prevent accidents (e.g. travelling only in authorised vehicles), and less commonly included measures to prevent malaria and other vector-borne diseases (e.g. the use of mosquito nets and repellents). Forty per cent of respondents perceived themselves as being at risk of future travel- related health problems, and 68% of respondents were willing to pay for travel-related health services in the future (70). Another 1996 questionnaire survey of 1197 university students, conducted among undergraduate students at the University of Hong Kong, showed that 75% of respondents took no pre-travel health advice, 41% of those who received advice did so from non- professional sources (i.e. sources other than GPs, travel clinics or university health services), and 48% took no travel precautions (69). Taken together, these studies suggest that Hong Kong residents are potentially willing to pay for travel health services, but the majority do not currently do so. They also suggest that although a substantial number of Hong Kong residents undertake health precautions when travelling, for most this apparently does not include obtaining professional health advice before travelling.

In a survey of 15 physicians in Hong Kong, including five tropical medicine specialists and 10 GPs, the majority of whom had substantial experience in providing travel health advice to patients, 70% agreed that lack of awareness of the existence of travel health services was preventing their use by more Hong Kong residents (92). Other reasons suggested for the low use of such services included concerns about fees, consistent with the observation that travel health advice was often sought during visits for other health conditions. Fees may be less of a concern for GP visits in Australia given the widespread availability of free (‘bulk-billed’) GP consultations under the Medicare system, but it may be a concern in regard to travel health specialty clinics in which only very limited rebates are available. However, GPs may not always be able to provide the most effective travel health advice, as previously mentioned in section 1.2.3.

1.3.2 Seeking health care

Patients who experience the onset of health problems while travelling may require to seek medical attention overseas, or, where possible, delay seeking treatment until they return to the country of usual residence. This option would be available for moderate, or initially moderate, illnesses, such as upper respiratory infections. However, it would also cause the transmission of diseases, including potentially pandemics, between countries. There has been no comprehensive study on how frequently each option is chosen, and under what circumstances. However, a random telephone survey of 406 Hong Kong Chinese residents regarding hypothetical illnesses while travelling to

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mainland China showed that for mild influenza, 70.9% of respondents would defer seeking medical treatment, and even for more severe conditions, 37.3–55.6% would do so (93). Reasons for deferring medical treatment included perceived inferiority of medical services in mainland China, not knowing where to seek medical treatment in mainland China, and the lack of support of family and friends (93). The reasons given would not be limited to mainland China, which suggests that the findings may also apply to a wider range of travel destinations.

In summary

Asian travellers have been shown to seek professional pre-travel advice less commonly than Western travellers (53, 86, 87).

Airport studies in mainland China and Hong Kong have found that, although seeking some form of pre-travel health advice was common, most participants did not consult with a health professional pre-travel. Knowledge and risk awareness deficits were also common, and travel health preparations were often inadequate (88-90).

Studies conducted in Hong Kong had also found that rates of obtaining professional travel health advice were low, even though a substantial proportion of travellers took some form of precautions while travelling, and many travellers stated a potential willingness to pay out-of-pocket expenses to prevent travel health problems (69, 70, 94).

1.4 Infectious risks in China relevant to VFR travellers

Part of this section was published as a review: Ma T, Heywood A, MacIntyre CR. Chinese travellers visiting friends and relatives: a review of infectious risks. Travel Medicine and Infectious Disease 2015;13(4):285-94. This article is provided in Appendix 3.

China is a developing country with many infectious disease risks that are uncommon in developed countries like Australia (95). China is a vast country with varying infectious diseases risks associated with different regions (95). Some VFR travellers may travel to rural areas of China or regions where tourists do not usually travel to (36), and may require a pre-travel assessment (including vaccinations) designed specifically with their itinerary and risk profile in mind (26, 29).

1.4.1 Influenza and other respiratory tract infections

There is generally a higher risk of acquiring upper respiratory tract infections while in China than in Australia. A pre- and post-travel serological survey of 387 travel health clinic patients in Australia

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concluded that influenza remains the most common vaccine-preventable illness for travellers to Asia, and travellers were 3.4 times more likely to acquire an acute respiratory infection while in China than in Australia (96). Travellers to China were also more likely to have acquired an acute respiratory infection compared with travellers to other Asian countries, including India, Thailand, Singapore, Malaysia, Indonesia and Vietnam amongst others.

Outbreaks and pandemics

Returned VFR travellers are a potential source of importation of diseases with pandemic potential. For example, SARS was initially brought into Canada by a VFR traveller (97). One reason that Australian Chinese VFR travellers deserve particular attention is that China has been the source of a number of international pandemics. Southern China has historically been a place where many new respiratory infectious diseases have emerged and infected humans. In recent times, these have included SARS and the highly pathogenic avian influenza A (H5N1). It has been hypothesised that southern China is an epicentre for the emergence of new, pandemic causing influenza viruses (11, 98, 99). There are various reasons for this, including farming practices and food preferences in Chinese culture (11).

The topic of outbreaks and pandemics in relation to Chinese VFR travel health is further explored in Chapter 4, including a separate in-depth literature review. The global spread of the recent SARS pandemic, the potential for future similar pandemics, and possible agents for future pandemics already circulating in China will be reviewed in Chapter 4.

Chinese wet markets and infectious disease exposure

Chinese wet markets have received particular attention regarding their potential role in the emergence of infectious diseases in humans (100). During the outbreak of human H5N1 influenza in Hong Kong in 1997, there were no new human cases after all poultry was slaughtered, suggesting that local live poultry markets were a source of the infection (100). The SARS pandemic in 2002– 2003 is another good example of the role of Chinese wet markets in the emergence of pandemics. During the epidemic, the SARS coronavirus was isolated from caged animals in wet markets in Guangdong province in southern China (101). Chinese wet markets are thought to provide a conducive environment for the emergence of new pathogens because animals of different species are kept in close proximity, promoting genetic reassortment and recombination between pathogens originating from different species (101). The newly emerged pathogens can potentially be transmitted to large human population frequenting these markets (101). Chinese wet markets are

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also important for reasons other than the transmission of epidemics. Many other infectious diseases, including bacterial and parasitic infections, can be transmitted either when shopping in the market, or when preparing or consuming food bought from the market (101). These markets are regularly visited by many people living in various parts of China for their daily shopping and are favoured for their fresh produce. As VFR travellers often live with and spend substantial time with the local population (19, 23, 36), it is likely that a significant number of VFR travellers would also visit these markets during their travel.

1.4.2 Viral hepatitis

Hepatitis A is transmitted via the faecal–oral route. It is usually self-limiting and may even be asymptomatic, especially in children, but there is a 0.015–0.5% risk of death from liver failure (102). Outbreaks of acute hepatitis A are a major public health problem in China. Several major outbreaks occur each year nationwide in addition to many more minor outbreaks, and over 60,000 cases are reported annually (102, 103). In recent years, there has been a marked decrease in the incidence rate of hepatitis A infections in China, which is likely due to improved living conditions and vaccination against hepatitis A (103). Hepatitis A vaccines were first available in China in 1992, but since 2008 hepatitis A is provided to children at 12 months of age as part of the funded national immunisation program (104). However, immunisation rates were reported to be high prior to the universal immunisation program, at least in some areas (104). There are also epidemics of hepatitis E, another acute viral hepatitis transmitted via the faecal–oral route (102). The estimated seroprevalence of hepatitis E in China is in fact as high as 23% (105). All this highlights the importance of food safety whilst travelling in China. This can be particularly important for Chinese VFR travellers, who often consume food that tourist travellers do not, as mentioned previously (19, 36).

Hepatitis B and C, which are transmitted via exposure to infected blood or bodily fluids, including via blood-prone medical procedures and via sexual transmission (106, 107), are also major public health issues in China (102). In China, 9.8% of the population are carriers of the hepatitis B virus (102). Furthermore, 3.2% of the population are carriers of the hepatitis C virus (102). This high prevalence has particular implications for travellers who may seek healthcare in China, either due to medical emergencies or planned medical tourism, including dentistry. There is a higher risk of exposure to unsafe blood and blood products in regional areas, which may pose a risk of hepatitis B and C as well as other blood-borne viruses (108).

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1.4.3 Tuberculosis

China is considered a moderate incidence country for tuberculosis (109), and outbreaks occur regularly (110). In 2010, the population prevalence of tuberculosis in China was 108 per 100,000 (111), and in that year there were about 1 million new cases of tuberculosis diagnosed (110). The number of cases of tuberculosis admitted to hospitals appears to have increased recently, but it is unknown whether this is an actual increase in the number of infections or a result of a higher rate of diagnosis (112). In Hong Kong, the incidence of tuberculosis is steadily declining. In 2009, there were 5193 new cases (74 cases per 100,000 population) (113).

There is also a major problem with multidrug-resistant tuberculosis (MDR-TB) in mainland China. A national survey conducted in 2009 found that 1 in 10 tuberculosis patients had MDR-TB, and 8% of those had extensively drug-resistant tuberculosis (XDR-TB). Also worryingly, most cases of MDR-TB and XDR-TB resulted from primary transmission (114). Therefore, it is not unlikely for previously uninfected travellers to acquire MDR-TB or XDR-TB whilst in China, with potential spread to further contacts when back in Australia. This is especially important for Chinese VFR travellers, as they are at an increased risk of tuberculosis transmission due to prolonged close contact with the local population (36). In Hong Kong, only 1% of culture-confirmed new tuberculosis cases are MDR-TB (113).

1.4.4 Dengue fever

Dengue fever is a viral disease transmitted by Aedes mosquitoes. It can cause a spectrum of symptoms, from a simple febrile illness to dengue haemorrhagic fever and dengue shock syndrome. It can occasionally result in death. There are four serotypes of dengue virus, designated DENV-1 to DENV-4. All have caused epidemics in China (115).

The incidence of dengue fever is increasing worldwide. In China, dengue outbreaks were first reported in 1978. Initially they were limited to the far southern provinces of Guangdong, Hainan and Guangxi, but now they have spread to Fujian, Zhejiang and Yunnan provinces. In the past three decades, there have been more than 650,000 cases nationwide, with at least 610 deaths (116). Dengue outbreaks now occur frequently in Southern China, often as a result of the virus being introduced by travellers returning from Southeast Asia where dengue is endemic (115). Dengue fever has also occurred locally in Hong Kong, where the continued presence of the required vector means that local transmission can happen at any time (117). There was even a small outbreak in 2002 (117). As there is currently no vaccine, prevention is by mosquito avoidance and vector

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management (115). It is therefore important that travellers to southern China undertake adequate mosquito avoidance measures.

1.4.5 Chikungunya

Chikungunya is a viral disease transmitted by Aedes mosquitoes, the same vector as dengue. It causes an acute febrile illness, associated with a skin rash and joint pain, which may lead to chronic arthropathy (118). Haemorrhagic disease and neurologic and myocardial involvement may also occur. Since 2006, chikungunya has been re-emerging in various parts of the world (119). Strains of the virus have been transmitted from Southeast Asia to China, and there was an outbreak in Guangdong province in 2010 (120). Although there have been no outbreaks in Hong Kong yet, the required vector is present (117). There is currently no vaccine, and treatment is symptomatic only (118). This further adds to the importance of mosquito avoidance whilst travelling in southern China.

1.4.6 Japanese encephalitis

Japanese encephalitis, a mosquito-borne virus, can cause symptoms varying from a non-specific febrile illness to severe encephalitis (121). Japanese encephalitis is found in most of China, but is most prevalent in southwestern and central China, where rice fields and pig rearing is common (122). Nationally, 5000–10,000 cases are reported each year, with several hundred deaths. Most cases (85%) occur in children under 15 years of age, but the disease is not uncommon in adults (121). Living near rice fields and pig rearing are major risk factors for Japanese encephalitis as the primary vector, Culex tritaeniorhynchus, is often found in irrigated rice fields, and pigs can be infected and have severe and prolonged viremia.

In Hong Kong, there were seven reported local cases of Japanese encephalitis between 1999 and 2008 (although reporting was voluntary before 2004). However, as most patients with Japanese encephalitis are asymptomatic, a population serosurvey is a better indication of infection rates. One such survey in 2004 found that 2.4% of the sample were seropositive (117).

1.4.7 Hand, foot and mouth disease

Hand, foot and mouth disease is common in China and outbreaks occur from time to time (108). It mainly affects children, and is caused by enteroviruses, most commonly enterovirus 71 (EV71) and the coxsackieviruses, especially coxsackievirus A16 (CoxA16). Although much attention has been paid to EV71 and CoxA16, other enteroviruses also cause a sizeable proportion of cases. Some of

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these other viruses are associated with higher risks of complications, and in some cases there can be co-infection with two or more viruses (123). For example, Coxsackievirus B3-associated aseptic meningitis in children under 5 years of age has also been reported to be an emerging infection in Hong Kong (124). Symptoms of hand, foot and mouth disease include fever, lesions on the palms and soles, knees and hips, painful herpes‐like lesions on the oral mucosa, coughing, headache, appetite loss, nausea and vomiting. In some cases, complications such as meningitis, encephalitis, pneumonia, pulmonary oedema and haemorrhage, acute paralysis, myocarditis and, rarely, death may occur (125). In China, there have been outbreaks in various regions in the past 30 years, including in Dandong, Wuhan, Hong Kong and Taiwan (125). Large-scale nationwide outbreaks have also occurred in recent years. In 2007, a total of 83,344 cases with 17 deaths were reported nationwide, involving large cities such as Beijing and Shanghai as well as more provincial areas (125). Of particular concern, laboratory studies into cases of hand, foot and mouth disease in China between May 2008 and April 2009 found that EV71 was the most common cause, and that EV71 cases tended to be severe and associated with mortality. This reflects the fact that EV71 infections often lead to pulmonary haemorrhage, deregulation of the autonomic nervous system and circulation failure (126).

Enteroviruses are transmitted person-to-person from faeces or oropharyngeal secretions to the mouth, eyes or nose. Handwashing has been shown to be effective in reducing the risk of acquiring hand, foot and mouth disease (127).

1.4.8 Streptococcus suis

Streptococcus suis is a zoonosis that can infect people in close contact with infected pigs or pork- derived products (128). Travellers who visit wet markets and come into contact with pigs and/or raw pork sold at the markets are therefore at particular risk for this infection. Streptococcus suis can cause systemic infection and sepsis, meningitis, streptococcal toxic-shock-like syndrome and death (128). It usually causes sporadic human infections only (128), but there were outbreaks of Streptococcus suis in both 1998 and 2005 in China (129). In the 2005 outbreak, there were 215 cases with 39 deaths (128). Streptococcus suis has also emerged as the third most common cause of community-acquired bacterial meningitis in Hong Kong (130).

1.4.9 Plague

Plague has long affected China. Yunnan province is considered the place where modern plague originated (131). Plague has caused occasional outbreaks in China in recent times. An outbreak

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occurred in 2009 in a remote part of China (132). It has been found that marmot hunting is associated with a high seroprevalence of plague (39.7%); the marmot is a host for Yersinia pestis (133).

1.4.10 Parasitic infections

Malaria is considered endemic in the rural parts of Yunnan, Guangxi, Tibet (Motuo County), Anhui and Hubei provinces, but is not present in urban areas of China (134). A 2012 study in five provinces affected by malaria in central China found that the incidence rate for each province was 0.05 per 100,000 or less (135). The malaria species found in China is primarily P. vivax, with P. falciparum common in select locations (134) with evidence of resistance to chloroquine and mefloquine (134). There are no known reports of malaria in VFR travellers returning from China, and GeoSentinel Surveillance data between 1998 to November 2007 report no cases of malaria amongst travellers to China (136).

Chlonorchis sinensis is a liver fluke that is widely distributed in East Asia, including most of China. In China, it is most prevalent in northeast and south-central China, including Guangdong, Jilin, Guangxi, Anhui and Heilongjiang provinces (137). It is endemic in some areas. Infection is often asymptomatic. If symptoms are present, they may include fever, malaise, jaundice, loss of appetite, epigastric pain and loose stools. Complications may include gallstones, pyogenic cholangitis and abscess. Infection is caused by eating raw freshwater fish (138), highlighting the importance of avoiding uncooked food while travelling in China.

1.4.11 Other Infectious Risks

Enteric fever is endemic in China, but improvement in sanitation has been associated with a sharp decline in incidence (139). China is considered a medium incidence country for typhoid nowadays (140, 141). In 2004, there were 3.9 cases of enteric fever (typhoid and paratyphoid) per 100,000 people nationally, with more than half of total reported cases in Guangxi, Guizhou, Yunnan and Zhejiang provinces (139). Rabies most commonly occurs in southern China, with an increase in the incidence of rabies in China in recent years (142). HIV/AIDS is also a concern in China according to the Australian government, especially with the risk of exposure to unsafe blood and blood products in regional areas (108). Tickborne encephalitis is found in the northeastern forests of China, as well as in Xinjiang province (115).

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1.4.12 Vaccinations

The CDC recommends that, in addition to the routine vaccines recommended in developed countries, travellers to all regions of China should also be vaccinated against hepatitis A and typhoid, with the latter especially recommended for VFR travellers (109). Hepatitis B vaccination is also recommended for those who may potentially seek medical treatment in China, as well as anyone else who may be exposed to blood and bodily fluids or have sexual contact with the local population (109). Furthermore, Japanese encephalitis and rabies vaccination is recommended for some travellers (109). Malaria prophylaxis is recommended for travellers to Yunnan province (134).

According to the WHO, China’s childhood vaccination program includes vaccination for diphtheria, tetanus, pertussis, polio, hepatitis A and B, tuberculosis, mumps, measles and rubella, Japanese encephalitis, and meningitis (143). Hong Kong was administered as a British colony prior to 1997, and the colonial government had a long-running, well-established immunisation program (144). This program covers immunisation for tuberculosis, hepatitis B, diphtheria, pertussis, tetanus, polio, measles, mumps and rubella (145). Even though both mainland China and Hong Kong have comprehensive vaccination programs, this does not guarantee that every migrant from China would have received every included vaccine. For example, coverage of hepatitis B vaccine has been reported to be substantially lower in Western China (49). Furthermore, it should be kept in mind that many migrants from mainland China may have been born prior to the vaccination programs beginning. Therefore, it should be noted that it is important to assess the immunisation status of each individual traveller.

In summary

Travellers to China are at increased risk of acquiring several common vaccine-preventable diseases, including most importantly influenza and hepatitis A and B, compared to in Australia (95, 96, 102).

Tuberculosis is another disease of concern for China (110). VFR travellers, who often have prolonged close contact with the local population, are particularly at risk (36).

Hand, foot and mouth disease is of particular concern in children, and the risk can be reduced by frequent handwashing (125-127).

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Japanese encephalitis, typhoid, malaria, tick-borne encephalitis, dengue fever, chikungunya and plague are all of potential concern for those visiting particular regions of China affected by these diseases (95, 108, 115, 120, 131, 134, 139).

1.5 Health beliefs in Chinese culture

The Health Belief Model states that the determinants of health service use include perceived susceptibility to disease, perceived severity of disease, perceived benefit of health service use, perceived barriers to health service use, calls to action and self-efficacy (146-149). Therefore, the perceived benefit of interventions to prevent infectious diseases during travel, including vaccination, and perceived barriers to the use of such interventions, including cultural beliefs discouraging their use, are relevant to the study of travel health behaviour. Furthermore, certain culture-specific health beliefs and behaviours are especially pertinent to the prevention and treatment of infectious diseases, for example, the use of traditional Chinese medicine by ethnic Chinese. In this section, health beliefs that may influence travel health behaviours among ethnic Chinese will be examined.

1.5.1 Beliefs and behaviour regarding vaccination

There have been no nationwide, comprehensive studies on attitudes towards vaccination in China. However, several regional studies regarding particular vaccines in particular settings have provided insight into community attitudes to vaccines. There is evidence of sub-optimal rates of vaccination generally across mainland China, Hong Kong and ethnic Chinese in Western countries.

Studies from Hong Kong

A survey of 992 female university students at the Chinese University of Hong Kong found that 89.3% of respondents believed that it was important to receive all government recommended vaccines (150). The majority (67.9%) of respondents were certain that they had completed all childhood vaccinations, with only 2.4% certain that they had not. Within the group that had not completed their childhood vaccinations, a majority stated that they ‘forgot’ doing so. In general, there appears to not be a negative sentiment towards vaccines. However, 57% of respondents in the study were unsure about their current vaccination status regarding vaccines recommended for adults (150).

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On the other hand, several studies involving diverse population groups suggest residents in Hong Kong have a low uptake rate of recommended but unfunded vaccines. A cross-sectional survey of 1404 pregnant women in a university obstetric unit in Hong Kong found that only 33% had received the hepatitis B vaccine at their own expense, even though with the population prevalence of hepatitis B in Hong Kong being 10% there was a significant chance of acquiring the disease for non-immune adults, and for pregnant mothers with the disease there is the risk of transmission to neonates (151). Uptake of the hepatitis B vaccine was associated with higher education levels. Another survey of 568 pregnant women in Hong Kong, conducted at government-operated obstetric clinics, found that only 3.9% had received seasonal influenza vaccination in the previous year, much lower than in the USA, and only 33% were inclined to receive influenza vaccination for the following year (152). This was despite 73.4% of respondents believing that influenza vaccination was effective. Of particular concern, only 21.4% knew that the government had recommended the vaccine for pregnant women. Community-dwelling older residents are also known to underutilise influenza vaccination. In 2004, vaccination rates were 31.1% in that population, compared to the 75% target recommended by the WHO (153). A survey of 197 participants from general outpatient clinics showed that concerns about side effects were an important barrier for this population. Another reason given for not receiving vaccination was that they thought other measures, including keeping warm and using Chinese herbal teas and soups, were effective in protecting against influenza (153). Taken together, these studies show that there are multiple barriers that need to be addressed to improve vaccination rates.

During the 2009 H1N1 pandemic, a cross-sectional random telephone survey of 301 adults in Hong Kong found that only 45% of respondents would be highly likely to take up the vaccine if it was free, and the number dropped significantly to 36% if the vaccine cost up to $100. This number dropped further still if the cost was higher (154). A qualitative study involving 40 chronic renal patients regarding the 2009 H1N1 vaccine again revealed that vaccine safety was an important concern (155). Bad experiences from previous vaccinations and ‘horror stories’ patients had heard also played a role for some in rejecting vaccination (155).

Studies from mainland China

A cross-sectional study in Hangzhou, China, regarding seasonal influenza vaccination in 2010 showed low acceptability of such vaccination. Of the 489 participants, including both healthcare workers and individuals from the general community, only 33% of respondents intended to accept the vaccine, with the results for healthcare workers and community participants being not

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significantly different (156). A majority of the respondents thought that the vaccine was effective, but half either thought the vaccine was unsafe or were unsure (156). Another survey regarding both dysentery vaccination and enteric fever vaccination, with each disease studied at a separate site in China involving 501 and 624 respondents, respectively, found that only about 60% of respondents thought adults should get vaccinated for each disease (157). In this survey, belief that there was effective treatment for the disease in question was associated with lower support for vaccination, while thinking that the disease was prevalent in the wider community was associated with supporting vaccination, suggesting that risk perception played an important part in attitudes towards vaccination.

Studies from Western countries

A survey of 442 Chinese adults in Australia regarding hepatitis B found that 52% had been vaccinated (158). Better knowledge regarding the disease and younger age were associated with vaccination. Seventy per cent of those vaccinated were vaccinated in China, thus this higher rate of vaccination in this study (compared to that in the Hong Kong study previously mentioned) does not appear to be due only to immigration to Australia. However, in contrast, a survey of 504 Chinese Canadians found a hepatitis B vaccination rate of only 38% (159), and another survey of 201 Chinese patients in the USA found a hepatitis B vaccination rate of only 36% (160). The higher rate of vaccination observed among Chinese migrants in Australia is therefore not well established. However, if true, it may mean that migrant populations, and hence VFR travellers, may constitute a subpopulation where vaccination is more accepted.

In conclusion, Chinese populations do not appear to have a generally negative attitude towards vaccination, but vaccination rates remain suboptimal. There are multiple reasons for this, including knowledge deficits regarding the benefit and necessity of a particular vaccine, safety concerns and concerns related to cost.

1.5.2 Beliefs and behaviour regarding outbreaks and pandemics

There is mixed evidence regarding the behaviour of ethnic Chinese in association with outbreak and pandemic situations. Various studies conducted in Hong Kong have all found that a high proportion of residents would adopt preventive measures during both actual and hypothetical outbreaks. On the other hand, studies conducted in mainland China have found a low level of concern about influenza outbreaks.

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Studies from Hong Kong

A random, anonymous telephone survey of 999 respondents in Hong Kong during the 2009 influenza A (H1N1) pandemic found that a high proportion of respondents had adopted preventive measures in their daily lives, including frequent handwashing and wearing of face masks, especially when experiencing an influenza-like illness (161). Previous studies have also provided evidence that Hong Kong respondents were generally more vigilant than UK respondents during the early stage of the 2009 H1N1 pandemic. Two surveys conducted at a similar time found that in Hong Kong, 73.6% of respondents had increased their handwashing frequency and 9.3% had avoided crowded places (162), compared with only 28.1% and 3.7%, respectively, in the UK survey (163). A random cross-sectional telephone survey of 503 Hong Kong adults regarding a hypothetical avian influenza A (H5N1) outbreak also found that the majority of respondents would practice preventive behaviour including frequent handwashing (86.7%) and using facemasks (73.8%), and if experiencing influenza-like symptoms, would seek immediate medical consultation (94.2%) (164). It is thought that the prior experience with SARS and continued government campaigns have resulted in this widespread acceptance and adoption of preventive behaviours when facing a new pandemic threat (161). This is supported by the results of a study consisting of two cross-sectional telephone surveys conducted in June and September 2003, involving around 800 participants each, which found that there were major improvements in the reported uptake of preventive behaviours compared with the pre-SARS period, and such improvements were often sustained even in the September survey, 3 months after the outbreak ended (165). A study of 13 cross-sectional surveys during the 2009 H1N1 pandemic in Hong Kong also found that, in each survey, around 50% of respondents would be worried if they developed influenza symptoms and a majority of respondents practised precautions such as washing hands after returning home and covering their mouth when sneezing or coughing (166). However, as these studies were all conducted in Hong Kong in the post-SARS period, the results may not be generalisable to mainland China, or to Hong Kong immigrants who had left the city before the SARS outbreak.

A cross-sectional random telephone survey of 1115 participants conducted in Hong Kong during the SARS epidemic showed that respondents with a higher level of risk perception and those who were more educated were more likely to comprehensively adopt preventive behaviours (167). Furthermore, the aforementioned hypothetical H5N1 outbreak survey found that perceived susceptibility and perceived high fatality of H5N1 were associated with adopting preventive behaviours (164), and the aforementioned post-SARS health behaviour change survey also found

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that participants who were concerned about contracting SARS were more likely to have improved their health-seeking behaviours (165). This shows that education to increase awareness about the risks of VFR travel may also result in the adoption of preventive measures. On the other hand, in a 2005 random telephone survey of 986 participants in Hong Kong, 36% of respondents agreed with the statement “buying live chickens is risky to health”, but 78% of respondents said their household bought live chickens, meaning at least 14% of respondents thought that buying live chickens was risky to health but continued doing so (168). This shows that even when one is aware of a practice being risky, one may still decide to engage in it, and therefore that risk awareness does not guarantee compliance with preventive measures.

Studies from mainland China

A telephone survey of 10,669 participants across multiple urban and rural areas, conducted during the 2009 influenza A (H1N1) pandemic, found a generally low level of concern about the outbreak and inadequate uptake of precautionary measures (169). In this study, 72.4% of respondents stated that they were not worried about contracting the pandemic virus. Only 42.9% of respondents reported avoiding crowded places, and 57.4% of respondents reported avoiding contact with people with influenza symptoms. A survey of 3731 residents in China, conducted in the several months after the peak of the avian influenza A (H7N9) outbreak in 2013, also found generally low levels of concern regarding the outbreak across both urban and rural areas in many regions of China (170). Even in Shanghai, located in the area where the most H7N9 cases were reported, only 28% of respondents would be worried if they developed influenza symptoms, and only 13.6% said they were worried about contracting H7N9 in the next week. The study also found that only 30% of respondents supported closing live poultry markets during periods of outbreak, further supporting the picture of low concern.

Trust in government

A random telephone survey conducted in Hong Kong, Taiwan and Singapore, all with majority ethnic Chinese populations, involving around 500 participants at each location, showed that respondents in all three Asian locations were significantly more likely than US respondents to trust government health authorities as a source of information during an outbreak (171). This suggests a higher level of trust in government authorities in handling outbreak situations, at least regarding the residents of Hong Kong, Singapore and Taiwan and their respective governments (Mainland China was not included in the study.) However, the trust in authority may not extend to Chinese living in

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other countries, under other governments. A questionnaire study of 300 Chinese immigrants in the UK and The Netherlands found that they had less trust in information on emerging infectious diseases from their doctors and government agencies, compared with the general population (172). The same study also found that Chinese immigrants often sought information from family and friends and Chinese language media. These results from two Western countries may be more generalisable to the Australian Chinese community, than the results from the Asian countries.

1.5.3 Beliefs about and use of traditional Chinese medicine

Evidence from the literature suggests that the use of Chinese medicine is quite prevalent in the Chinese population. A survey of 362 chronic hepatitis B patients at a university hospital clinic in Hong Kong found that 32% reported a history of using Chinese medicine to treat their condition, and, among those, 84% believed that Chinese medicine was effective for their condition (173). A survey of 198 US Chinese immigrants conducted at a community clinic serving a mainly lower- income population found that almost all respondents had used traditional Chinese medicine during the previous year, and respondents would commonly use Chinese medicine for abdominal pain, cough, runny nose, dizziness and headache, all symptoms of common infectious diseases (174). A survey of 259 pre-operative patients in a Hong Kong teaching hospital showed that 90% used Chinese herbs regularly and 44% had consulted a Chinese medicine practitioner in the past 12 months, even though only 13% were taking Chinese medicine regularly (175). A study of 76 Hong Kong HIV patients on anti-retroviral therapy found that around 60% used Chinese medicine, although often for ‘minor ailments’ and ‘general health maintenance’ rather than specifically for treatment of HIV/AIDS (176). The aforementioned studies show that Chinese medicine is commonly used in a wide range of contexts, for a wide range of purposes in both China and by Chinese migrants living in Western countries.

In mainland China, traditional Chinese medicine has long been promoted by the government, but has declined in importance in recent years, with the decline being more rapid in urban areas (177). In 2006, Chinese medicine was estimated to account for 10-20% of health care provision in China (178). Data from a government-conducted household survey in Hong Kong in 2005, involving a random sample of 33,263 participants including 18,087 respondents who had used outpatient services in the previous year, showed that, of those respondents, 80.2% visited Western medicine doctors exclusively, 3.2% visited traditional Chinese medicine practitioners exclusively, and 16.6% used both types of services (179). The study also found that middle-aged patients were most likely to use both types of services. The results are consistent with another cluster analysis study of 503

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participants recruited at Hong Kong outpatient clinics. It found that there were three clusters of patient attitudes towards Chinese versus Western medicine: the biggest cluster (63%) had considerably more belief in Western medicine than Chinese medicine, and they tended to be younger; another cluster (24%) were sceptical of Western physicians, and tended to be older, poorer, female and were more likely to have chronic health problems; and the remaining cluster (14%) had strong faith in both Chinese and Western medicine, and were of intermediate age (180).

A qualitative focus group study in Hong Kong involving 29 participants found that respondents believed Western and Chinese medicine to both have their strengths and weaknesses. Chinese medicine was thought to be better for “curing the root of the problem” (quoting the author), while Western medicine was quicker and more powerful, but had more side effects. Both types of medicine were used concurrently by many respondents (181). A qualitative study on Chinese immigrants in the USA, involving 30 Chinese and Western medicine health professionals and 75 non-health professional participants, also found high rates of self-treatments and home remedies, and low rates of exclusive use of Western medicine (182).

Use of Chinese medicine may be associated with socioeconomic status, though the relationship remains unclear. In mainland China, richer households in both urban and rural areas are less likely to consult Chinese medicine doctors (177). However, a National Health Interview Survey conducted in Taiwan in 2001, including 5971 children and adolescents, found that children of parents with higher income were more likely to have visited Chinese medicine practices (183). Hong Kong may be a special case regarding Chinese medicine use due to the lack of government approval for using Chinese medicine during the colonial period (184). However, this may be changing, with a 2002 government survey in Hong Kong involving a random sample of 31,762 residents finding that respondents of higher socioeconomic backgrounds emerged as a new class of Chinese medicine users (184).

Because Chinese medicine use and its concurrent use with Western medicine are both common, studies of health behaviour in ethnic Chinese populations should explore the use of Chinese medicine and any effects it may have on attitudes to Western medicine interventions. In this thesis, the topic of Chinese medicine use in relation to VFR travel will be explored in Chapters 2 and 3.

1.5.4 Self-medication

Self-medication, that is, the purchase and use of medicines without the advice of a health professional, in lieu of seeing a doctor when ill, is common in China (185). Also of particular

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concern is that self-medication users often do not know about the side effects of their medications (186). A qualitative study involving 30 participants in Fuzhou, China, found that cost and convenience considerations were important in the decision to self-medicate (185). Respondents also said they were more likely to self-medicate if faced with a health problem they thought they were familiar with. Self-medication is also very common in Hong Kong. A survey of 563 university students in 1995 found that 94% of respondents self-medicated. Information from other family members, which may not be reliable, was an important source of information when self-medicating (187). Furthermore, a random telephone survey of 1068 Hong Kong residents in 1989–1990 found that 32.5% of the respondents had self-medicated within the previous 2 weeks, and Chinese and Western medicine were used equally (186). These findings have important implications for Australian Chinese VFR travellers, who may self-medicate without receiving medical advice while overseas. This topic will also be explored in Chapters 2 and 3.

In summary

Multiple studies in mainland China and Hong Kong have found relatively low acceptance for a variety of vaccines. Risk perception, financial factors and safety concerns have been found to be major barriers to vaccination (151, 152, 154, 156, 157).

Studies conducted in Hong Kong in the post-SARS period have found that participants were generally very vigilant regarding new outbreaks, and the majority would practice preventive measures (161, 162, 164). Such studies may not be generalisable to immigrants from Hong Kong who left before the SARS outbreak. On the other hand, studies conducted in mainland China have found low concern regarding outbreaks, and inadequate practice of preventive measures (169, 170).

Studies regarding outbreaks in Hong Kong have also found that risk perception positively correlated with adopting preventive behaviours (164, 165, 167).

A study found that Hong Kong, Singapore and Taiwan participants were more likely than US participants to trust information from government authorities regarding outbreaks (171). However, another study of Chinese immigrants in Europe found that participants were less likely to do so compared with the mainstream population (172).

The use of Chinese medicine, including in conjunction with Western medicine, remains common among ethnic Chinese (174, 177, 179, 182). There is a common belief that Chinese and Western medicine are best used for different purposes (181). The use of self-medication is also common

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(185-187). Hence, these topics must be explored in any study of travel health in ethnic Chinese populations.

1.6 Conclusions

In a time of increased international travel, with the associated increase in the transmission of infections including infections with outbreak potential via travellers, travel medicine has become an important public health priority. Travellers visiting friends and relatives are at an increased risk of acquiring a wide range of infectious diseases during travel. VFR travellers have been shown by multiple studies to have low rates of seeking professional travel health advice, and commonly have knowledge deficits and misconceptions regarding various infectious diseases. They also commonly undertake inadequate pre-travel preparations and practice inadequate precautionary behaviour during their travel. VFR travellers have long been understudied in travel medicine; however, for the reasons above, it is important that this does not continue.

There have been no published studies regarding Chinese VFR travellers in particular, despite constituting a substantial proportion of VFR travel in some Western countries, including Australia. The infectious risks present in China differ substantially from the infectious risks present in the commonly studied VFR destinations (e.g. India, Latin America and Africa), and China has also been the source of multiple pandemics in the recent past. Moreover, ethnic Chinese travellers in general have many travel health-related issues in common with VFR travellers in general, including low rates of seeking pre-travel advice, low rates of vaccination and high rates of inadequate precautionary measures. As a result, such issues are potentially compounded in the case of the Chinese VFR traveller. This study aims to address this important gap in research, to inform future interventions to improve the travel health outcomes of Chinese VFR travellers, with resultant benefits to public health in Australia.

36 Chapter 2: Focus groups with Australian Chinese VFR travellers

Chapter 2 Focus groups with Australian Chinese VFR travellers

37 Chapter 2: Focus groups with Australian Chinese VFR travellers

2.1 Abstract

VFR travellers are known to inadequately prepare for their travel and also have inadequate precautionary behaviour during travel, and they are at a higher risk of acquiring certain infections compared with other travellers. Ethnic Chinese are one of the largest migrant groups in Australia, yet there have been no published studies in Australia or elsewhere regarding this population as VFR travellers. Issues specifically related to Chinese culture can influence health behaviour, potentially causing issues specifically relevant to Chinese travellers visiting friends and relatives. Moreover, China has been an epicentre for emerging infections in recent years, and Chinese travellers visiting friends and relatives are an important risk group for the future importation of such infections.

To study the travel health-related knowledge, attitudes and practices of Australian Chinese VFR travellers, focus groups were conducted at two locations in Sydney. Participants were recruited from the general community, were aged 18 years or older and had travelled to China for VFR purposes in the preceding 18 months. Recruitment was conducted via a variety of means to increase the diversity of participants. Five focus groups with a total of 51 participants were conducted. Each session was conducted with a standard focus group guide, derived from a previous literature review. Sessions were recorded and then manually transcribed. The transcripts were then analysed together, using thematic analysis assisted by the software nVivo 10.

Participants were found to generally have suboptimal pre-travel health preparations for VFR travel, and most did not seek health advice before travel. Participants described multiple factors that influenced their travel health behaviour, including low risk perception and awareness, cultural barriers to seeking health care, travelling on short notice, a reluctance to receive vaccinations for travel, and a reliance on family and friends and online sources for travel health information. Participants were generally unaware of travel medicine specialist services. Many participants also did not undertake adequate precautionary behaviour during travel, often due to low risk awareness. Respiratory illnesses and food-borne diseases (both infectious and non-infectious) were the two major concerns for participants. The influence of family and friends in both attitudes towards pre- travel preparations and activities undertaken during travel was found to be strong.

This research has provided important insight regarding the knowledge, attitudes and practices of Australian Chinese VFR travellers. It has provided additional evidence that published findings regarding VFR travellers in general, for example inadequate pre-travel preparations and precautionary behaviour during travel, including commonly not seeking pre-travel medical advice,

38 Chapter 2: Focus groups with Australian Chinese VFR travellers

and low risk perception, also apply to this population. In addition, there were several findings specific to the influence of Chinese culture on VFR traveller health, including the use of Chinese medicine and dietary habits. Overall, this research has provided important information which should inform future education interventions to improve travel health behaviour in this population.

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2.2 Introduction

Travel is a major way in which infectious diseases can spread globally (1). Travellers in general are often inadequately prepared for international travel (22, 86, 188, 189), and this is especially true of those visiting friends or relatives (VFR) (22, 23, 36, 52). Many lack sufficient travel health knowledge and report low rates of accessing pre-travel health services (18, 22, 33, 47), and hence do not take appropriate precautions (19, 36). This places them at increased risk of infectious diseases acquired during travel (15-17) and facilitates the global spread of infections (1, 2).

China is the third largest foreign country of birth amongst Australia’s population, and as of 30 June 2013, 1.8% of the total population in Australia was born in China (81). VFR travel also accounts for a substantial portion of total travel from Australia to China. Of resident departures from all Australian airports to mainland China and Hong Kong in 2010, 28.9% was for visiting friends and relatives (84). With continued immigration from China (82), the volume of VFR travel is expected to continue to rise. However, internationally, data are lacking on the travel health risks and knowledge, attitudes and practices of Chinese migrants returning to mainland China or Hong Kong to visit friends and relatives. While some aspects of VFR traveller behaviour have been found to be generalisable to VFR travellers of multiple ethnicities, each ethnic group also has culture-specific health behaviour, for example, the use of Chinese medicine in ethnic Chinese. Although there has been research of VFR travellers generally or specifically regarding travellers of various ethnicities (16, 22, 24, 42, 52, 54, 65, 190), there are no relevant Australian or international studies of Chinese VFR travellers.

China has been the source of several important emergent infectious diseases and the epicentre of global outbreaks (11) including new influenza strains and SARS. Travellers returning from China have the potential to carry important infectious diseases into Australia and other countries to which they travel (2, 3). Understanding Australian Chinese VFR travellers and their travel health-related behaviour and risks is important for many reasons, including for the health of the travellers themselves, as well as for disease control measures from a public health perspective. In this chapter, issues relating to VFR travel health-related behaviour and risks are explored in focus groups involving participants from the Australian Chinese community. Other travel health-related behaviours, for example, the use of Chinese medicine, the use of self-medication while overseas with potential implications for antibiotic resistance (191, 192), and medical tourism with potential for various health risks, including the acquisition of blood-borne infections (193, 194), are also explored.

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2.3 Methodology

2.3.1 Study design

A qualitative study was conducted using focus groups of ethnic Chinese Australians. A qualitative research methodology was deemed appropriate for the study of Chinese VFR travellers due to the paucity of data in this field. No previous studies of knowledge, attitudes and practices towards travel health in Chinese VFR travellers have been published and few qualitative studies explore travel health knowledge, attitudes and practices among VFR travellers in general. Such previous studies have, however, identified major cultural reasons underlying important travel health behaviour, such as inadequate pre-travel preparations, in the ethnic groups they studied (54, 65). Therefore, a qualitative research methodology is appropriate to identify themes that may not have been ascertained from studies of VFR travellers in general or from other cultural groups, especially in regards to the health beliefs of ethnic Chinese and how such beliefs influence behaviour.

Compared to quantitative methodologies, qualitative research methods provide a more in-depth and detailed view of a topic (195, 196) when the collection of data is not restricted to a static quantitative questionnaire. It is therefore especially suitable for exploratory research (197), where much about the topic remains essentially unknown or uncertain. Qualitative research may also identify missing links by providing insights into the underlying dynamics that led to a particular behaviour or viewpoint (198). For example, the relationship between certain behaviours and health beliefs may only be uncovered in the narratives of participants. Finally, qualitative research can illustrate both the presence of phenomena contributing to health outcomes, and also the underlying reasons for their occurrence. This is particularly important for this study in that previous quantitative research has identified VFR travellers to have low uptake of professional pre-travel health advice (86, 87), but qualitative studies may be able to elucidate reasons why this is the case (199).

Of the qualitative methods available, it was determined that focus groups would be the most suitable for the purposes of this study for a variety of reasons. The group under study, Australian Chinese VFR travellers, are a relatively homogenous group, sharing a common cultural background, and are therefore suitable for focus group study (200). In such circumstances, participants’ interactions and exchanges of ideas can provide greater insight into the issues. For example, participants can challenge and probe each other’s points of view, and participants also have an opportunity to add to and further develop a theme raised by another participant (201, 202).

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In focus groups, group discussion may also lead into unexpected territory, prompting the exploration of new themes (203). Moreover, focus groups conducted with participants of similar cultural background are conducive to the study of social norms, which is an important part of health beliefs and behaviour (204). Finally, as more people can be included in the study with less resources compared with using individual interviews (200, 202), more experiences and points of view can potentially be explored.

2.3.2 Development of interview guide

The development of the interview guide was informed by the multidimensional literature review presented in Chapters 1 and 4. This review included the following topics: Chinese travellers and travel health; VFR travellers and travel health; infectious diseases prevalent in China that may pose a risk to VFR travellers (205); previous major pandemics originating in China; attitudes to vaccination among ethnic Chinese in different settings; attitudes to self-medication with medicines bought without a prescription or consultation with a healthcare professional; traditional Chinese medicine practices; and other relevant health-seeking behaviours. The inclusion of topics in the focus group interview guide was based on prominence in the literature and pertinence to travellers. The interview guide was reviewed by other investigators (Dr Heywood and Prof MacIntyre, the supervisors for this thesis) for content and clarity. The final focus group interview guide (Appendix 2) contained the following major themes:

1. health-related preparations for travel and sources of pre-travel health advice

2. attitudes, practices and experiences regarding vaccination, both generally and specifically for travel

3. risk perception regarding travel to China and related attitudes and behaviour

4. potential infectious disease risk activities during VFR travel

5. infectious disease outbreak awareness

6. attitudes and practices towards the use of traditional Chinese medicine

7. self-medication

Although not directly related to travel medicine, the use of traditional Chinese medicine and self- medication were included as these practices were commonly reported among studies of Chinese in the literature (174, 175, 185, 186).

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Within each theme, a series of prompts were included. These prompts, again derived from the literature review, were designed to ensure the important issues of each theme were explored, although their usage would be flexible during the focus groups. Having a structure to the questions explored in each group allowed the research questions to be effectively answered and also ensured some consistency between groups, while the flexibility allowed ample opportunities for deeper exploration of issues and for participants to raise new issues within individual focus groups (201).

2.3.3 Sampling and recruitment

Eligible participants were ethnic Chinese Australians who were residents of Sydney, aged 18 years or older, and who had travelled to mainland China or Hong Kong for the purpose of visiting friends or relatives in the past 18 months. Participants were recruited to the study using a variety of methods including Chinese newspaper advertisements, shopfront advertisements and street recruiting in suburbs with high Chinese populations, and snowball sampling. This diverse combination of sampling techniques aimed to achieve diversity among focus group participants.

Interested participants were invited to register for focus groups conducted in either Ashfield or Chatswood in Sydney, Australia. These suburbs were chosen for their relatively high proportion of Mandarin or Cantonese speaking residents, according to 2011 census data. Among a total of 21,204 Chatswood residents, 2958 were Mandarin speakers (14% of total) and 2711 were Cantonese speakers (13% of total) (206, 207). Among a total of 22,183 Ashfield residents, 2964 were Mandarin speakers (13% of total) and 1330 were Cantonese speakers (6% of total) (206, 207). In addition, both suburbs are shopping hubs for surrounding suburbs which also have relatively high proportions of Chinese-speaking residents (206).

2.3.4 Focus group procedure

Five focus groups were conducted between 1 June and 15 June 2013, with a total of 51 participants. Written, informed consent was obtained at the focus group location, prior to commencing the focus group sessions. Participants also completed a demographic survey (Appendix 2) which included questions on age group, education and employment background, length of residence in Australia, and the number of previous return trips to China. During the focus groups, selected themes were explored in sequence, based on the interview guide. Each focus group took between 1 and 2 hours. Focus groups were conducted mainly in English, but some of the conversation was conducted in Cantonese and Mandarin, depending on the preferences of the participants. Two of the moderators were available to translate certain Chinese terms where required. As an incentive for participation,

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participants received a $30 gift card, university stationery and a travel health information pack. The travel health information pack included printed information useful for Chinese VFR travellers. The travel health information pack included printed information from the Australian government, the World Health Organization (WHO) and the US Centers for Disease Control and Prevention (CDC) which was deemed useful for Chinese VFR travellers, and also included university stationery. Ethics approval was obtained from the university prior to recruiting participants and conducting focus groups.

All focus group discussions were recorded, and then transcribed manually by two transcribers fluent in Mandarin and/or Cantonese. All conversation in Cantonese or Mandarin was translated verbatim into English where possible. However, translation of colloquial words and phrases aimed to preserve as much of the original meaning as possible. Random sections of the transcripts were checked for accuracy by a third transcriber who was fluent in Mandarin and Cantonese.

2.3.5 Data analysis

Thematic analysis was used to identify themes contained in the data (202). As focus groups were culturally similar and addressed many of the same themes, all transcripts were grouped together and analysed as a whole. In thematic analysis, qualitative data is encoded into explicit ‘codes’ (208). Coding is the starting point for most methods of qualitative data analysis, and involves a process of examining the data, defining what each section of the data is about, and giving each section a meaningful label (202, 209). Coding can be conducted using codes derived from prior research or theory, or it can be based entirely on the data obtained (inductive coding or data-driven coding) (208). As there was little prior research or theory available on the topic being studied, inductive coding was used for this study. In inductive coding, themes or codes are not pre-determined in any way, but are derived directly from examining the raw data (208).

Coding is a process of pattern recognition (208), where patterns or themes are observed in the data and noted. Therefore, the first step is to gain familiarity with the data. To this end, the transcripts were closely and repeatedly examined to identify the themes and produce a draft list of themes. Coding for this study was conducted using QSR nVivo software, version 10, and was completed in two stages, as per common practice (209). Using standard practice for thematic analysis (210), the first stage consisted of closely examining each line of transcript, and coding sections whenever a significant theme emerged from the data. The draft list of themes was used to guide this process; however, new codes were created in instances when data did not fit into pre-existing themes. This

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process resulted in the majority of data assigned with one or more codes. In the second stage, the codes were re-analysed, in an attempt to refine the codes into useful analytical categories. In this process, codes identified as representing the same phenomenon were merged, and some codes were further split into two or more new codes when two or more independent themes were able to be identified within them.

The codes generated from the coding process described above were gathered into a structure of themes and subthemes (202), again using the coding function of nVivo 10. In this process, codes representing related concepts were categorised into major themes. The list of themes and codes were independently examined by another researcher (Dr Heywood, supervisor for this thesis), using nVivo 10, and discrepancies were discussed. A final list of themes and codes was then compiled, with the agreement of both researchers (Dr Heywood and myself). A thematic map was also developed to visually explore how the major themes may relate to each other and is shown in Figure 1.

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Figure 2.1: Thematic map

Once the structure of themes was finalised, each theme was studied again separately. The codes under each theme were scrutinised, analysed and summarised. Within the description of each code, selected cases and quotes were used to further demonstrate the ideas underlying the code and to provide context (209) where appropriate. Within each theme or subtheme, the code descriptions were then combined and arranged into a description providing a complete picture of each theme. The final results, arranged by themes, were then prepared.

2.4 Results

2.4.1 Participant characteristics

A total of 51 respondents participated in five focus groups ranging in size from 5 to 17 participants. The first three groups were conducted in Chatswood followed by two in Ashfield. The final two focus groups yielded similar themes to the first three and no major new themes emerged. The demographic characteristics of the focus group participants are presented in Table 2.1.

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In general, participants were mostly middle aged and older adults, with 79% of participants aged 45 or older. The participants had mostly lived in Australia for relatively long periods of time, with the majority of participants having lived in Australia for more than 10 years. The majority of the participants had completed tertiary education and eight participants were currently studying. Thirty- one participants were either retired or unemployed, and 17 had some form of employment. Since living in Australia, the participants had made an average of 5.5 return trips to China.

Table 2.1: Focus group participant demographics (N=51)

Number Percentage Characteristic (n) (%)

Age (years) 18–24 0 0 25–34 4 8 35–44 6 12 45–54 13 25 55–64 14 27 ≥65 14 27 Gender Male 13 25 Female 34 67 Unspecified 4 8 Education School certificate 2 4 High school certificate 12 24 Certificate / diploma 13 25 University degree 22 43 Not reported 2 4 Employment Not employed or retired 31 61 Full-time or self-employed 11 22 Casual and part-time 6 12 Not reported 3 6 Study Not studying 41 80 Full- or part-time study 8 16 Not reported 2 4

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Length of residence in Australia Less than 1 year 1 2 1–5 years 9 18 5–10 years 8 16 More than 10 years 32 63 Not reported 1 2 Born in Australia 0 0 Number of trips to China since living in Australia Average* 5.5 – Range 1–20 –

* The average number of return trips to China includes only participants who provided a response to the question “Since you have lived in Australia, how many times have you been back to China?”. If participants provided a range, the midpoint of the range was used. No response was recorded for 5 participants.

Pre-travel issues

2.4.2 Risk perception and awareness of travel-associated infectious diseases

Participants generally believed that China was a low-risk destination for travel-associated infectious diseases and a number of reasons were given for this perception. Familiarity with the destination, including spending their childhood in China, was commonly perceived by participants. On the other hand, participants from Hong Kong saw travel to mainland China as higher risk.

I was born and grew up there, what is there to be scared about? … There are 1.3 billion people in China, so it’s not that bad a place that you can’t have people living there. (Participant 701, lived in Australia for less than 5 years)

Hong Kong is better. Air is better, the food is cleaner than in China. (Participant 604)

Accompanying a low perception of risk was a low awareness of potential infectious disease risks during travel to China, including during travel to rural and regional areas. However, some participants identified rural travel as posing a higher risk than travel to cities in China, including the perceived need to carry “a little bit more medicine” as preparation for rural travel. Very few participants were aware of the need for a rabies vaccine if bitten or scratched by animals, few

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participants were concerned about sanitary conditions in rural areas, and there was a generally low awareness of vector-borne diseases of concern during travel to China. When asked specifically about mosquito avoidance and vector reduction measures, one focus group concurred that they were not particularly worried about the issue.

In contrast with their attitude towards travel risks in China, group participants were generally in agreement about the need to seek medical advice prior to travel to destinations in the developing world including India, countries in Southeast Asia or Africa. Participants clearly viewed that travel to China posed a much lower health risk than travel to such other destinations. Comparing China to India, one participant (102) said that “India’s health condition is worse than China”. This was despite few participants actually having any experience in seeking medical advice for travel and few having experience of travelling to such other destinations.

Some participants who have been living in Australia for a long time described perceived issues of changed immunity and increased susceptibility to certain infectious diseases when returning to China. However, more recent immigrants were less likely to consider this factor over their perceived familiarity with China.

My immune system is used to very clean food in Australia. Withdraw your ability to go against bacteria. (Participant 610, lived in Australia for more than 10 years)

In contrast, even among participants who see travel to China as low risk for themselves, concern for the potential travel risks for children who did not grow up in China was raised by participants. One participant (203) mentioned that they were worried about their son, and had previously consulted their GP to vaccinate him against hepatitis A and B before travelling to China.

2.4.3 Preparing for travel to China

Although some participants sought professional advice, the majority did not, including some who reported no health-related preparation prior to travel to China. Those participants who did obtain travel health advice did so from a variety of sources. Few participants reported seeing a health professional before any of their return trips to China. The majority reported that they instead sought health information pertaining to their trip from other sources, particularly family and friends in China and news publications from China, often online. Familiarity with the travel destination was an important factor in the participants’ perception that pre-travel health preparation and seeking advice on minimising infectious disease risks were not necessary.

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Consultation of medical professionals

Participants expressed a range of views on the need for pre-travel advice from a healthcare professional. There was a perception among many participants that if you are not sick, you do not need to see a doctor, or that there is no point in seeing a doctor for travel.

Although the majority of participants reported some form of travel health-related preparations, including seeking travel health advice, getting vaccinations and bringing medications, several participants reported doing nothing at all in terms of travel health preparation for their previous trips to China.

Last time I didn’t do anything, just go. But I’m OK. (Participant 207)

While several participants planned their trips well in advance, travelling whenever cheap tickets were available, other participants reported departing from Australia at short notice, for example, for family emergencies. One participant (705) had to urgently visit their father in hospital, and did not seek any travel health advice. Furthermore, onward travel, often including destinations not determined at the time they leave Australia, may present a problem for appropriate pre-travel vaccinations.

Every time I go back to Hong Kong I try to join tours whatever is available, so I couldn’t tell you exactly when I’m going or where I’m going. (Participant 303)

On the other hand, a minority of participants had consulted a GP for one or more of their previous trips to China, including several participants who did so before every trip. Participants who consulted a GP before trips to China, either for some or all trips, tended to be female, had tertiary education and had migrated to Australia 10 or more years ago. Reasons provided for consulting their GP before travel included vaccination, the need for prescription medications and a perception of a change in their immunity after an extended residence in Australia. A few participants cited the need for vaccination as a reason to consult with a GP before travel. However, the only vaccines specified by participants were hepatitis A and/or B (not specified in some cases) for themselves (participants 208, 209, 703) or their child (participant 203), and in one case also assessing hepatitis A and B antibody levels prior to travel (participant 304). Some participants consulted their GP to obtain medications including prescriptions to use during their trip to China. Some also reported obtaining a prescription from their GP in case they needed to use it in China.

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I scared to go get the medicine from when I travel, I always ask my GP to write the prescription so I could bring it back there to get it. (Participant 710)

Perception of changed immunity was also raised as a reason for seeing a GP, by two participants. One participant who saw their GP before every trip said:

I think from my knowledge or experience, for those who have been in this country for long, normally aware because our immune system is different, we’ve been in this country for so long, we’re not used to those environment, that kind of environment, so the chance of getting any sickness is higher than here. (Participant 711, lived in Australia for more than 10 years)

Only one participant was aware of the availability of travel medicine specialists and travel health clinics. After receiving information on the activities of travel clinics, many participants were interested. However, the cost associated with clinic visits remained a major concern for many participants and many were reluctant to use them for future trips to China. Several participants however did indicate that they may at least consider using such clinics.

I guess being healthy is very important, and before I going to China it’s necessary to avoid disease or illness in China, so I guess I will seek some advice from the professional doctor. (Participant 703)

Health information sources

The kind of information participants sought before they travelled mainly related to the weather and any major disease outbreaks, for example, avian influenza outbreaks. The internet, especially websites from China, was a common source of such information. Participants reported using general Chinese portals (one example given was www.online.sh.cn) and local Chinese news websites. Participants relied on advice available on the internet in place of professional advice from a GP for some visits.

If we didn’t see the GP then we look up. Otherwise we just see the GP and take their advice. (Participant 711)

Just check the internet. From local internet you can check what happens there. (Participant 102)

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Family and friends in China are also major sources of information for participants, which was sometimes in conjunction with seeking internet-based advice.

Most time I go to the internet, and I call my family just to ask the kind of situation there. (Participant 207)

Mostly from the internet, I guess, or my friends and relatives. (Participant 703)

Vaccination

General attitudes towards vaccination General immunisation decision-making processes by participants tended to balance the benefits of accepting a vaccine against the potential safety issues, including for vaccines recommended by health professionals. Consistent with this idea, some participants’ willingness to receive a vaccine depended on their perceived risk of acquiring the disease and/or their perceived risk of serious consequences arising from the disease.

As well, take it is take a risk, not take it sometimes as well take a risk as well … I prefer take the vaccine. (Participant 301)

If something I don’t know and I doubt very much I will get that, I wouldn’t take the vaccination. Unless it’s well publicised that this is going on, like AIDS and things like that. (Participant 303)

For many participants, concerns regarding the vaccine efficacy, or lack thereof, was a major consideration in their decision-making process. Discussion among participants focused on influenza vaccination, with opposing views on its effectiveness. A previous good experience after vaccination, for example a perception of fewer influenza infections after having the influenza vaccine, increased confidence in the vaccine among some participants. Those who perceived poor effectiveness had low intentions for future vaccination, including those with previous experience of influenza-like infection even after influenza vaccination.

I think I would be better not taking it. I’ve been taking once 3 years ago and nearly the same, so I don’t want to take it. (Participant 710, in relation to the annual influenza vaccine)

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Because last year I had a very very bad flu cold, I think one month … and this year thought oh I better take it, and I did. (Participant 207, in relation to the annual influenza vaccine)

The flu, even if I’m not travelling, in Australia, every March or April I went to the GP and have my flu vaccination because it seems to work for me very well. Since I retired I still do that. Before I work in an office and the office arranged for a doctor to come in and give flu injections to all staff. And since then I find it very good, so I thought I’ll just keep on with it. (Participant 303, in relation to the annual influenza vaccine)

Many participants were concerned about the safety of vaccines and some cited pain as a reason not to have a vaccine. Some participants stated that they were reluctant to receive a vaccination without knowing its side effects and a few were particularly concerned because they had heard of cases of severe side effects from vaccination. On the other hand, other participants reported minor side effects after certain vaccinations, but were not particularly concerned because they were generally short-term and self-limiting.

One of my friends, 2 years ago she had the injection and she fainted at home, and the second day her daughter feel uncomfortable with the tummy, so they’re worried about from the vaccination, the flu vaccination. (Participant 207)

At least I have to get the doctor to explain what’s the side effect and what’s that vaccine’s going to help me. I have to really understand what I’m taking before I decide on what to take. (Participant 303)

One major concern among participants was that there were no vaccines covering many emerging diseases. There was also the perception that the influenza vaccine was not useful due to ongoing mutations and that the influenza vaccines were playing ‘catch-up’ as the influenza virus mutated.

It can prevent certain disease, but not all the disease. Certainly not the emerging one still troubling. (Participant 108)

Last year I didn’t take the flu injection because I thought not really very useful because the virus, they can change to another. (Participant 207)

Some participants reported a belief that only certain at-risk groups (e.g. the elderly) need to be vaccinated, and because they are not in that group themselves they do not need to get vaccinated.

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Having the annual influenza vaccine was prevalent among older participants, but younger participants generally believed that they do not require it. Some participants also reported a belief that if one had a good immune system, vaccines are not necessary. Others also believed that their immune system may be better off in the long run without vaccination. One participant (610) cited this reason for ceasing to have the annual influenza vaccine.

I think it’s not necessary for the people if they are not old. (Participant 608, in relation to the annual influenza vaccine)

I think it’s most important to have a strong immune system. I won’t go to a GP to ask to have vaccinations because there are too many different vaccinations. (Participant 601)

Many participants demonstrated significant misconceptions about vaccination in general. Several participants thought that if they were healthy or had a strong immune system they did not need to get vaccinated, or that getting vaccinated too often would adversely affect the immune system. Some participants also had misunderstandings about particular vaccines. For example, one participant thought the influenza vaccine offers protection for SARS as well. Some participants felt that they were not well-informed about vaccines in general.

I think I can ask but about vaccinations there are too many types, so if I were to get a vaccine just to go back, I wouldn’t know what vaccine to take because I’m not very informed in this area. (Participant 609)

Many participants reported that they have had all or nearly all of their childhood vaccinations. Some said they were unsure or that they did not remember clearly and had no records, and a few said they did not complete their childhood vaccinations.

Vaccinations and travel

Many participants felt that vaccination was not specifically needed for travel to China and many had never received a vaccine for the purpose of protecting against travel-associated diseases. However, many participants were willing to receive a vaccine prior to travel if the disease was specifically associated with a current outbreak. This was explored in depth in the focus groups and is described separately in Chapter 4. Apart from outbreak situations, when asked if they would be willing to receive a vaccine for travel if recommended by their doctor, many participants said it

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would depend on other factors, including the seriousness of the condition, vaccine side effects and safety; others were not willing to receive travel vaccines at all.

If you’re not sick you don’t need the vaccination. (Participant 101, in relation to vaccination for travel)

I wouldn’t really go for vaccines because I think I’m healthy. (Participant 616, in relation to vaccination for travel)

Other barriers to low uptake of pre-travel vaccination included the lack of recommendations from their GP, not having enough time to obtain such vaccinations for those travelling on short notice, and fear of allergies to vaccines affecting their ability to travel.

I think so, some people will get allergic to something, so you don’t want to really get sick before your trip. (Participant 303)

A few participants did assess their vaccination status prior to travel. As a consequence of the focus group discussion, several other participants have also indicated that they may ask their GP about vaccinations before their next trip. Several participants also reported a habit of getting their yearly influenza vaccines before travel. As with the influenza vaccine in general, such participants tended to be older.

When you’re travelling there’s a higher risk of getting flu due to the changing weather and not being used to it. Therefore I take the vaccine before travelling. (Participant 617, aged ≥65)

Actually even if there’s no flu in that area, the travel doctor still advise to take those because we’re long enough in this country and our system is used to the environmental atmosphere in Australia, and our immune system cannot stand that. So I will, even when there is no flu or no particular disease. (Participant 711, aged 55–64)

The use of prescription and non-prescription medication

Self-medication was common among participants. Some said they would take medications to China for use as part of their travel preparations. Participants mentioned both Chinese medicine, such as Ban Lan Gen (Isatis root, a herbal medicine), and Western medicine, such as Panadol, in relation to this.

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One participant (605) said they took antibiotics, given to them by their son, before going to China. Another participant said they took some Chinese medicine before meals “to avoid food poisoning”.

Issues during travel

2.4.4 Travel activities and itineraries

Participants commonly reported activities undertaken with family and friends during their return visits to China, such as eating outside the family home and touring other parts of China. Although the majority of participants confined their visits to urban areas, particularly large cities, several participants across a number of focus groups described travel to rural areas. These rural trips were described as holidays and weekend trips taken with their friends and relatives or trips to stay with other friends and relatives. Participants undertook both self-organised holidays and travel as part of an organised tour group departing from their hometown or travel base; these trips were often unplanned at the time of departure from Australia. Although the majority of participants reported staying with family and friends during their return trips to China, some participants reported living in their own houses which they still owned. Hotels were mainly used during travel to parts of China outside their home city.

2.4.5 Particular health concerns during travel

Respiratory illness: infections and air pollution

Respiratory illness was a major health concern during travel to China. For the participants, the issue of respiratory illness included both respiratory infections and the problem of pollution in China’s major cities, and the two issues were considered collectively. Participants who had experienced symptoms of upper respiratory discomfort in their previous trips to China were unsure whether the cause was an infection or pollution. While the emphasis of the focus groups was infectious disease risks, it is worth noting that air quality was of greater concern to many participants. Some participants also attributed symptoms such as headaches and sore throat to the poor air quality in China.

I have sick with bronchitis. It’s the air, it’s the pollution. Since I came to Australia, I felt free. (Participant 605)

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When we go to China we are not used to the air quality, so you get sick. If you live there longer, like one months, two months, you get used to it, so everything still fine. (Participant 102)

Some participants reported they got an upper respiratory infection every time they returned to China. One participant from Hong Kong (604) thought that there was a higher risk of getting influenza in mainland China than in Hong Kong. Some participants believed that ‘keeping healthy’ (i.e. maintaining good general health by sleeping well, eating well and exercising) can prevent regular respiratory infections.

Participants frequently associated respiratory infections with crowded areas. China is a very populous country, and many participants reported visiting crowded areas during their trips, including shopping centres. Although some participants mentioned avoiding crowded areas as a possible way to reduce the risk of respiratory infections, it was mentioned that in Hong Kong this was difficult because ‘everywhere is crowded’.

Participants had mixed attitudes to face masks as a method of reducing the risk of acquiring respiratory infections. Several reasons were given for the use of face masks, including poor air quality, cold weather and outbreaks of respiratory infections. Others preferred not to use masks because they look “weird” or were uncomfortable but noted that wearing masks in public was more socially acceptable in China than in Australia.

If nobody around me wears a mask I wouldn’t wear. (Participant 411)

It depends on the season. There are a lot of people wearing masks during winter ’cause it’s really warm as well, but in summer I don’t think people will wear masks. (Participant 407)

Food safety

Food safety was a particular concern for many participants during travel to China, including potential contamination from both infectious and non-infectious sources. Unsolicited concerns related to infectious sources included food poisoning and hepatitis. Unsolicited concerns related to non-infectious sources included claims of carcinogenic substances in food grown in China and the use of poor quality or ‘recycled’ cooking oil by food establishments in China. Although this study was focused on infectious disease risks, the non-infectious aspect of food safety was a major concern for many participants.

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A significant proportion of the discussion around food safety was dedicated to the consumption of street food and, to a lesser extent, restaurant choices in China, with many participants describing attempts to carefully select food establishments. Again, participants from Hong Kong generally believe mainland China to pose a higher risk than Hong Kong in terms of food safety. One participant from Hong Kong (108) specifically stated that they were not worried about food safety in Hong Kong, but were worried about food safety in mainland China.

Participants were divided over whether it is safe to eat street food in China. Those who were willing to consume street food were generally not concerned about associated health risks, as they perceive it to be a common practice. Among those who were cautious about street food consumption, hygiene concerns were the main reason for limiting or abstaining from this practice. Attitudes to street food did not appear to be related to demographics. However, attitudes and practices appeared to be influenced by family and friends.

Everyone’s eating it so we do too. We’re not concerned at all. (Participant 106)

It’s quite dirty. (Participant 708, explaining why they would not eat street food)

We eat as well, because we go there, that is the particular specialty in that area, why not then, but we just try to have less. (Participant 711)

Concerns about food safety practices of restaurants in China were widespread. Restaurant choice was subjective and most often based on visiting restaurants by reputation.

The way they cook it and the restaurants in general is not very hygienic really, not as clean as here I think. (Participant 201)

In China, the easiest way to get ill is by eating, because the chopsticks, because after being washed it is used together. (Participant 610)

I try to go to bigger restaurants, although those aren’t particularly safe either. (Participant 602)

Much of the discussion around restaurant choices described the influence of family and friends. Since participants spent a lot of time with family and friends, and eating together at restaurants was a major activity for many participants, their eating habits and food choices in China were influenced by their family and friends.

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When I was in China, I absolutely lost control. I went crazy. They were so friendly, they were like been missing you, and offering all this food. (Participant 201)

I eat what other people eat. (Participant 607)

Participants reported that their family and friends in China would consciously choose restaurants they perceive to be lower risk for them and many participants felt that it is safer to accept the recommendations of family and friends when choosing restaurants.

We live here quite a long time, so maybe not like them, they eat every day, should be okay, no problem. They will ask you to some restaurant they think is little bit health and safe, so they most time just let you go there. They’re concerned, they know. (Participant 206)

I don’t normally eat outside or in a place I don’t know. I only go to places my friend took me, or joining a tour group, that would be safer. (Participant 303)

Other techniques for avoiding or treating food-borne illnesses included hand hygiene through the use of hand sanitisers and carrying diarrhoeal medication such as Imodium. Participants also described the belief that alcohol or the consumption of garlic kills germs.

Other concerns: wet markets, animal contact and hepatitis

Most participants reported no animal contact during their previous trips to China, apart from the animals being sold in the wet markets. Visiting wet markets and food preparation were not commonly reported. However, many participants reported that their family members prepared food purchased from wet markets during their stay. Participants were not concerned about the risk of infections acquired at wet markets. The general impression was that changes to wet market practices had removed the risk.

Both hepatitis A and hepatitis B were a concern for some participants. Some participants reported prior vaccination, as discussed previously. Some raised concerns about hepatitis A when discussing food safety. However, others, including those who sought to have dental procedures in China, did not share the same level of concern regarding hepatitis B and other blood-borne illnesses.

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2.4.6 General healthcare-seeking behaviours and the use of medicines

Chinese medicine

The use of traditional Chinese medicine was a common, but not universal, practice among participants. Some participants reported using Chinese medicine in China more than in Australia because of greater availability, wider variety and lower cost. However, other participants said they used Chinese medicine at the same frequency in both China and Australia.

When using Chinese medicine, some participants saw professional Chinese medicine therapists, while others self medicated. Some participants used Chinese medicine regularly for its perceived long-term health benefits. Those who used Chinese medicine often did so in combination with Western medicine. The general consensus among participants was that Western medicine was more effective and necessary for acute health problems, while Chinese medicine worked slowly and was therefore more appropriate for chronic conditions and long-term health maintenance. Some participants believed that Chinese medicine had fewer side effects, but there were participants who disagreed with this.

Self-medication

Many participants reported self-medicating, using both Chinese and Western medicine, for what they perceived to be minor illnesses. This happened in both China and Australia. Some participants said they self-medicated more in China because many medications do not require a prescription there. However, some (but not all) participants said that a prescription is now required for purchasing antibiotics in China. Some participants also said they would purchase medicines in China and bring them to Australia to use. Mostly, this involved Chinese medicine but some participants bought antibiotics in China and brought them to Australia.

Comparative health care in Australia and China

Participants had mixed views of the comparative quality of the medical care in China and Australia and their preferred country for seeking health care. Some participants preferred accessing health care in China because of familiarity, including being surrounded by family and friends and knowing where to access health services. Several participants from Hong Kong also said they would prefer to wait to see a GP in Hong Kong if they got sick while travelling in mainland China. The language barrier in Australia was another reason for preferring China. Many participants also criticised the inconvenience of health care access in Australia. This included the need to book appointments and

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long waiting lists for surgery. This resulted in some participants reporting that they would wait to seek treatment during their next trip to China.

If I get sick, as long as I can walk, and I can wait, I would see the doctor in China. It’s too slow here. You have to wait forever here. If I need an examination here, I have to wait until the end of the year. I can see the doctor whenever I want in China. (Participant 602)

On the other hand, some participants preferred seeking healthcare in Australia, as they were more concerned about problems with the Chinese healthcare system.

In China there was a major social problem is that if you are going to have a surgery you have to pay the doctor special pocket money in order to put you in the first of the queue or pay more attention to you. That’s a kind of really a norm, social norm there in China, it’s unspoken kind of thing, which was really horrible. (Participant 201)

Cost was another factor affecting participants’ preference for seeking health care in either Australia or China. Of the participants in our focus groups, some had government healthcare coverage in Australia but not in China, and some had coverage in both countries. Furthermore, some participants said they would go to China to see the dentist and for elective dental work because it is cheaper there; dentists are generally not covered under the government’s Medicare program in Australia.

I have a Chinese friend with a tooth problem, who flew back to China just to get his teeth done, and it was still cheaper than doing it here. (Participant 701)

One participant (201) did, however, say that hygienic standards of dentists in China may not be up to Australian standards. Although this participant acknowledged that there may be risks regarding blood-borne illnesses (e.g. hepatitis B), this did not over-ride lower cost as the determining factor for seeking care in China.

An important related factor was that some participants said they would travel on a plane between Australia and China even if they were sick. This was raised in a context not specifically related to healthcare location preferences, but there may be potential interplay between the two issues.

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2.5 Discussion

2.5.1 Overview

Five focus groups were held, involving a sample that was diverse in education and employment background, and place of origin in China and likely to capture a broad range of views and experiences within the Australian Chinese VFR traveller context.

Consistent with the published literature on VFR travellers in general (16, 19, 22, 36, 211), participants in the focus groups were found to commonly undertake suboptimal travel health preparations for VFR travel, due to both multiple barriers to health care access and a generally low risk perception of VFR travel. This finding is also consistent with published literature showing that Asian travellers had low rates of obtaining pre-travel advice and receiving travel vaccinations (86).

Participants’ main health concerns regarding VFR travel were respiratory illnesses, both infectious and due to pollution, and food safety concerns, again both infectious and non-infectious. This is consistent with a GeoSentinel database analysis showing that respiratory illnesses and acute diarrhoea were among the most prevalent presenting conditions of travellers to China (136). Participants were found to commonly use Chinese medicine for both curative and preventive or health maintenance purposes. Mixed use of Chinese and Western medicine was also common, consistent with findings from the literature (173, 181). Self-medication was common, including in some cases with antibiotics, which some participants even brought to Australia from China. This concern has also been previously highlighted in the literature, with Australian Chinese immigrants found to have high rates of antibiotic storage at home, and substantial rates of bringing antibiotics into Australia (32% in one study) (212).

2.5.2 Multiple causes of suboptimal travel health preparation

According to the Health Belief Model (HBM), people use or do not use health services based on several key determinants, including perceived susceptibility to illness, perceived severity of illness, perceived benefit of accessing health care, perceived barriers to accessing health care, calls to action and self-efficacy (146-149).

Among focus group participants, there was a general perception of VFR travel to China as low risk. The low risk perception among study participants, which will be discussed in detail in the following sections, was due to multiple factors, including a perception of familiarity, knowledge deficits and misconceptions. In the HBM, perceived susceptibility and severity, which can be further combined

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into the concept of ‘perceived threat’ (213), are closely related to risk perception. Therefore, using the HBM, it can be predicted that low risk perception reduces the drive to participate in risk reduction activities. In fact, studies have shown that risk perception correlates with vaccination behaviour (214, 215) and a variety of other health behaviours (216-219).

According to the HBM, perceived barriers to health care access are another important reason for inadequate use of health services. Among this group of Australian Chinese VFR travellers, few reported experience of consultation with a healthcare provider to manage health risks prior to travel to China. Multiple barriers to seeking pre-travel medical consultation were identified, including unfamiliarity with the Australian healthcare system, the language barrier, and cost barriers. All these will be further explored in the following sections.

Due to the multifactorial causes of suboptimal travel health preparation, any future education campaigns to improve pre-travel health preparation and outcomes in VFR travellers should be similarly multifaceted. Campaigns should have dedicated components to target each factor, while also keeping the other factors in mind. For example, awareness campaigns to improve risk perception and knowledge need to provide information in a linguistically and culturally accessible manner. These ideas have in fact been reflected in published recommendations for improving VFR traveller health outcomes (19, 220).

2.5.3 Multiple barriers to accessing health care

For more recent immigrants, unfamiliarity with the Australian healthcare system was identified as a barrier to seeking health care in Australia. Many participants reported being dissatisfied with the Australian system, for example, because GP consultations are only available with an appointment, and because specialist consultations are not directly available without first seeking a GP referral. This is in contrast to China, where appointments, including with specialists, are often available right away. Those who are not used to the Australian system often found it cumbersome. Unfamiliarity and dissatisfaction with the healthcare system has also been reported in other migrant studies (221- 223). A study of Iranian migrants to Canada found dissatisfaction with the referral system in Canada, as patients in Iran (as in China) can directly access specialist care (222). Education of recent migrants on the benefits of the appointment and referral systems in Australia and how patients can effectively obtain health care under such a system is therefore needed, for both Chinese and other immigrants.

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Given the unfamiliarity with the Australian healthcare system among participants, it was not surprising that there was also a widespread lack of awareness of professional travel health clinics. This is consistent with published literature regarding VFR travellers in general, which reports very low rates of using travel health services (23, 47). Clearly, it is necessary to increase the awareness of professional travel health clinics among the Australian Chinese community and likely also among VFR travellers in general.

The cost of vaccination and specialist travel health services was another major barrier to accessing these services. When told about the availability of professional travel health clinics, many participants were initially interested. However, when told that they would have to pay to attend the clinics, some participants showed a reluctance to pay. This is a significant issue as, not only do the clinics charge a fee, patients generally also have to pay out-of-pocket for any vaccinations they receive. Out-of-pocket costs of travel vaccinations are commonly recognised by health professionals as an important barrier to uptake of these vaccines (58). Although multiple previous studies in VFR travellers have found that cost was not among the most commonly given reasons for not undertaking adequate prophylaxis or not obtaining pre-travel advice, it was still sometimes given as a reason (24, 33, 52). Therefore, besides raising awareness among VFR travellers about specialist travel clinics, it will be equally important to address why using such clinics, especially for more complex travel itineraries, and paying for recommended vaccinations is worth the expense.

As previously mentioned, according to the HBM, people are more likely to use health services when they have a higher level of risk perception, and also when they perceive strong benefits from using health services. Therefore, campaigns to both raise risk awareness for VFR travel in general and to educate travellers on the benefits of vaccination (including evidence for efficacy) are likely to encourage more VFR travellers to pay for vaccination out-of-pocket. However, for those with less economic resources, accessing non-critical health care out-of-pocket is often not an option they will consider (224). Therefore, if medical coverage of travel health clinics could be provided by the government, a major barrier to access can be removed. Although there may be objections on the grounds that travel is not essential, funding travel health clinics may be justified on the basis of their benefit to Australian public health.

Professional travel health services are usually provided in English in Australia which creates a language barrier for some VFR travellers. This can be an issue even for some Australian Chinese who are fluent in English, as demonstrated by the fact that some participants who could otherwise converse in English nevertheless had difficulties with understanding and expressing medical

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concepts in English. The necessity to understand culture-specific practices is also important, as demonstrated by participants’ widespread use of Chinese medicine, for both preventive and curative purposes, in conjunction with Western medicine. Linguistic and cultural appropriateness is a major requirement for effective health care access in migrant groups, including Chinese migrants (223, 225, 226). Therefore, to improve access to professional travel health services by VFR travellers, linguistically and culturally appropriate services, for example, delivered by Chinese-speaking doctors, need to be developed. Where these services are not yet available or feasible on a large enough scale, the use of interpreters, though not a complete solution to cultural barriers, can be helpful. However, a recent study has estimated that only less than 1% of medical consultations in Australia use interpreters (227). Clearly, more needs to be done to raise awareness among medical professionals and highlight the benefits of using the interpreter system in Australia.

Language, cost and system barriers to health care access have not been reported as major factors hampering optimal pre-travel health preparations in VFR travellers in previous quantitative studies (24, 25, 32, 47). However, as quantitative studies typically only allow respondents’ answers to be classified into several limited options, they may not be telling the whole story. In fact, a qualitative study in Texas, USA, on Nigerian VFR travellers found quite a lot of common themes with this study (54). As with this study, the US-Nigerian study also found a low rate of obtaining pre-travel health advice, with travellers instead relying on family and friends and other information sources; self-medication was common and cost was a barrier to accessing health care. Thus the issues identified among Chinese VFR travellers in this study appear to be generalisable to VFR travellers in general.

Another major factor in the failure of study participants to attend for pre-travel health consultations was a strong belief that there is no need to see a doctor if one is not sick. This may reflect a lack of understanding among parts of the Chinese community in Australia about the role of healthcare providers in disease prevention in the Australian healthcare system, which also relates to their unfamiliarity with the Australian healthcare system more generally. The concept of preventive medicine is not totally unfamiliar to the participants, as many have used Chinese medicine for health maintenance and preventive purposes. However, they may still be unfamiliar with the concept of preventive medicine in the context of Western medicine, and travel medicine in particular. The fact that many participants thought Western medicine was better for acute illness while Chinese medicine was better for health maintenance supports this view. This is an area that

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has not been explored in the published literature, and future studies to explore the above ideas will be useful.

2.5.4 Familiarity a key factor in low infectious disease risk perception

China was generally perceived as a low-risk destination in terms of infectious diseases. Consequently, participants were of the opinion that there was no need for pre-travel health advice. These two beliefs arise partly from the participants’ perceived familiarity with China, as they have generally lived in China for extended periods of time without encountering serious infectious illnesses. Awareness and knowledge deficits, which will be discussed in the next section, also contribute to these two beliefs. Combined, these two beliefs meant that most participants saw seeking pre-travel health advice for travelling to China as unnecessary.

Although participants in this study generally believed that China was a low-risk destination for themselves, some travelling with children not born in China stated that they would specifically seek professional health advice and vaccinations for their children. This notion has also been found in other qualitative VFR traveller studies, including the US-Nigerian study mentioned previously (54) and a Spanish study of Latin American and African VFR travellers (65). Consistent with this, a quantitative review of consultations at a travel clinic also showed that the majority of VFR traveller consultations at that clinic were paediatric (228). Although this was only one clinic, it supports the idea that some adult VFR travellers may seek professional pre-travel advice for their children even if they do not do so for themselves. This shows that Chinese and other VFR travellers are aware that travel to their country of origin is not risk-free, at least for children, and obtaining professional health advice can help mitigate these risks. Education campaigns should highlight and explain that there are still substantial risks in VFR travel for adults, even though they have lived in their country of origin for extended periods and are ‘familiar’ with the country. GPs serving the Australian Chinese community can also play a role in spreading this message to Chinese VFR travellers. This study also found that those who have lived for longer in Australia were more willing to seek professional pre-travel health advice. This is consistent with other studies showing that access to health services and preventive health care increases with increasing acculturation (229, 230), and highlights the special importance of reaching out to newer migrants.

2.5.5 Knowledge deficits and low risk awareness

The general perception among study participants of travel to China as low risk may be related to a lack of awareness of certain infectious risks present in China, particularly in rural areas. For

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example, although regions in southern China are endemic for dengue (115), and parts of China are endemic for vector-transmitted Japanese encephalitis (122), participants’ general awareness and concern about vector-borne diseases was poor. Proffered responses to potential infectious risks in China did not include diseases endemic in many parts of China or with a higher incidence than in Australia, such as hand, foot and mouth disease, chikungunya, typhoid, malaria, HIV/AIDS or parasitic infections (see Chapter 1 Section 1.4 for full list). This is in stark contrast to the level of awareness about the various high profile outbreaks that have occurred in China over the past decade, including SARS in 2003, the pandemic H1N1 influenza in 2009 and the recent H7N9 avian influenza outbreak. While respondents reported spending most of their time in large cities during return travel to China, low awareness of infectious disease risk in rural areas of China is pertinent to unplanned internal travel. Travel health information provided to VFR travellers to China should challenge the perception that return travel to China is low risk and advise travellers to prepare for unplanned trips to unfamiliar regions of China.

Participants also did not mention any infectious risks related to the use of Chinese wet markets, although such risks are well-documented in the literature (100). These findings should be made accessible to travellers in the community, especially Chinese VFR travellers. It is already known among the Chinese community that wet markets have played a role in previous outbreaks, and that governments have had to mitigate this risk by enforcing a change in practices. This should be a good starting point to discuss the continuing risk from wet markets and how travellers who still intend to use these markets can take adequate precautions, both for medical professionals giving advice to Chinese VFR travellers and for future education campaigns and programs.

Another area of knowledge deficit among study participants was regarding changed immunity, that is, a decreased level of immunity to certain pathogens after prolonged absence of contact with such pathogens. This knowledge deficit is known to also be common among VFR travellers of other ethnicities (21). Diseases where changed immunity plays an important role in clinical outcome are not a major risk for the majority of Chinese VFR travellers (malaria, the main example of this, is confined to certain rural areas in China, as described in Chapter 1). However, there is evidence that the composition of intestinal microbiota, which can be affected by environmental and dietary factors, can interact with the intestinal immune system and change the likelihood of intestinal inflammation when potentially pathogenic bacteria are encountered (231, 232). Therefore, ‘changed immunity’ regarding gastrointestinal infections is possible, and VFR travellers should be particularly cautious regarding food safety. Although it is encouraging to know that some

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participants, particularly those who have lived in Australia for a long time, were aware of this issue, many participants were not. Education on this issue is therefore important, especially for more recent immigrants.

Low risk awareness and the idea that pre-travel health consultation is not required for VFR travel have also been reported among other VFR travellers, in quantitative studies (24, 25, 32, 47) as well as in the qualitative study on US-Nigerian VFR travellers mentioned previously (54). This is despite the infectious risk profiles for the countries covered in these studies being quite different to that in China. As with this study, other studies in VFR travellers have also found that knowledge deficits and misconceptions about diseases and their prevention were prevalent (24, 54), even though the diseases in question were different. Thus the phenomenon of low risk awareness and poor knowledge contributing to suboptimal pre-travel health preparations appears to apply to VFR travellers in general, rather than being disease-specific or country-specific. Compared with the participants in the US-Nigerian study (54), however, the Chinese VFR travellers in this study appeared to have more awareness and knowledge about hepatitis A, although this would need to be confirmed by a quantitative study.

Given that there are so many substantial knowledge deficits, multiple campaigns would be required to target the major areas of misconception; for example, one campaign targeting risk awareness, and another targeting vaccination-related misconceptions. Campaigns could also target specific diseases, especially during or immediately after outbreaks. Such campaigns should be delivered via a variety of modes simultaneously to reinforce the message, for example, via the internet, GPs, pharmacies and airport information. Education campaigns will be further discussed in Chapter 5 – Conclusions.

2.5.6 Strong influence of family and friends

The findings of this study are consistent with some previously known characteristics of VFR travellers in general, regarding their activities during travel, which explain the different risk profile in VFR travellers. These include close and prolonged contact with the local population, consumption of food that is not often consumed by tourists, using local health and social facilities, and the potential for visits to remote destinations (14, 19, 36). In this study, the context in which these factors arise was also explored. The influence of family and friends was found to be a major common factor behind all these behaviours.

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During their VFR travel to China, many participants spend a lot of time with their family and friends, and often enjoy activities and meals together. In this way, VFR travellers would have prolonged contact with not just their own relatives but also other people they meet in their everyday activities, for example, when shopping or going to wet markets. Prolonged (as opposed to short- term) close contact with the local population not only generally provides more opportunities for pathogen transmission, it is a known risk factor for acquiring some infections, for example, tuberculosis (19, 36). This is a particularly important risk in China in light of the recent reemergence of tuberculosis there (233).

Because the family and friends of VFR travellers are likely to generally have a lifestyle similar to the rest of the local population, Chinese VFR travellers spending a lot of time with family and friends would be expected to be more similar to the local population in terms of activities, the places they go and the food they eat compared with tourist travellers. They are therefore particularly exposed to diseases that may be circulating in the local population, including food-borne illnesses that are spread through the local food. Since the food choice of Chinese VFR travellers is highly influenced by their family and friends, they often consume food not usually consumed by tourists, including food cooked in local homes, food from restaurants not visited by tourists, and even street food in some cases. This lack of choice in food consumption arising from having to eat with local families and in family homes during VFR travel has previously been described in the literature for VFR travellers generally (19, 36). However, this study found that family and friends often eat out with VFR travellers, and are sometimes concerned about taking VFR travellers to ‘clean’ restaurants. This may be a unique aspect of Chinese VFR travellers.

Because the influence of family and friends is substantially related to many major factors believed to increase the health risk in Chinese VFR travellers, future quantitative questionnaire studies should include questions around this influence. Future education campaigns also need to take into account the influence and interaction with family and friends. For example, when suggesting practical ways to undertake adequate precautions during travel, advice on how to discuss these issues with family and friends would be important.

2.5.7 Use of China-based sources of pre-travel health information

Because most participants did not get a medical consultation prior to travel to China, it is unsurprising that many instead relied on other sources of travel health advice, which are considered potentially unreliable by health professionals. Such sources included family and friends, particularly

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those living in China, unofficial sources on the internet (i.e. not from governments or international health authorities like the WHO or the CDC), and other news media. These sources provided useful information to Chinese VFR travellers in some cases, for example, advising them of the latest disease outbreaks in China. China-based sources are particularly useful for time-sensitive information, for example, on outbreaks, where Australian GPs may not always be up to date. On the other hand, travellers may receive misinformation about various topics from such non-professional sources. This has implications for both pre-travel preparation and for making the decision to travel or not during an outbreak (which will be further explored in Chapter 4). It has been shown that relying on non-professional pre-travel advice leads to a greater risk of poor travel health outcomes (69). Therefore, although information from family and friends in China and news media based in China may sometimes be useful, it must be made clear to VFR travellers that such information is not a substitute for professional travel health advice.

It would be ideal for all Chinese VFR travellers to obtain professional pre-travel advice for their VFR travel. However, it is unrealistic to expect this in the foreseeable future, given the widespread reluctance of VFR travellers to seek such advice. Therefore, it is important to try and improve the quality of the travel health advice available to VFR travellers, even from non-professional sources. The fact that some participants reported their family and friends selecting ‘cleaner’ restaurants for them to eat out at shows that many family and friends in China are interested in helping to improve travel health outcomes for VFR travellers. Given the strong propensity for many Chinese VFR travellers to rely on family and friends in China for travel health information and advice, VFR traveller education should also be delivered to travellers’ family and friends. Possible methods of delivery include pamphlets written in Chinese or social media-based material that VFR travellers are encouraged to share with family and friends. Such material should also encourage VFR travellers and their family and friends to have conversations about various topics pertinent to VFR travel, including both pre-travel preparations and precautionary behaviour while travelling, to increase awareness at both ends. Also, given that many participants reported using China-based websites for obtaining travel health information for China (rather than travel websites or Australian government sources), such information should be made readily accessible on commonly visited Chinese news websites and portals. Ideally this should be attempted by international health agencies like the WHO, providing material that could be hosted on such websites. Another method would be via paid advertising on such websites, targeting visitors from Australia (and other Western countries), with links to Chinese language travel advisories on the WHO or Australian government websites, for example.

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2.5.8 Possibility for improving pre-travel vaccination

Among study participants, there was widespread reluctance to be vaccinated for travel in general, and especially for VFR travel to China, due to a lack of perceived need. This is consistent with published quantitative studies which show that VFR travellers have low rates of accepting vaccination and complying with other prophylactic measures for travel, and compare unfavourably to other travellers in this regard (24, 52, 62, 63). A lack of perceived need for vaccination logically follows from the low risk perception surrounding VFR travel. This is also consistent with an airport study finding that Asian travellers were less likely than Western travellers to receive vaccinations for travel (86). The findings of this study suggest that, to encourage the uptake of recommended vaccines in Chinese VFR travellers, it will be necessary to address both the low risk perception of VFR travel as well as misconceptions surrounding vaccination.

Many participants had misconceptions about vaccination in general. For example, it was a common belief that vaccines are only for certain at-risk groups, such as the elderly and those with underlying medical conditions; participants believed that if they are not in these at-risk groups, they do not need to get vaccinated. The misconception that frequent vaccination can adversely affect the immune system is a particularly important barrier to accepting vaccination. This belief may be related to concepts within Chinese medicine, which has a strong emphasis on balance (234). Alternatively, it may relate to a generally low confidence in vaccines in China, as demonstrated by the lower rate of influenza vaccine uptake compared with the West (235). Public perception of vaccination in China has also been further affected by recent controversies over vaccine safety (236-238). There were also knowledge deficits and confusion among study participants over specific vaccines, for example, whether a particular vaccine is considered permanently effective, or what infectious agents a particular vaccine covers. Finally, participants expressed the very common belief that one can prevent contracting infectious diseases simply by ‘keeping healthy’ and therefore vaccines are not necessary. These misconceptions and knowledge deficits can all be important barriers to the uptake of vaccines for VFR travel.

However, some of the participants’ responses indicate that, if misconceptions and knowledge deficits can be effectively addressed by education, VFR travellers may become more receptive to the idea of pre-travel vaccination. Importantly and encouragingly, the vast majority of participants were not strongly anti-vaccination. Many participants would accept a vaccine as long as there are substantial benefits, and no major side effect or safety concerns. The perception of a lack of substantial benefit contributes to participants not accepting vaccination for VFR travel to China.

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Many participants did agree though that vaccinations were necessary for certain travel destinations. Therefore, they were not completely closed off to the idea of getting vaccinated as part of pre-travel preparations.

Correction of risk perception regarding VFR travel to China and specific education on the benefits of vaccination prior to travel to China, supported by evidence of vaccine efficacy and safety, are therefore likely to be effective in addressing the problem of under-vaccination. Education to improve knowledge has been shown to significantly increase vaccination rates in other contexts (239, 240), and even short, one-off education interventions can improve knowledge substantially (241). A study on Australian Chinese migrants, which showed that vaccination against hepatitis B was associated with better knowledge of the disease (158), further supports the potential utility of educating Chinese VFR travellers on vaccination. There is also evidence that more intensive and multimodal education interventions, for example, combining telephone outreach with brochures or face-to-face sessions, are most effective (242, 243). Therefore, education of Chinese VFR travellers regarding vaccinations should be delivered simultaneously through a variety of channels, as part of a multimodal education strategy regarding VFR travel health in general. This will be further discussed in Chapter 5.

2.6 Conclusions

Chinese VFR travellers are a population that deserve study from the point of view of Australian public health, and this research has provided insight into the travel health-related knowledge, attitudes and practices of this population. Overall, participants in this study generally had suboptimal pre-travel health preparations for VFR travel, consistent with findings previously reported in the literature regarding VFR travellers in general. Multiple factors contribute to this outcome. Participants generally believed VFR travel to China carried no substantial health risks. This was due to both a perception of familiarity and a lack of awareness of infectious risks. Respiratory illnesses and food-borne diseases were the two major areas of health risk that participants were concerned about when travelling to China. In both cases, concerns were raised about both infectious and non-infectious risks. The influence of family and friends on activities undertaken during VFR travel was found to be strong and is a major reason for the different health risk profile in VFR travellers, compared to other travellers.

Participants often obtained and relied on non-professional sources of health information for VFR travel, including the internet and family and friends. Although this is not ideal, education

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interventions should aim to improve the quality of advice from these sources wherever possible, as part of their overall strategy. Also, as such sources are often based in China, they are sometimes useful for time-sensitive information. Participants had mixed views regarding health care in China versus Australia. However, substantial barriers in Australia, including language and lack of familiarity with the healthcare system, contribute to the suboptimal use of pre-travel health advice. Participants were generally not open to vaccination for VFR travel, largely due to a perception that such vaccination was unnecessary and provided no substantial benefit. The findings of this research will be valuable in informing the design of future education and awareness-raising campaigns to improve pre-travel preparation by VFR travellers to China.

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Chapter 3 Focus groups with Chinese international students

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3.1 Abstract

International students frequently travel for VFR purposes. Moreover, university-aged travellers have been found to share many issues with VFR travellers in general, which may be compounded in the case of international student travellers. International student travellers have unique issues compared to VFR travellers in general, due to their student visa status, their non-permanent residence in Australia, and, on average, their younger age. The fact that they study on university campuses and have frequent close contact with a large student body also has important implications from an infection control point of view. Therefore, this population deserves specific study. China is the biggest source for international students studying at Australian universities, therefore Chinese international students as VFR travellers particularly warrant study.

To study the travel health-related knowledge, attitudes and practices of Chinese international students studying in Australia, focus groups were conducted at UNSW Australia, involving students who were aged 18 years or older and who had travelled to China (including mainland China and Hong Kong) for VFR purposes in the preceding 18 months. Recruitment was conducted via a variety of means to increase the diversity of participants, including poster advertisements placed around the campus and electronic advertisements distributed via sources including the student magazine, student associations and faculties and schools across the university. Two focus groups with a total of 28 participants were conducted. Each session was conducted with a standard focus group guide, derived from a previous literature review. Sessions were recorded and then manually transcribed. The transcripts were then analysed together, using thematic analysis assisted by the software nVivo 10.

Chinese international students generally had low risk perception and awareness regarding VFR travel. Particularly unique to international students was a sense of travel as ‘returning home’. They generally did not seek pre-travel medical consultation, inadequately prepared for travel, had inadequate precautionary behaviour during travel, and showed a reluctance to receive vaccination for VFR travel. Many participants also strongly relied on parents in China for travel health advice. Internet-based sources of travel information including social media were much more extensively used for health information seeking, compared with the community focus group participants.

This research has provided important information regarding Chinese international students as VFR travellers. This includes the finding that many issues applying to Chinese VFR travellers generally also apply to this population, as well as identifying additional issues unique to this population. This

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information should inform future education interventions targeting this population for improving their travel health outcomes.

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3.2 Introduction

As described in Chapter 2, Chinese VFR travellers often lack proper travel health knowledge and have a low rate of accessing travel health services. As a result, they do not take appropriate precautions before or during travel, which places them at increased risk of acquiring infectious diseases. Understanding the reasons for the attitudes and behaviour of Chinese VFR travellers is important, as interventions can be developed to change their behaviour and hence improve travel health outcomes. In Chapter 2, several important reasons and potential interventions were explored. However, as the participants in that study were mainly older immigrants, the study may not be representative of the younger immigrant population.

International students are a sizeable population in Australia, with 589,860 total enrolments in 2014 (67), and they are more likely than other university students to undertake VFR travel (71). China is by far the major source country for international students in Australia, accounting for more than a quarter of such enrolments in 2013 and 2014 (67, 244). International students from China therefore represent a sizeable population of ethnic Chinese living in Australia and would be expected to account for a sizeable proportion of total VFR travel to China.

University-aged students are an important group of travellers, with their own unique risk profile. Previous studies have suggested that university-aged travellers are generally at a higher risk of travel-related illness than older travellers (69, 70). Travellers of this age group commonly have low risk perceptions regarding travel-related infectious risks, and hence often undertake inadequate travel health preparation. Previous studies have shown that younger travellers are more willing to take health risks (72, 73), for example, eating street food while travelling (72), less likely to comply with travel-related preventive measures, for example, taking antimalarial chemoprophylaxis (72), and less willing to cancel air travel if unwell during outbreaks (245). A quantitative online survey of students studying at UNSW Australia in 2010 found that students generally had low risk perception across a wide range of potential health threats, including respiratory infections, vector-transmitted illnesses, food poisoning, and other infectious and non-infectious risks (71). The study also found that international students were less likely than domestic students to have undertaken adequate preparations for travel in a wide variety of areas, including obtaining travel health insurance, bringing medication for use while travelling, bringing a first aid kit and insect repellent, and avoiding certain foods and tap water while travelling (71). Similar to VFR travellers generally, international students have also been shown to have a low rate of uptake of travel health advice (71).

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Compared to other VFR travellers, international students pose an additional public health concern to Australia because they are studying, and often living, in a campus environment. University campuses are a type of ‘total institution’, where work, recreation and residence are all concentrated in one organisation, and are therefore particularly conducive to the spread of certain infectious diseases (74). Having a large population with varying immunisation status in frequent close contact further adds to this risk (75). Students living in dormitories are particularly at risk, due to especially close interpersonal contact while sharing bathrooms and sleeping quarters (76). There have been multiple reports of outbreaks of influenza with high attack rates associated with university campuses (74, 77, 78). Of particular interest is an outbreak in 1978, in which it was hypothesised that the intersemester vacation allowed many students to be exposed to the disease, and the resumption of classes then facilitated rapid spread among students (74). There is therefore concern that international students returning from VFR travel could trigger similar outbreaks on Australian campuses. Activities on campus may also cause student encounters that may not otherwise happen, providing further opportunity for disease spread. For example, it has been reported that during the 2009 H1N1 influenza pandemic, a university vaccination clinic may actually have increased the number of cases on campus by providing an additional avenue for disease spread (246). Besides influenza, campus-based outbreaks of other diseases like mumps, norovirus infections and conjunctivitis have also been reported (247-249). More serious infections may also be carried by international students, and potentially spread to other students. The diagnosis of polio in a returned Pakistani international student in Melbourne in 2007 highlighted this risk (79, 80). Also of particular concern is that more than half of the reported cases of multi-drug resistant tuberculosis in Victoria, Australia, during the 10 years up to 2007 were in international students (250). Further compounding these risks is the fact that, in general, university students are not aware of their increased risk of infection, and therefore undertake inadequate preventive measures, even during outbreaks. In a study during the 2009 H1N1 pandemic, it was reported that 60% of students were not aware that dormitory living posed an additional risk (76). In other studies, it was reported that most students were not concerned about the pandemic (251), and generally were not aware that university students were at increased risk (252). Not surprisingly, it was found that only 20.8% had adopted hand hygiene, and, worryingly, 66.5% would still attend university with flu-like symptoms, if they had an examination or assessment deadline (251).

In light of the above, it is important to ensure that international student travellers are aware of their infectious risks, and undertake adequate travel health preparations and precautions in relation to their travel. Therefore, understanding the travel-related health risks pertaining to the Chinese

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international student population in Australia and developing potential interventions to improve their VFR travel health outcomes is vital. The aim of this chapter is to explore the knowledge, attitudes, risk perceptions and travel health-seeking behaviours of Chinese international students studying in Australia who travel to mainland China or Hong Kong to visit friends and relatives.

3.3 Methodology

3.3.1 Study design

A qualitative focus group study was employed, using the same method and interview guide as used in Chapter 2 (for community focus groups). The target population were Chinese international students studying in Australia. As this is a relatively homogenous group, they are therefore suitable for focus group study (200).

3.3.2 Sampling and recruitment

Eligible participants were ethnic Chinese international students currently enrolled at UNSW Australia (the University of NSW), who were aged 18 years or older and who had returned to mainland China or Hong Kong during the preceding 18 months for the purpose of visiting friends or relatives.

As with the community study, a combination of recruitment methods was used to broaden the diversity among focus group participants. Participants were recruited via poster advertisements placed on campus, and electronic advertisements on selected university publications and websites. Heads of School across all faculties, the UNSW Chinese Student Association and the UNSW Hong Kong Student Association were approached to assist with distributing the study information. Invitations to participate were sent to students by Heads of School and student associations via email distribution lists.

3.3.3 Focus group procedure

Two focus groups were conducted in June 2013 at UNSW Australia. Written, informed consent was obtained prior to commencing the focus group sessions. Participants also completed a short demographic questionnaire. During the focus groups, selected themes were explored in sequence. Each focus group took approximately 2 hours. Focus groups were conducted in English, but two of the moderators were available to translate certain Chinese terms where required. As an incentive for participation, participants received a $30 gift card and a travel health information pack. The travel

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health information pack included printed information from the Australian government, the WHO and CDC which was deemed useful for Chinese VFR travellers, and also included university stationery. Ethics approval was obtained from the university prior to recruiting participants and conducting focus groups.

All focus group discussions were recorded, and then transcribed manually by two transcribers fluent in Mandarin and/or Cantonese. The portions of the conversation in Cantonese or Mandarin were translated verbatim into English where possible. Where there were occasional difficulties in direct translation, translations aimed to preserve as much of the original meaning as possible. Random sections of the transcripts were checked for accuracy by a third transcriber who was fluent in both Mandarin and Cantonese.

3.3.4 Data analysis

Thematic analysis was conducted, using the same method employed in Chapter 2. Again, as both groups were culturally similar and appeared to address similar themes, transcripts from both sessions were grouped together and analysed as a whole.

3.4 Results

3.4.1 Participant characteristics

A total of 28 respondents participated in the two focus groups. The demographic characteristics of the focus group participants are presented in Table 3.1.

In general, the participants were young adults who had been living in Australia for relatively short periods of time. The majority of participants were aged less than 25 years. All participants had lived in Australia for 5 years or less, and 39% had lived in Australia for less than 1 year. Just over half of the participants reported that they had previously completed tertiary education. Twenty-three participants were not employed, and five had some form of employment. Since living in Australia, participants had made an average of 2.6 return trips to China.

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Table 3.2: Focus group participant demographics (N=28)

Characteristic Number Percentage (n) (%)

Age (years) 18–24 25 89 25–34 3 11 Gender Male 6 21 Female 22 79 Education High school certificate 13 46 University degree 15 54 Employment Not employed 23 82 Casual and part-time 5 18 Study Full- or part-time study 28 100 Length of residence in Australia Less than 1 year 11 39 1–5 years 17 61 Number of trips to China since living in Australia Average* 2.6 – Range 0–8 –

* The average number of return trips to China includes only participants who provided a response to the question “Since you have lived in Australia, how many times have you been back to China?” If participants provided a range, the midpoint of the range was used. No response was recorded for 7 participants.

Pre-travel issues

3.4.2 Risk perception and awareness of travel-associated infectious diseases

As with the community focus group participants, international students generally believed that China, including rural areas, was not a high-risk travel destination for infectious diseases, and reported familiarity as the main reason for this perception. The international students still had a

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family home to return to in China and many had not made the decision to permanently emigrate to Australia. Therefore, there was a particularly strong feeling of China being ‘home’, which reinforced the perception of familiarity and low risk.

One important theme identified was the differences in risk perception for different geographical areas and different seasons in China.

Really I didn’t worry about the disease, ’cause it seems like the disease all break out at the eastern part or southern part of China, but in the northern part winter is really cold. (Participant 516)

When the weather gets cold, then the rate of disease will decline in my hometown. (Participant 504)

When discussions were directed towards travel to other regions, including less developed countries with a high infectious disease burden such as Southeast Asia, India or Africa, the majority of participants said they would seek pre-travel medical advice. One participant (506) said that “when you go to place more nasty you just be more careful” when comparing travel to Thailand versus China. This differential view in the health risks of travel destinations also applied to other countries. The general attitude was that for countries where the perceived travel risk is low, including both China and Western countries, travel health preparation is not necessary. Again, familiarity also played a role.

Like, if you’re going to Europe or America, then maybe not really necessary, ’cause you know it’s more developed. But if you’re going to like India, then you know that’s different. (Participant 501)

It’s just like, some countries like Thailand or India, it’s just places we’re not familiar with. (Participant 502)

3.4.3 Preparing for travel to China

Consultation of medical professionals

None of the participants reported consulting a medical professional before any of their trips to China. However, some participants said they were open to seeking pre-travel medical advice before going to China after long-term immigration to Australia.

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I think if once settled in Australia probably yes, ’cause I see in this group most of us have been in Australia for like 2 years, which is a pretty short time, and the health awareness is not that strong compared with those Australians. I think after 10 years we live in Australia, probably the health awareness will be rise … if you get a job, I think the job will, the organisation will grant you some health insurance, and some other stuff, and you will get used to a GP regularly. But for us international students, we stay here for studying and we go back home regularly. And again, as she said, it’s our hometown, we don’t really care, or that awareness is not that strong as your case. (Participant 505)

None of the participants were aware of travel medicine specialists or specialist travel health clinics. When informed of their existence, none of the participants expressed an inclination to consider using them for their next trip to China. Some participants were, however, open to using such a service for travel to other countries such as India.

The cost of seeing a doctor was also a factor in not seeking medical advice. One participant said they would not consider seeing the GP due to cost, but when asked if they would see the GP if it was free, this participant (408) changed their view and would ‘maybe’ consider a pre-travel health visit. Another participant (505) said that they may see a GP prior to returning to China if they lived in Australia for a long time, because they would have health insurance through their job which would encourage them to see a GP regularly.

There was also a concern that doctors in Australia may not know the situation in China very well.

I don’t think the doctor in Australia knows more than me. (Participant 504)

Health information sources

The majority of participants instead relied on health information from other sources, particularly family and friends in China and the internet. Familiarity was again an important reason why participants did not seek professional pre-travel medical advice.

I’m just going home. (Participant 405)

We know this place well. (Participant 408)

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You grew up in China and you’re familiar with all the environment, and you can adapt to changing circumstances. So you don’t feel unsafe because you grew up there. (Participant 508)

The internet was a particularly common source of information for participants. Participants described their use of social media in China, including Weibo (the Chinese version of Twitter), and online Chinese news websites to source information. Google and Facebook were also mentioned. The internet was used both for searching for information and for communicating with family and friends in China about their need for specific preparations prior to travel.

I think the first source is the internet, ’cause information is shared through the internet, and everyone go to internet and we can talk with friends and talk about what they think about if we go back to China. (Participant 502)

Official and unofficial sources were both used and some participants expressed distrust of government sources to provide all the relevant infectious disease information.

There are also some articles released on the social websites, so you can also check, and some are officially authorised and some are not, so you have a variety sources there, and you can make a judgement on that and make your decision. (Participant 502)

Usually I will check my relatives’ advice, and local news, because sometimes the Chinese authority will cover some kind of disease or flu cases there, so you’re gonna have some news from your relative as a reference. (Participant 506)

Family and friends in China are also major sources of information. Relatives may even provide unsolicited advice, including influencing changes to travel plans in the event of infectious disease outbreaks.

I think I will rely on my family and friends and news more than Australian clinics. (Participant 403)

It’s easy for us to get access to our families and friends, so we don’t bother to book, to make a reservation. (Participant 411, regarding why they preferred to obtain information from family and friends rather than a medical consultation)

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I don’t really seek advice on purpose but some of my relative would tell me that there’s some flu in Hong Kong, and they would try to persuade me tell me not to go back to Hong Kong for quite a few months. (Participant 511)

Vaccination

General attitudes towards vaccination As with participants in community focus groups, students’ willingness to be vaccinated depends on their perceived risk of acquiring the disease, and how they perceive the seriousness of the disease. Cost was also an important factor.

I’m not going to have the vaccine, since I think that you may not have the chance to take that disease even though you don’t have that vaccine. (Participant 402, on the human papillomavirus [HPV] vaccine)

I’m thinking about having that vaccine back in Hong Kong because as a university student you get some kind of discount. (Participant 404)

Efficacy of the vaccine was a major concern for many participants. Furthermore, a good experience with efficacy seemed to increase confidence in a vaccine.

Actually that’s the main concern about taking HPV or not. Side effects and whether or not they’re effective. (Participant 505, about the HPV vaccine. After being told that efficacy was 70%, she said that “it’s not high enough”.)

It will protect you in some way. Because after I took the flu vaccine I rarely had any flu. (Participant 503, in relation to the annual influenza vaccine)

Some participants described obtaining information from a wide range of sources before deciding whether to have a vaccine. In relation to getting the HPV vaccine, one participant (411) said that she visited government websites, Yahoo Answers, ‘Googled’ information and asked friends who were studying medicine before making a decision to get the vaccine. She expressed a need to know how the vaccine works as well as the side effects. She also said that her doctor did not mention any side effects, and she only learned about the side effects from her own research.

Many participants reported that they were up to date with their childhood vaccinations as mandated by the Chinese government. Some participants were unsure or had no records, while one participant

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(504) said they did not complete their childhood vaccinations “because I moved from one city to another so I missed some”.

Many participants were concerned about the side effects and safety of vaccines. Some participants were particularly concerned about safety after they heard of cases of adverse reactions.

There was one person in Shanghai got the vaccine, and because he is allergic to it, he died. (Participant 405, on why their parents did not want them to have a vaccine)

Two participants were concerned that vaccines safe for people of European descent may not be as safe for Asians. However, many others said they did not share the same concern.

I’m always having this concern that the vaccination in Australia are better for Western people’s body condition rather than for our Asian bodies. (Participant 407)

As with the community focus group participants, some international students felt that they were not well informed about vaccines in general. There was also confusion over how long vaccines are effective for.

I would think that for general citizens we lack proper information about the exact vaccination we are getting. (Participant 407)

Sometimes we are confused because some vaccines are once and for all, but some are short term. (Participant 506)

Vaccinations and travel Participants were open to the idea of receiving vaccines prior to travel to China if recommended by their doctor.

I think I would take it no matter the cost, for precaution. (Participant 509)

Some participants said they still would not accept the vaccine, while others said the decision would depend on a number of factors, for example, if there was a current outbreak, the prevalence of the disease, the seriousness of the disease, and potential side effects and safety. One participant (403) said they would still prefer to rely on their family and friends for vaccine advice prior to travel. Furthermore, two participants (407, 408) said they believed Australian GPs may overestimate the risk and the need for vaccination.

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They may think we’re pretty fragile but I think I am really tough. We’re from this land. We’ve adjusted to this land anyhow, like we’ve survived by their food, we survived by the air, so my body will just adjust to the environment. (Participant 407)

But I don’t think we’re so tough, at least I don’t think I am, but I think the Australian doctors may be overestimating the risk. (Participant 408)

Issues during travel

3.4.4 Travel activities and itineraries

As with participants in the community focus groups, international students described involvement in a variety of activities with family and friends during their return trips to China. These included eating outside the home and visiting rural areas or other parts of China with family and friends.

Students commonly reported timing their return trips to China during the Australian university summer holidays (December/January), which coincides with the Spring Festival in China.

Usually when we’re going back to China from December to February, we usually have Spring festival dinner with families, so that’s our usual activity. (Participant 506)

3.4.5 Particular health concerns during travel

Respiratory infections

Compared with community focus group participants, international students appeared to be less concerned about respiratory infections, apart from outbreaks of severe diseases such as SARS and avian influenza. Respiratory infections and their risks were not a major point of discussion in either international student focus group.

Although the focus of this study was infectious disease risk, it is again worth noting that air quality was a major concern for some participants.

At the end of last year, there was a really strong mist and dust mixed together in Beijing, and during that time I had an internship in Beijing, so I had to go out every day. And then every day when I went back home there are black stuff in my

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nose. I had to wash my face, and then brush my teeth blah blah blah, and then wash my hands regularly, ’cause that’s just really strong. (Participant 407)

Food safety

Many participants identified food safety as a potential issue of concern and it was the “biggest concern” for several participants. As with community focus group participants, food safety concerns of many students included both infectious (e.g. ‘food poisoning’ and hepatitis A) and non-infectious (e.g. carcinogenic substances in food) causes. Non-infectious causes were reportedly of more concern for many participants, whereas concerns regarding the risk of infectious diseases were limited to street food. As with participants in community focus groups, students were divided over whether it is safe to eat street food in China. Some participants said they would eat street food, while others said they would not. Some participants limited their exposure to street food but still ate it infrequently. One participant (505) said they would eat street food in Hong Kong, but not mainland China. Others reported experiencing diarrhoea after eating street food, but were not concerned.

I think just once, it won’t really seriously get injured, so why not try. (Participant 509)

One participant (507) thought that Chinese international students had higher immunity against food poisoning in China, compared to Australian travellers. Another participant (405) was specifically concerned about hepatitis A. However, several other participants said they were not concerned.

I think every kind of food, including street food and restaurant food. I think I’m currently worried about any types of food in China. (Participant 401)

A few years ago we went to China. All of us were fine but some Australians were sick. That’s the difference between the people. (Participant 507)

Friends may also be part of the decision to eat street food, something not previously mentioned in the community focus groups.

If I’m happy and my friends are all very passionate about the street food, yes we’d go ahead and we’d buy some sticks to eat and something, but we would not do that regularly because we’re uncertain about the safety issue there. Maybe try once, twice per month is okay. (Participant 508)

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Recycled or unhealthy oil, toxins in food grown in China, such as chickens that were inappropriately fed antibiotics and vegetables with unsafe fertilisers and pesticides, were the main non-infectious concerns regarding food safety reported by participants. Participants also noted that many of these concerns applied even to groceries purchased for home cooking.

Travelling when sick

Worryingly, some participants said they would travel on a plane between Australia and China even when sick. Some participants also said they would not necessarily see a doctor before travelling.

If it’s a deadly disease I won’t board the plane, but if just a cold then it’s like normal. (Participant 504)

3.4.6 General healthcare-seeking behaviours and the use of medicines

Chinese medicine

There were many similarities in the use of and attitude towards traditional Chinese medicine to that found in the community focus groups, with use reported by some but not all participants. The general belief that Western medicine was better for treating acute illnesses while Chinese medicine was useful for chronic conditions was also held by the international student focus group participants.

It’s like for Chinese doctors, they’re trying to adjust your body from the head to the bottom, but for Western it’s like you’re sick you eat this and you’re alright, it’s just like quick transformation but not thoroughly changing. (Participant 407)

As in the community focus groups, some participants believed that Chinese medicine was safer, while other participants disputed this. Some participants reported a higher likelihood of using Chinese medicine in China as it was more readily available there. Interestingly, one participant felt that Chinese medicine was more effective when used in China.

When I’m in Shanghai I take some traditional medicine I feel alive, but when I get a flu here I take the medicine, it doesn’t work. What I do is I take Panadol, and I’m alright now. (Participant 405)

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Self-medication

Similar to the community focus group participants, many students reported self-medicating for what they perceived to be minor illnesses. Participants had misconceptions about medications when self- medicating. For example, one participant thought she should take a reduced dose for some medicines because she was Asian, young and female:

It’s like one pill for adult, and my friends would tell me that for Asian girls just over 18 you just have half a pill every day. So it’s like I automatically reduce the amount. (Participant 407)

As in the community focus groups, some participants said they would purchase medicines, including both Chinese and Western medicine, in China and bring them to Australia to use. Again, there were participants who purchased antibiotics in China and brought them to Australia for use if required.

Comparative health care in Australia and China

Participants had mixed views regarding their preference for seeking health care in Australia compared with China, similar to the community focus group participants. When issues of the quality of health care in China compared with in Australia were discussed, participants again had mixed views. The language barrier in Australia, being with family, and knowing where to find good doctors were all factors participants mentioned for preferring health care in China. As in the community focus groups, many participants also complained that accessing health care was not convenient in Australia, resulting in some waiting to seek treatment in China.

Sometimes you have to wait a long time here, because one of my friends, he’s having some kind of surgery and he’s considering having it here, but the doctor said the machine only works for four or five people one week, so he’ll have to book and he is going to have to wait two more months, so he’d rather go back to China to have that surgery. (Participant 409)

However, other participants gave reasons for preferring health care in Australia. One participant (411) found the Australian system of booking doctors’ appointments convenient. Participants also mentioned serious problems with the Chinese healthcare system.

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If you don’t know anyone in the hospital, they will tell you that there is no bed for you after 3 months, even if you have a very serious broken leg, they won’t give you bed. (Participant 405)

In China, if you want to get percentage of the insurance of the doctor you have to give them something, red pocket. (Participant 509)

Cost is another factor in participants’ preference for seeking health care in Australia or in China. Participants in the international student focus groups generally had government healthcare coverage in China but not in Australia, but they had varying levels of private health insurance in Australia too.

If it doesn’t cost me anything here, my insurance cover, I will see the doctor here. But if I have to pay the money, I’ll definitely go back. (Participant 507)

Some participants said they went to China for their annual check-ups. One participant said they would go to China to see the dentist for elective dental work if time allowed, because it is cheaper there. Going to China to see the dentist was also raised in the community focus groups.

3.5 Discussion

3.5.1 Overview

This study identified that international student participants shared many attitudes and risk perceptions with other Chinese VFR travellers. The most important of these is the common underestimation of the risk of VFR travel, unwillingness to seek pre-travel medical advice, lack of awareness of professional travel health clinics, and hesitancy and knowledge deficits regarding vaccination. Participants from both studies said they may seek elective health care in China, particularly dental procedures. The participants had mixed views on their willingness to get vaccinated for travel, and on subjects like street food consumption, the use of masks, and health care in China versus Australia. The mix of views expressed on these topics largely mirror the mix of views found in the community focus groups. Also similar to the community groups, participants commonly used traditional Chinese medicine and generally believed that it was better than Western medicine for chronic conditions. This shows the use of Chinese medicine is common, even among younger Chinese people.

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3.5.2 Strong feeling of China as ‘home’

Many international student participants expressed a strong feeling of China as their ‘home’. This may be because many international students have not made a decision to permanently emigrate to Australia, and they often have family in China but not necessarily in Australia. Many of the Chinese VFR travellers in the community focus groups believed that they do not need to seek pre-travel health advice because they are familiar with China, but this strong expression of China being ‘home’ was unique to the international student participants in this study. This means that international students may not think of VFR travel to China as ‘travel’, but rather just ‘returning home’ and hence do not identify the need to seek medical advice before return visits. Not seeking pre-travel health advice due to not identifying the need to do so has been reported to be common in other studies of VFR travellers (25, 52). It has also been reported that some VFR travellers believe that being born in the destination country is a good enough reason not to seek pre-travel advice (25, 63), and some VFR travellers have never even considered seeking such advice (33, 52). This must be taken into account when designing education material targeting international students. Chinese international students should be educated regarding their extra responsibility to protect themselves from infection, as well as the fact that they study on a campus with thousands of other students and can potentially become the index case for an outbreak on campus (74, 77, 78).

As participants feel a strong familiarity with China, having lived there, some believe that Australian health professionals are not as familiar with China as they are. This is a further reason not to consult a health professional in Australia before VFR travel to China. This will be further explored below.

3.5.3 Low risk perception and low awareness of changed immunity

As the participants are international students from China, they (and their family and friends) have lived in China for long periods of time. Because they may have done so without encountering severe infectious diseases, they generally believe that travel to China does not pose much risk for acquiring severe infections. This attitude is common to both Chinese international students and other Chinese VFR travellers, as reported in Chapter 2 and also confirmed by other studies (24, 25, 33).

As mentioned previously, a survey study among UNSW Australia students in 2010 found that international students were less likely than other students to practice preventive travel health measures (71). Of the international respondents in the survey, 52.2% selected “visit friends, relatives or return home” as the reason for travel, providing further evidence that international

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students who travel for VFR purposes often undertake inadequate preparations. As with the community focus group participants, low risk perception was a major factor in international students not seeking pre-travel health advice or undertaking adequate preparation for travel. Correcting this low risk perception is important for encouraging adequate pre-travel health preparations. As discussed in Chapter 2, according to the Health Belief Model, perceived susceptibility to and perceived severity of disease, which can be combined into the concept of perceived threat of disease, is an important motivator for health-seeking activity (146, 149, 213). Perception of being at risk has been correlated with preventive and risk reduction activity in multiple areas of health care, including vaccination (215, 217, 253).

Finally, the international students in this study lacked awareness of possible changes in their immunity to certain diseases since leaving China. This was evidenced by their attitudes to the different risks in acquiring food-borne infections between Chinese and Australian travellers to China. As mentioned in Chapter 2, ‘changed immunity’ to gastrointestinal infections is possible, and VFR travellers should therefore be more cautious than locals regarding food safety. In contrast with some of the participants in the community focus groups, changed immunity was not a consideration at all for international students. This was unsurprising, as these participants have lived in Australia for shorter periods of time than the community participants. Awareness-raising and education on this topic among Chinese international students, and perhaps other recent immigrants, is clearly needed.

3.5.4 Use of internet and social media

The use of the internet in pre-travel preparations was more extensive among the international student participants in this study than among the older community participants. This is consistent with a previous study on US student travellers, in which use of the internet as a source of travel health information was commonly reported (254). Although some participants of the community focus groups used the internet to get information as part of their pre-travel preparations, for example, from news websites, international student group participants reported more extensive usage of the internet. Student participants reported searching extensively for information on the internet, including information and opinions on vaccination, and the use of both official and unofficial sources of information. The participants reported also using the internet for communicating with family and friends in China. The use of social media in particular was commonly reported by student participants. The finding that university student VFR travellers were more likely than other VFR travellers to use the internet and social media to seek information is

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supported by feedback from a public health education initiative for international students regarding VFR travel health in Victoria, Australia. The report on this initiative states that “informal feedback from interested personnel in agencies” identified electronic and social media as a preferred way of disseminating health information (68). The internet and social media are therefore potentially very effective avenues for raising awareness of VFR travel-related health risks and promoting proper pre-travel health preparations among international students.

3.5.5 Reliance on parental advice

Most international student participants unsurprisingly had family, including parents, in China. Many reported that their parents provided advice regarding both health issues in general as well as travel health-related issues. For example, one participant’s parents advised them not to have a vaccine due to a case of adverse reaction reported in China. Family and friends as a major source of advice among student travellers has been previously reported in the literature. A US study of student travellers found that family and friends are a common source of advice (254). Reliance on advice from family may be an important reason for not seeking professional travel health advice. A study of Australian travellers found that ‘country of origin or staying with family’ and ‘advised by friends or others it was safe’ were commonly reported reasons for not seeking professional pre-travel health advice (63).

It appears that advice from relatives may be both helpful, for example, advice about current outbreaks in China, and counterproductive, for example, advice not to take a vaccine based on unjustified reasons. It is notable that a study on Hong Kong university student travellers found that those who received non-professional travel advice were more than twice as likely to experience travel-related illness compared to those who received professional advice (69).

3.5.6 Significant misconceptions still to be addressed

Generally speaking, the international student participants in this study appeared to be better informed and more willing to gather information about various issues than the community participants. This may be because of their higher level of education and extensive use of the internet. However, some still have significant misconceptions regarding various issues. For example, one participant thought it was appropriate for her to take half the normal dosage of some medications because she was a young Asian female, and another participant thought that vaccines in Australia are more suitable for “Western bodies”. There is a danger that some students may think they are very well informed and do not need to seek extra advice, when they actually have

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important misconceptions that may adversely affect their decisions and behaviour. When combined with the low risk perception discussed above, it means that health messages regarding the risks of VFR travel must be proactively disseminated to this population, for example, via university publications or social media.

International student participants were generally not keen on receiving vaccinations for VFR travel. This may be related to Chinese culture generally, as it is known that the uptake of annual influenza vaccination is lower in China than in Western countries (235). However, the concept of vaccination itself should be familiar to young adult Chinese students, as China has a comprehensive national vaccination program that covers BCG, tetanus, diphtheria and pertussis, hepatitis A and B, Japanese encephalitis, measles, mumps and rubella, meningococcal A and C, and polio (143).

Many participants were very concerned about the safety and side effects of vaccines. This lack of confidence in vaccine safety is likely to be another important reason for the reluctance to receive vaccinations. A study conducted on university students in Turkey regarding 2009 H1N1 influenza vaccination found that “it is not safe” and “I don’t trust it” were the leading reasons for not accepting vaccination (255). As the international student participants were more well informed in general and more willing to search for information using the internet than community participants, recent media reports of controversies over vaccine safety in China (236-238) are more likely to have had a stronger impact on this population. Previous studies have found that among young adult students, acceptance of various vaccinations was more common for participants who were more well informed (256-258). This study also found, consistent with several other studies, that many university students seriously consider the costs and benefits of vaccination when deciding whether to have a vaccine (259, 260). Therefore, education material that corrects common misconceptions and outlines the specific benefits of each vaccination may be useful for improving vaccination acceptance rates in this population.

There also appears to be a lack of awareness among international students of the utility of consulting a health professional before VFR travel. Although participants generally agreed that consulting a health professional before travel to China was not necessary, some participants also identified that they had knowledge gaps and questions regarding vaccinations. Awareness that a GP, for example, can suitably address these questions may encourage more travellers to visit their GP before VFR travel. International students need to be educated regarding the wide range of advice Australian GPs and travel health clinics can give.

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3.5.7 Barriers to accessing health care in Australia

One participant in this study mentioned that if they have lived in Australia for more than 10 years in the future, they may be more likely to seek pre-travel health advice. An increased willingness to undertake travel health preparations after longer term migration has also been reported in a quantitative study of South Asian VFR travellers in Canada. That study reported that 58% of respondents who had lived in Canada for more than 20 years used malaria chemoprophylaxis during VFR travel, compared to only 22% of respondents who had lived there for a shorter period (24). This demonstrates the necessity of encouraging more recent migrants, including international students, to seek pre-travel advice for VFR travel. In this study, the aforementioned participant stated increased health awareness, having a regular GP and having health insurance coverage as potential reasons why longer term migrants are more likely to seek pre-travel health advice. Therefore, low risk awareness, not having a regular GP and inadequate health insurance coverage are potentially important barriers for more recent migrants and international students that need to be addressed. As many international students are recent arrivals in Australia and may not have a regular GP, provision of travel health advice and vaccinations at the university clinic would potentially greatly improve access for some international students. Studies regarding vaccinations and students have previously found an association between access to health services and vaccination rates (256, 261).

As international students, the participants were not covered by Australia’s Medicare and Pharmaceutical Benefits Scheme (PBS) systems. They instead have compulsory private health insurance coverage (known as ‘Overseas Student Health Cover’), with some services mandated to be covered by the Australian government, and additional coverage available at extra cost (262). In the basic package, vaccinations are not covered, and there is only limited coverage of pharmaceuticals (262). For the participants in this study, cost appears to be an important factor in their decisions regarding whether to obtain vaccinations or services for which they have no insurance coverage. The cost factor may affect students’ decisions to seek professional health advice before travelling, whether to use a professional travel health clinic, whether to have a vaccine, and even whether to delay seeking treatment until they are in China.

Another important barrier identified in this study was the view that Australian doctors are not as familiar with China as the students are, and thus do not understand the students’ health needs regarding travel to China. A Spanish qualitative study which explored travel health issues in Latin American and African VFR travellers also identified that participants viewed Spanish health

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professionals as having “poor capabilities to treat tropical diseases” that the travellers would encounter in their home countries (65). To convince Chinese international students, and other Chinese VFR travellers, to consult Australian health professionals before VFR travel, it is necessary to demonstrate to them that these health professionals, even if they are not from China, have a strong understanding of travel health-related issues pertaining to China, and can provide health knowledge and advice that can benefit Chinese VFR travellers.

It must be ensured therefore that the health professionals they consult are indeed familiar with the health situation in China. Health professionals giving inadequate or incorrect advice further reinforces the notion that Australian healthcare workers are not familiar with China and are therefore unable to provide helpful pre-travel advice. It has been reported in the literature that health professionals may be unfamiliar with infectious risks not found in their home country, and may even give incorrect advice to their patients. A study conducted with physicians and nurses interested in travel medicine in Taiwan found that many had knowledge gaps related to travel-related illnesses including malaria, yellow fever and dengue (263). A study of Canadian South Asian VFR travellers found that in 76% of cases their GPs prescribed inappropriate malaria chemoprophylaxis regimens (24). Another study of doctors and nurses working at practices that serve higher-educational establishments in the UK found that in 23% of cases correct advice regarding immunisations for travel was not given, and that incorrect advice was especially common for some diseases including malaria (264). Encouraging the use of professional travel health clinics may reduce the risk of inadequate and incorrect advice, but even these clinics may not be free from this problem. The aforementioned Canadian study found that even for those who visited travel health clinics and public health centres, 36% received inappropriate prescriptions (24). Another study in Greece conducted among travel medicine consultants found that many such practitioners gave inadequate recommendations regarding rabies (265). A potential solution would be to provide a certification process for GPs and travel health specialists with a special interest in travel health issues regarding China, and then to recommend certified health professionals to Chinese international students and other Chinese VFR travellers for travel health consultations. Another possible solution would be for the university to establish a travel health service, with practitioners being specially trained regarding travel health issues in common travel destinations, including China.

3.5.8 Travelling to China during the influenza season

Many international student participants reported travelling to China around the time of the Spring Festival, in January to February each year. Although other Chinese VFR travellers may also choose

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this time for travelling, international students are especially likely to do so, given that it is also the time of the annual vacation for Australian universities. However, this period is also the peak period for seasonal influenza in many parts of China (266-268). Therefore, it would be particularly important for people travelling during this period to be vaccinated for seasonal influenza prior to their travel, and be aware of ways they can reduce their risk of getting influenza during their trip. One major barrier to this is that the northern hemisphere influenza vaccine is not licensed for use, and is therefore not available, in Australia (269). The WHO releases semiannual recommendations for influenza vaccine formulations, in preparation for the peak influenza seasons in the northern and the southern hemispheres respectively. The composition of annual vaccinations patients receive prior to the peak season in each hemisphere are therefore based on information only 8 months old (270). If Chinese VFR travellers travel to China in December or January and obtain influenza vaccination in Australia before they travel, they would still be receiving the southern hemisphere vaccine for the previous season. The vaccine formulation would be based on information that is more than 1 year old and less up to date than if they were immunised using the current northern hemisphere vaccine. This situation can be improved if the Australian Therapeutic Goods Administration were to license the use of the northern hemisphere vaccine for use in travellers, and suppliers are willing to supply this vaccine to Australia.

3.5.9 Specific issues to be addressed in education campaigns

Chinese international student VFR travellers appear to share a lot of common attitudes and barriers with other Chinese VFR travellers. Education campaigns targeting Chinese VFR travellers in general, such as those discussed in Chapter 2, would be applicable among Chinese international students. Promotion of travel health services and proper pre-travel health preparation, as well as education campaigns targeting food safety, proper health behaviours during outbreaks (including avoiding non-essential travel, washing hands and avoiding crowds), and correcting misconceptions associated with vaccinations appear to be just as needed among Chinese international students as among other Chinese VFR travellers. As international students often use the internet and social media for information gathering, education could be delivered to students via these channels, more so than for other Chinese VFR travellers. The use of multiple channels to deliver education interventions for Chinese VFR travellers will be further explored in Chapter 5.

Although Chinese international students would benefit from education campaigns targeted at Chinese VFR travellers in general, there are specific issues that need to be addressed among student

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VFR travellers. This means that in addition to general VFR traveller education, there needs to be specific education directed at international students, addressing these specific issues.

International students are generally not among the target groups for annual influenza vaccination, due to their age. However, as they are very likely to travel to China during the peak influenza season, Chinese international student VFR travellers should be specifically advised to undertake influenza vaccination if travelling during this period. Future education campaigns should highlight the timing of the peak influenza season in China, and the benefits of receiving such vaccination for travellers travelling to China during this period.

International students generally have not been living in Australia for a long time, and often view China as their home. This, combined with a low awareness of issues around changed immunity, may mean they severely underestimate the risks of their VFR travel, possibly even more so than other Chinese VFR travellers. Thus education campaigns around changed immunity and the associated need for proper travel health measures becomes even more important.

International students appear to often receive travel health advice from parents, some of which may be counterproductive. This may include advice to travel to China even during an outbreak, or to refuse particular vaccines. Education campaigns need to counteract such advice, for example, by putting the risk posed to individuals undertaking non-essential travel during an outbreak into proper perspective, and emphasising the safety, efficacy and necessity of vaccines.

As obtaining proper travel health advice and undertaking vaccination may be costly, especially for international students, campaigns should emphasise the benefits of such preparation, and clearly explain how it is well worth their money for an individual to take these steps.

Use of the internet to target younger VFR travellers

The extensive use of the internet to search for information and the use of social media among younger Chinese VFR travellers present a great opportunity to disseminate targeted education campaigns to this population. This could be done in multiple ways. Information could just be made available in an accessible form on the internet that could be searched for via search engines like Google, something participants from this study said they would do. There could also be campaigns to correct misconceptions in online discussions regarding various health issues (271). The use of social media is also likely to be helpful. Social media accounts (e.g. on Facebook, Twitter and Weibo) could be set up to connect with younger Chinese VFR travellers, and then disseminate information via these connections. Such information may then be further shared and disseminated

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via social media to even more potential Chinese VFR travellers (271, 272). The Australian government would have a major role to play in this area, but international health agencies like the WHO and CDC should also be involved, as some participants raised the issue of distrust of advice from governments.

There has recently been some interest in the use of social media for travel health promotion (271, 272). Use of the internet for health promotion purposes remains a new development, but early evidence from various studies is encouraging. This evidence will be discussed in Chapter 5 as part of an exploration of possible education interventions.

3.6 Conclusions

Understanding international students and their travel risk perceptions is important for the targeting of disease control initiatives in this high-risk and highly mobile population. This focus group study on issues surrounding the VFR travel of Chinese international students studying in Australia was unique in that there are currently no published qualitative studies regarding international students as VFR travellers. As such, several important issues have been newly identified or explored in further depth than in existing published literature.

The Chinese international student participants in the focus groups often strongly viewed China as their ‘home’. They therefore viewed VFR travel as ‘returning home’, which often meant they perceived pre-travel health preparations as unnecessary. Unsurprisingly, they often had low risk perceptions regarding VFR travel, and were generally unaware of issues surrounding changed immunity. They were also not confident that Australian health professionals are familiar enough with China to be helpful for their VFR travel.

Participants commonly had misconceptions regarding vaccinations, and this affected their willingness to receive vaccinations for VFR travel. In addition, they were concerned about the costs of vaccinations and services not covered by their health insurance. This is an important barrier to address. Participants also often travelled to China during the peak influenza season. Availability of the northern hemisphere influenza vaccine in Australia would be useful for this population. Participants commonly relied on health advice from their parents, some of which may be helpful, but some of which may not. This may be another reason for not seeking professional travel health advice. Students also commonly used the internet and social media to seek health advice and information, and this presents an opportunity for education interventions.

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Overall, this research has provided information on Chinese international students as VFR travellers, especially regarding areas where travel health preparation is inadequate, and identified issues that commonly apply to Chinese VFR travellers as well as issues specific to this population. This information should inform future education interventions targeted at improving the travel health outcomes of this population.

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Chapter 4 Outbreaks of infectious disease in China – literature review and focus group analysis

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4.1 Abstract

China has been the source of multiple respiratory pandemics in the last century, and it has been hypothesised that China is an epicentre for the emergence of such pandemics. Therefore, Chinese VFR travellers, who frequently travel to China are at higher risk of contracting respiratory illnesses and subsequent introduction of future outbreaks into Australia compared with tourist travellers.

This chapter includes three components: a literature review exploring the recent past experience with outbreaks and pandemics originating in China, and the potential for future pandemics originating in China; an analysis of the changes in VFR travel during the 2003 SARS pandemic; and focus group data relating to outbreak behaviour drawn from the studies described in Chapters 2 and 3. This is followed by a discussion drawing upon and combining results from all three components.

It has been hypothesised in the literature that China is likely to continue to be an important source of future pandemics, due to environmental and cultural conditions that are not easily amenable to behaviour change. Moreover, there is concern that a new pandemic strain of influenza with high pathogenicity and human-to-human transmissibility may arise in China in the near future, as there are already several strains of avian influenza that have caused human infection circulating in China. The history of the global spread of SARS highlights how international travel can facilitate the spread of a new pandemic to distant countries in a very short time frame, and the fact that SARS was introduced to Canada by a returning VFR traveller highlights the potential of such travellers as important sources of infection in countries with large Chinese migrant populations. The analysis of data from the Australian Bureau of Statistics showed that decline in VFR travel was smaller, compared with other travel, during the SARS pandemic of 2003, consistent with focus group findings that Chinese VFR travellers do not always cancel non-essential travel during outbreaks, despite WHO advice. The focus groups also found that while Chinese VFR travellers were generally aware of outbreaks in China, they often had low risk perception regarding outbreaks and pandemics, often had misconceptions about effective preventive behaviours, and practiced recommended preventive behaviours inadequately.

The fact that China is a likely source for future respiratory pandemics means that Chinese VFR travellers are a potentially important source of future importation of pandemics into Australia. This is further compounded by Chinese VFR travellers continuing to undertake non-essential travel to China during outbreaks, and their inadequate precautionary behaviours while travelling which

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further increases their risk of infection. Therefore, targeted education interventions in this population to improve risk perception, correct misconceptions and reinforce proper preventive behaviour surrounding outbreaks should be a priority, with the objective of mitigating the risk of future outbreaks for Australia.

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4.2 Introduction

Global outbreaks of several important newly emerged infections have originated in China, including historical pandemics, such as the 1957 Asian influenza and the 1968 Hong Kong influenza pandemics, and more recent outbreaks such as SARS and H5N1 and H7N9 avian influenza. It has also been hypothesised that China will continue to be an important source for similar outbreaks in the future (11). The climate and cultural conditions in southern China are believed to play an important role in this. In particular, common practices such as the consumption of exotic animals, and the Chinese wet market environment where a wide variety of animals are kept in close contact with each other, are thought to facilitate the exchange of viruses among different hosts, and thus are favourable to the emergence of new respiratory viruses (11).

International travel has always been an important facilitator of the spread of emerging infections and pandemics in human history (1). The modern situation of high volume, high frequency and rapid international travel especially favours disease emergence, re-emergence and global spread, as has been seen in a variety of diseases (1, 273-276). Of particular concern, however, is the role of travel in establishing global pandemics, potentially in very short time frames. As we have learned during previous outbreaks like SARS, international travel can cause the rapid spread of epidemics around the world, establishing a global pandemic within weeks. Modelling studies have demonstrated that, although travel restriction and quarantine measures may somewhat delay the entry of pandemic illnesses into countries, it is very difficult for any country to close its borders and completely prevent the importation of a pandemic in modern times (277-281). This has been confirmed by the experience of recent pandemics such as the 2009 H1N1 influenza pandemic (282, 283). However, as the experience of SARS has shown, there is potentially great benefit in delaying the introduction of a pandemic for as long as possible; countries which were first to receive imported cases, when they were not yet well prepared, often had some of the most severe local epidemics (3, 284). Therefore, even though the importation of pandemics can only be delayed at most, it is still important to attempt to prevent the importation of communicable diseases with epidemic potential as much as possible.

Because China is a potential source for the emergence of pandemics (11), travel to and from China may play an important role in the introduction of a future pandemic to countries like Australia. VFR travellers in particular are potentially important sources of infection for several reasons. VFR travellers account for a substantial and increasing proportion of international travel (13, 14). In 2010, 28.9% of resident departures from Australian airports to mainland China and Hong Kong was

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for visiting friends and relatives (84). VFR travellers are at greater risk of acquiring certain infectious diseases compared to other travellers (15-17). This is due to multiple factors, including residence in local family settings and prolonged close contact with the local population facilitating the spread of certain infections such as influenza; prolonged duration of travel providing more opportunities for infection; and eating habits more similar to the local population than tourist travellers. These factors have all been found in this study (see Chapters 2 and 3) and other previous studies (14, 19, 23, 24, 36). In addition, as described in Chapters 2 and 3, Chinese VFR travellers often undertake inadequate pre-travel health preparations and inadequate precautionary behaviour during their travel, which also increases their risk of acquiring infections. Furthermore, as reviewed in Chapter 1, studies have shown that residents of mainland China had low concern regarding previous outbreaks and undertook inadequate outbreak precautions (169, 170). This is of relevance to Chinese VFR travellers because, as described in Chapters 2 and 3, activities undertaken by VFR travellers in China are often strongly affected by family and friends.

Taking the above factors into account, there is a risk of Chinese VFR travellers importing pandemics originating in China into Australia and other Western countries with large Chinese migrant populations. This risk is highlighted by the introduction of SARS to Canada via a returning VFR traveller, causing the local epidemic (12, 97). The risk of VFR travel-related pandemic importation could, however, potentially be minimised if VFR travellers were aware of outbreak risks and took appropriate precautions to reduce their own risk of being infected. Such precautions may include cancelling non-essential travel and undertaking adequate preventive behaviour if already overseas, such as not consuming street food or uncooked food, avoiding live poultry markets and crowded areas, washing hands frequently, and using face masks (164, 167, 285). The promotion of adequate preventive behaviour should therefore be a major objective of any future interventions for Chinese VFR travellers.

This chapter aims to explore some of these issues by combining a literature review of respiratory outbreaks in China and focus group qualitative data obtained from the studies described in Chapters 2 and 3.

4.3 Methodology

A literature review was conducted around major outbreaks and pandemics of respiratory pathogens originating in China in the previous two decades. The important outbreaks in the previous two decades included SARS and H5N1 and H7N9 avian influenza. The Medline database was used to

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retrieve published literature on each of the above outbreaks in relation to China, using a combination of keywords and MeSH headings of ‘SARS’, ‘H5N1’ or ‘H7N9’, combined with ‘China’ or ‘Hong Kong’. Articles were assessed using their titles and abstracts and selected for possible inclusion based on their relevance. At the time of the literature search, influenza A H7N9 was newly emerged and was only known to have caused outbreaks in China. Therefore, the search strategy applied no restriction to China as a search term. As this is a review specifically on outbreak risks, articles providing an overview of each outbreak, articles discussing the global spread of each outbreak, and articles discussing potential future outbreaks in China or Hong Kong were considered for inclusion; other articles, such as those discussing individual case studies or series of cases presenting to hospitals, or clinical management, were excluded. Articles listed on Medline as of 31 August 2015 were included. Studies were restricted to the English language. Reference lists of all relevant articles, including reviews, were reviewed to identify additional studies. Because the statistics quoted in individual studies may not be up to date, quantitative data provided by the WHO regarding SARS, H5N1 and H7N9 were used in this review to provide a more accurate quantitative description of each outbreak. Grey literature was not otherwise reviewed, as the focus was on articles describing infectious risks rather than the quantitative surveillance data which forms the bulk of grey literature in this area.

Focus groups were conducted among Chinese VFR travellers in the community and Chinese international students studying in Australia, as described in Chapters 2 and 3, respectively. For the community groups, participants were ethnic Chinese Australians living in Sydney, aged 18 years or older, who had travelled to mainland China or Hong Kong for the purpose of visiting friends or relatives in the previous 18 months. They were recruited via Chinese newspaper advertisements, shopfront advertisements, street recruiting and snowball sampling. For the student groups, participants were ethnic Chinese international students enrolled at UNSW Australia aged 18 years or older, who had returned to mainland China or Hong Kong for the purpose of visiting friends or relatives in the previous 18 months. They were recruited via poster advertisements, advertisements on selected university publications and websites, and invitations distributed by the Heads of School in various Faculties, the UNSW Chinese Student Association and the UNSW Hong Kong Student Association.

Focus groups were conducted mainly in English, but Cantonese and Mandarin were also used when required. A focus group guide, derived from both the broader literature review in Chapter 1 and the literature review in this chapter, was used for all groups. Focus group discussions were recorded

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and then transcribed manually by two transcribers fluent in Mandarin and/or Cantonese. Conversation in Cantonese or Mandarin was directly translated into English during the transcription. Random sections of the transcripts were checked for accuracy by a third transcriber. Thematic analysis was then conducted on the transcripts. The data were encoded into a structure of codes, with each code representing a theme or an idea. Coding was conducted using nVivo 10 software. The coding process is described in detail in Chapter 2. Coded data were then analysed and summarised.

The qualitative results relating to outbreaks from the focus groups are explored in depth in the results section of this chapter, specifically results regarding general awareness and attitudes towards outbreaks and pandemics, travelling during outbreaks, and outbreak-related preventive behaviour, including the use of face masks. These results are then analysed in combination with findings from the literature review in the discussion section of this chapter.

The literature review on outbreak risks was further supplemented by an analysis of VFR travel during the SARS pandemic of 2003, compared to travel for other purposes. This analysis was conducted after the focus groups, in light of several participants stating that they did not cancel non- essential travel during a previous outbreak or pandemic, or would not do so for a hypothetical future outbreak. The analysis was conducted using freely available quantitative data provided by the Australian Bureau of Statistics, regarding overseas arrivals and departures data by purpose of travel during 2002 and 2003 (286).

4.4 Results

4.4.1 Findings from the literature

Risk of emerging infections in China

Southern China has historically been the origin of many new respiratory infections such as the 1957 Asian flu, the 1968 Hong Kong flu and, more recently, SARS, and H5N1 and H7N9 avian influenza. It has been hypothesised that southern China may be an epicentre for the emergence of new, pandemic-causing influenza viruses in future (11, 98, 99). There are various reasons for this. Various farming practices and food preferences in Chinese culture potentially encourage the mixing of human and animal viruses, and the development and spread of new strains of influenza and other viruses (11, 98, 99). In particular, farming practices like duck farming on flooded rice fields close to where humans live, causing long-term close proximity of humans and livestock, and the sale and

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consumption of exotic meats like snakes and civet cats, which may be potential hosts and sources of a range of emergent infections, are of major concern. Furthermore, Chinese wet markets catering for the Chinese preference for fresh food, where live poultry as well as the aforementioned exotic meats are kept and sold, provide an environment conducive to transmission of viruses between different species of animals (11). Although various levels of government in both mainland China and Hong Kong have attempted to change these practices, such as requiring wet markets to undergo regular vigorous disinfection and regular closure to mitigate risks (287, 288), these measures have not been completely effective in making wet markets risk-free. For example, the Hong Kong government has ordered that certain animals including ducks, quail and geese be excluded from wet markets, and that all markets be simultaneously emptied and cleaned twice a month. However, even this has not been effective in keeping H5N1 out of wet markets, as the virus was repeatedly detected in the markets even after the new regulations were imposed (288, 289). On the other hand, more radical changes, such as banning the sale of live poultry altogether, as practiced in Beijing, has resulted in the continuation of the illegal live poultry trade there (290). It is clear that these are long- held cultural practices which are difficult to change, as they are deeply embedded in Chinese history and culture (11).

Lessons from the SARS pandemic

SARS (Severe Acute Respiratory Syndrome) is a viral respiratory illness that caused a worldwide pandemic with significant mortality during 2003 (2). It is caused by a coronavirus, SARS-CoV, which most likely originated in an animal host (291). As a similar virus was isolated in civet cats in wet markets in Guangdong province during the pandemic, Chinese wet markets are likely to have played an important role in the chain of events resulting in transmission of the virus to humans (292). During the SARS pandemic, the WHO recommended postponing all non-essential travel to multiple provinces of mainland China, Taiwan and Hong Kong (293).

The SARS virus originated from Guangdong province in southern China around November 2002 (2). Until February 2003, cases of SARS were limited to mainland China. In February 2003, a physician who was infected with the virus travelled from Guangdong province to Hong Kong to visit family (294), and stayed at ‘Hotel M’ in Kowloon, Hong Kong. During his stay in the hotel, 10 other guests were infected, and subsequently spread the virus around the world by air travel. Of the 10 infected guests, 3 travelled to Singapore, 2 travelled to Canada, and 1 travelled to each of the United States, Ireland and Vietnam (2). The infected guests who travelled to Vietnam, Singapore and Canada then spread the infection in their own countries, resulting in significant local epidemics

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in all three places (3). The guests who travelled to Singapore and Vietnam were also later related to cases in Bangkok and Germany, respectively, again facilitated by air travel. Two of the infected guests and the index case were admitted to hospitals in Hong Kong, where they infected numerous healthcare workers who then spread the infection nosocomially; the index case also infected two of his family members. The epidemic thus started in the wider community in Hong Kong (294). This whole sequence of events shows the power of air travel in facilitating the rapid spread of new pandemics. Of particular note, the index case for the SARS epidemic in Canada was a returned VFR traveller, who transmitted the infection to a family member, who in turn was admitted to hospital and caused a large nosocomial outbreak (12, 97). This highlights the potential of Chinese VFR travellers as sources of infection in pandemics originating in China, in countries where there are large Chinese migrant populations.

Beyond the initial spread from Hong Kong, air travel continued to be pivotal in the spread of the SARS virus around the world. In the first few weeks of the epidemic, the majority of the suspected cases in the USA were in travellers who travelled to Hong Kong, Guangdong province, Hanoi or Singapore (294). The first case of SARS in Taiwan was found in a man who travelled to Guangdong and Hong Kong, and there was also a late second outbreak of SARS after an infected Hong Kong resident visited Taiwan (295). From these examples we can see the importance of travellers from affected countries in the initial introduction of an epidemic into new countries.

One phenomenon that remains not well understood is the role of ‘super-spreading’ events in the SARS pandemic. Super-spreading refers to cases where one individual disproportionately infects many more individuals than expected. For example, one of the initial cases admitted to a Hong Kong hospital resulted in the infection of more than 100 people. It has been estimated by mathematical modelling that 70% of SARS cases in Hong Kong may in fact have resulted from super-spreading events (296). Although this phenomenon remains quite a mystery, it means that, as occurred with SARS, it may be possible in future for a single imported case of an emergent infection to potentially cause an explosive epidemic.

In summary:

SARS originated in mainland China in late 2002

In Feb 2003, a physician who was infected stayed at a hotel in Hong Kong, infecting other guests who travelled to Singapore, Canada, United States, Ireland and Vietnam, spreading the

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infection globally

Severe local epidemics were soon established in Hong Kong, Singapore, Canada and Vietnam

Further spread of the pandemic to other countries from both mainland China and other places with established pandemics then occurred, again facilitated by air travel

By the time the SARS epidemic had been contained, there were a total of 8098 cases globally including 774 deaths. Mainland China and Hong Kong accounted for 87% of the cases and 84% of the deaths (291). As with many other newly emerged pathogens, at the time of the outbreak a lot was unknown about the properties of the virus, which hampered the development of effective prevention measures (297). Therefore, the countries where SARS was imported relatively early in the pandemic often had very significant local epidemics. Canada, Singapore and Vietnam were the three countries with the highest number of probable cases outside China (284).

Ongoing threat of avian influenza

All four influenza pandemics of the last century (i.e. the 1918 H1N1 ‘Spanish influenza’, the 1957 H2N2 ‘Asian influenza’, the 1968 H3N2 ‘Hong Kong influenza’ and the 2009 H1N1 ‘swine flu’) were caused by an antigenically novel influenza strain derived from an animal source (298). Because mammalian influenza viruses are believed to have evolved from avian influenza viruses, avian influenza viruses are particularly likely sources of such pandemics (299). Recently, the H5N1, H7N9, H9N2 and other subtypes of avian-origin influenza viruses have emerged as human pathogens in various locations around the world. This has caused concern that a new, highly pathogenic and human-to-human transmissible strain will emerge, and possibly cause a pandemic in the near future (299).

H5N1 Of all the avian influenza viruses that have recently infected humans, the H5N1 subtype of the highly pathogenic avian influenza virus (HPAI H5N1) has caused the most concern, because it has infected humans in multiple outbreaks around the world, with a high mortality rate. In the period from 2003 to 17 July 2015, there were 844 cases of infection across the world, including 52 from China, and 449 deaths across the world, including 31 from China (300). The crude mortality rate is around 60%, and the mortality rate reaches above 70% in patients aged 10–39 years (301).

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The HPAI H5N1 virus seems to have originated from southern China. It was first isolated from geese in Guangdong province, southern China, in 1996 (302). The first known case of H5N1 infecting humans was found in Hong Kong in 1997, where there was subsequently a small outbreak. Since then, there have been outbreaks in multiple countries in Southeast Asia and in mainland China, and further outbreaks in Hong Kong. This virus is not capable of human-to-human spread presently; infection is usually passed directly from birds to humans (299). A pandemic of HPAI H5N1 has therefore not occurred as yet. However, further genetic reassortment of the virus with human viruses in another animal host, for example, pigs, could lead to the virus becoming capable of human-to-human spread and a pandemic may occur (100). As HPAI H5N1 has a high mortality rate, such a pandemic may cause many deaths around the world as well as great economic catastrophe (299).

Since 1999, HPAI H5N1 has been consistently isolated from animals in southern China, and has undergone extensive genetic reassortment (303). It is now considered endemic in poultry in southern China (303). Although originating in southern China, the virus has since spread to other parts of China, and has caused both avian and human outbreaks in multiple provinces of China and other countries in the region (302, 304). The Chinese government recognises the threat posed by H5N1 avian influenza and has concrete plans and measures to deal with outbreaks (304), as well as a continued culling and vaccination strategy to reduce outbreaks in poultry (302).

Live poultry markets were a likely source of the 1997 H5N1 outbreak in Hong Kong. More recently, H5N1 viruses were isolated from live poultry markets associated with cases of human infection in Beijing and in the provinces of Guizhou, Hunan and Xinjiang This suggests a continuing link between live poultry markets and cases of human infection (305). As with SARS, this again highlights the importance of Chinese wet markets as a potential source of transmission of newly emerged pathogens to humans, and also the importance of dealing with the issue of visiting wet markets during travel in Chinese VFR travellers.

H7N9 A human outbreak of avian influenza A subtype H7N9 was first reported in Eastern China in February 2013 and, as of 9 March 2015, 611 cases had been reported in multiple provinces throughout mainland China, and 13 cases in Hong Kong (306). Sustained human-to-human transmission of H7N9 has not been documented, but, because H7 viruses have tendencies towards genetic promiscuity (307), efficient human-to-human transmission through further mutations or reassortment is a possibility (308). In addition, H7N9 appears to be more transmissible to humans

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than H5N1 (309). The rate of H7N9 spread is higher than for H5N1, with a different epidemiologic pattern, and almost as many H7N9 cases have occurred in the first 2 years as have occurred over a decade for H5N1 (285, 289). H7N9 has a high case-fatality rate, estimated at 22% based on data up to January 2014 (310). The majority of known cases and deaths have been in older adults with underlying medical conditions, whose median age was approximately 60 years, the majority of whom were male (289, 311, 312). However, there have been reports of cases in children: one asymptomatic child in Beijing who tested positive for H7N9 (308), and two children aged under 5 years with mild symptoms (311). Therefore, it is not yet known if H7N9 is more severe in certain subpopulations, nor the extent of asymptomatic infection in the wider population. Also, although in most cases there was known animal contact, human-to-human transmission could not be ruled out in a small number of cases (313). To date, there have been no known cases involving VFR travellers. However, as there have been ongoing reports of cases in China, travellers to China, including Chinese VFR travellers, remain a potential source for the transmission of H7N9 to other countries. In October 2013, Chinese scientists announced that they had developed a vaccine for the new virus (314). However, the vaccine is not currently available for use by the general population.

Other avian influenza viruses There have been cases of human infection with avian influenza subtype H9N2 reported in Hong Kong. There have only been a few cases and none have been fatal (315). In addition, there have been reports of H10N8 human infections in China recently (316). Since the H5N1, H7N9, H9N2 and H10N8 viruses have all been able to infect humans directly, it must now be assumed that all subtypes of influenza viruses, including H1–15 and N1–9, have the potential to become a new pandemic strain (100). This new view of pandemic influenza means that there is now a much larger pool of precursor influenza viruses that may trigger a pandemic.

4.4.2 Changes in the volume of VFR travel during the SARS pandemic

In response to the SARS outbreak in China, the WHO recommended postponing all non-essential travel to multiple provinces of mainland China, Taiwan and Hong Kong (293). Although previous experience during pandemics and modelling studies of hypothetical pandemics have shown that it would generally be very difficult to avoid a pandemic completely using border measures and travel restrictions, such measures may delay introduction of the pandemic for a limited time (277, 278, 282, 283). As previously discussed, countries in which SARS was imported early in the pandemic often had severe local epidemics, and delayed importation allowed a country to be better prepared. Therefore, it is important that travellers follow WHO advice and cancel non-essential travel to

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affected countries accordingly in order to delay introduction of a pandemic infection into countries like Australia.

During the SARS pandemic, international travel in general declined, especially to East Asia where there was a 41% decrease in tourist arrivals during the period 1–21 April 2003, compared with the same period in 2002 (317). There was also a sharp decline in international short-term departures by Australian residents during March to May 2003 (286). Both VFR departures and total departures declined compared with the same period in 2002, but, as illustrated by the tables below, VFR travel declined less than travel for other purposes.

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Table 4.3: Short-term overseas departures by Australian residents (in thousands), March to May 2002 (286)

March April May Total (95% CI)

Total departures 283.5 267.9 294.5 845.9 (844.1–847.7)

VFR travellers 68.8 60.1 76.8 205.7 (204.8–206.6)

Holiday travellers 118.4 112.8 123.5 354.7 (353.5–355.9)

Business travellers 49.2 53.2 49.2 151.6 (150.8–152.4)

Table 4.2: Short-term overseas departures by Australian residents (in thousands), March to May 2003 (286) and decrease compared to same period in 2002

March April May Total Decrease vs Percentage (95% CI) 2002 decrease (95% CI) (95% CI)

713.9 132 15.6 Total departures 245.5 232.1 236.3 (712.2–715.6) (131.3–132.7) (15.5–15.7) 179.9 25.8 12.5% VFR travellers 59.9 59.1 60.9 (179.1–180.7) (25.5–26.1) (12.4–12.7) 288.8 65.9 18.6% Holiday travellers 94.5 101.8 92.5 (287.7–289.9) (65.4–66.4) (18.4–18.7) 126.4 25.2 16.6% Business travellers 48.5 32.9 45.0 (125.7–127.1) (24.9–25.5) (16.4–16.8)

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Figure 4.2: Short-term overseas departures by Australian residents by purpose of travel, March to May 2002 compared with March to May 2003

400

350

300

Travellers (thousands) 250

200 Mar-May 2002 Mar-May 2003

150

100

0 VFR travellers Holiday travellers Business travellers Purpose of travel

Source: Australian Bureau of Statistics (318-320). Error bars show 95% confidence interval. The decline in all travel categories during this period was statistically significant.

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The percentage decline in VFR travel (12.5%) was statistically significantly less than both the decline in total departures (15.6%) and the decline in departures for holiday or business travel (18.6% and 16.6%, respectively). Data suggests that during the SARS pandemic, VFR travellers were less likely than holiday or business travellers to delay or cancel their trip, as recommended by the WHO.

4.4.3 Findings from the focus groups

Outbreak awareness and concern

Even when not preparing for travel to China, focus group participants were generally aware of major outbreaks of respiratory infections occurring in China. Sources of information about disease outbreaks included Chinese newspapers and websites, and family and friends who live in China. Participants were generally concerned about outbreaks in China, whether they were planning to travel to China or not. Some participants said they worry about their relatives in China when outbreaks happen, and, in general, participants appeared more concerned about outbreaks than about other infectious risks during travel.

However, of concern was that some participants thought that they were not at risk because of their behavioural patterns, or that they could adequately reduce their risks using only certain behavioural changes. In particular, one community participant (106) said they would not be worried even if they were in China when an outbreak like SARS happened because they did not go out much.

If we were to go out I’d wear masks, but it really isn’t that big an issue. We’re old anyway, it’s not like we would go anywhere, we usually stay at home. The most we do is just to gather together with relatives or friends. (Community participant 106, regarding a potential respiratory outbreak)

Another community participant (201), when specifically asked, said they would not see a GP before VFR travel even if there was an avian influenza outbreak. Instead they “might eat healthily and do more exercise”.

Participants’ concerns about outbreaks of respiratory infections, particularly influenza, were not echoed by their relatives in China. Regarding the 2013 H7N9 outbreak:

At this time when we go to China, our family in Australia, they worry about [me] very much. They are very nervous. But in Shanghai, totally very calm. (Community participant 103)

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For international students the concern or lack thereof of their parents was very influential in their own perception of outbreak risk.

I don’t really care about the diseases because I can see my parents [and they] don’t really care. (Student participant 509)

Outbreak-related changes to travel plans

The concern of participants about outbreaks occurring during their trips to China influenced their information-seeking behaviours prior to travel. Similar to sources of travel health information more generally (see Chapters 2 and 3), participants’ sources of information about outbreaks included health professionals, family and friends in China, and information on the internet. International student participants were particularly likely to obtain information from the internet and social media. However, few participants said they would see their GP for advice before travel when there is an outbreak.

Discussion of cancelling or changing travel plans in the event of an outbreak included differing opinions. Some, but not all, participants stated that they would cancel travel to China. In addition, one community participant from Hong Kong (109) specifically said they would not go to mainland China when there is an outbreak. Circumstances around the need to travel, such as visiting sick relatives, were considered by many participants in their decision not to cancel travel during an outbreak. Otherwise, the decision to cancel the trip or not may depend on the severity of the outbreak or the level of perceived risk. Some participants would only cancel non-essential travel when they perceived the outbreak to be severe.

I think if it’s not a serious one, probably I would go, but take some precaution or don’t go to the crowded area, or if people coughing you just get away from him, something like that. Common sense. (Community participant 302, in relation to the 2013 H7N9 outbreak)

At least one participant stated that they would cancel a trip altogether if vaccination is recommended for travel.

If the medical advice is you need a special vaccine to go to the city because of too many infection, then probably I would cancel. (Community participant 302)

However, the risks of both actual and potential travel during outbreaks were often underestimated by participants. One community participant (707) described their travel to China during the SARS

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pandemic. Information from Chinese relatives prior to travel described life as normal in China and a perception that the risk was not serious. The seriousness of the outbreak was only discovered after returning to Australia.

Among the international student participants, two (411, 511) reported family in China advising them not to travel to China during outbreaks. On the other hand, other participants reported family and friends telling them that there is not much to worry about, and to travel to China.

My friends say it’s okay, it’s fine. It’s just happening with families who are not very concerned about their health. It’s not a major problem in Shanghai, so come back, we want to see you. (Student participant 405)

Participants may even rely on their parents to make the decision for them.

I wouldn’t really care about it, if really serious maybe my parents will stop me to go back. (Student participant 509)

When deciding whether to travel or not, international students may be concerned about potential delays to their studies if they get sick in China.

I think I would stop the trip, cancel the trip. Because once you get the flu you may not get back to Australia before March [the start of University semester]. (Student participant 506)

Behavioural changes during outbreaks

Overview Some, but not all, participants reported they would change their behaviour during trips where there was an outbreak. Participants said they would avoid crowded areas, be particularly vigilant about personal hygiene and washing hands, refrain from eating certain foods, or wear masks during an outbreak. Some participants also said they would consider not going out.

Actually, this time when we go to Shanghai, there’s the period of chicken flu. So we were very careful, and many of our time stay at the hotel, and we meet our friends, our colleagues in the restaurant around the hotel. (Community participant 103)

Some participants said they were aware of local government campaigns to encourage washing hands or the use of masks during trips where there was an outbreak. However, despite this

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awareness, there were participants who said they would not wear masks because they thought masks were useless.

Among both community participants and international students, some said they would adopt preventive behaviour, while others were less concerned. Again, for students, parental advice may play a role here.

The chicks, and the ducks, my parents were suggesting that I do not eat those kind of things in Australia or during the flight. (Student participant 407, in relation to the 2013 H7N9 outbreak)

Use of face masks Participants had mixed attitudes to face masks. Some appeared to be very comfortable with the use of face masks, and would even wear them whenever the air quality was poor or the weather was cold (i.e. not just during outbreaks). Others preferred not to use face masks because they look “weird” or were uncomfortable.

Many, but not all, participants were willing to wear masks during outbreaks of infectious diseases.

SARS, yes. SARS only, not usually. (Community participant 109, when asked whether they had ever worn a mask when in China)

We did it when SARS was going on, when we travelled. (Community participant 101, when asked whether they had ever worn a mask when in China)

Wearing a mask when you go out, or avoid going out. (Student participant 407, in relation to prevention measures during outbreaks)

Other participants, however, were not convinced about the effectiveness of masks.

Generally, masks are useless. (Community participant 107)

One community participant (302) said they carry masks in their luggage when they travel to China in case of an outbreak. Another community participant (304) said they took masks with them wherever they went when they were in China during the SARS pandemic.

Some participants noted that they would not wear masks if nobody around them was wearing masks. However, they would be more likely to use masks if everyone around them also wore masks, for example, during an outbreak. One community participant (206) also noted that wearing

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masks in public was more socially acceptable in China than in Australia, and this may increase participants’ willingness to use masks.

I would look weird. If everyone else don’t wear it, you would be the only one who wear a face mask. (Student participant 405)

‘Keeping healthy’ to prevent getting sick during an outbreak There was a common idea expressed by many participants that, during outbreaks, one should ‘keep healthy’ to prevent getting sick. When asked what ‘keep healthy’ means, one community participant (109) answered “sleep well, keep exercise, and don’t [get] sick”.

Some other participants had similar views.

I just believe in being generally healthy. Like you look after yourself, eat the right food, be happy, sleep well and all that. It all depend on this. (Community participant 201)

Vaccination and use of Chinese medicine Many participants were willing to receive a vaccine during an outbreak to protect them against the disease involved. One community participant (208) said they had a hepatitis B vaccine before going to China 3 years ago because there was a hepatitis B outbreak, and another (611) had an influenza vaccine before their trip because there was an influenza outbreak.

Some participants would be willing to receive a vaccine during serious outbreaks, even if they otherwise would not consider vaccinations for travel. For example, one community participant (305) said they would in general refuse vaccines recommended by their GP for travel because they were worried about vaccine safety, but when asked specifically about whether they would have had a SARS vaccine during the pandemic if there had been one, they said they would.

Participants from both international student and community groups also reported using or considering the use of traditional Chinese medicine to protect themselves against an outbreak. One (community) participant said they would drink a Ban Lan Gen (Isatis root) drink to protect themselves against SARS. Another (student) participant said,

I would take those herbal soup or herbal tea that like boost your immune system so you’ll have a lower risk to get sick. (Student participant 501)

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4.5 Discussion

4.5.1 Overview

The literature review provided evidence that China is likely to continue to be the source of pandemics of respiratory illnesses in the future. Of most concern is the ongoing presence of multiple strains of avian influenza with some ability to infect humans, and their potential for further reassortment into highly pathogenic strains with human-to-human transmission, and thus pandemic, potential. With a high frequency of travel to China and a higher risk of acquiring respiratory illnesses circulating in the local population during their travel compared with tourists, Chinese VFR travellers are thus important potential sources for future importation of pandemics into Australia. This risk is further compounded by several factors. VFR travellers are less likely to cancel their travel during outbreaks, as demonstrated by the example of SARS, and consistent with the focus group finding that they often underestimate the risks of travelling during an outbreak. Chinese VFR travellers also commonly have misconceptions as to how they can best prevent getting ill during outbreaks, for example, believing that traditional Chinese medicine can help or that sleeping well and exercising is adequate to prevent illness. On the other hand, they often practice preventive behaviours recommended by health professionals inadequately. Misinformed VFR travellers put themselves at risk by travelling during outbreaks in China and by undertaking inadequate preventive behaviour during travel. As a result, the risk of VFR travellers introducing pandemics into Australia earlier, leading to a severe local epidemic, is increased.

4.5.2 VFR travellers may underestimate the risks posed by an outbreak, and undertake non-essential travel and inadequate precautions

This study has uncovered a rich diversity of beliefs, practices and travel behaviours among Chinese VFR travellers which have not previously been well documented. Although participants were generally aware of outbreaks that were happening in China during previous trips, some participants underestimated the risks such outbreaks posed to their personal health. Risk estimation was often dependent on advice from family and friends in China, and some participants may take an overly relaxed attitude to an outbreak, especially during its earlier phases. (This will be further discussed below.) Some participants also believe that they would not be at risk for acquiring the infectious agent during an outbreak if they ‘keep healthy’ or if they use certain Chinese medicines.

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Underestimating the risks or severity of an outbreak sometimes meant that participants travelled to China for non-essential reasons when, according to WHO advice, they should have cancelled the trip. This finding from the focus groups can also be correlated to the international departures data from the Australian Bureau of Statistics, which showed that VFR travellers were less likely to cancel their travel during the SARS pandemic than were business and holiday travellers. Frequent travel to and from pandemic-affected countries increases the risk of early importation of pandemics into Australia before the country is well prepared, and, as the example of SARS in Canada, Vietnam and Singapore showed, this increases the likelihood of a severe local epidemic. Therefore, it is important that Chinese VFR travellers understand the importance of following the advice of authorities like the WHO and the Australian government to cancel non-essential travel during outbreaks, even where an outbreak does not look severe initially. To achieve this, it will be necessary to raise awareness among Chinese VFR travellers regarding the serious risks of travelling during an outbreak and the need to be careful about any outbreak even if initially it seems contained and not severe, and to dispel misconceptions like ‘keeping healthy’ or taking Chinese medicine being adequate measures to prevent one from getting sick.

Low risk perception also means that VFR travellers may not practice an adequate level of preventive behaviour during their travel. This will be discussed further below.

4.5.3 Chinese VFR travellers’ risk perception is based on information from both professional and non-professional sources

Participants’ sources of information about outbreaks are similar to their sources of travel health information more generally (see Chapters 2 and 3). These include sources as diverse as Chinese newspapers and websites, their general practitioner, and family and friends who live in China. This finding is consistent with a previous study conducted in the Netherlands and the UK which found that Chinese immigrants often sought information regarding emerging infectious diseases from family and friends and Chinese language media (172).

Focus group participants were generally aware of outbreaks in China, having received information about them from the aforementioned sources. Although this awareness is a positive thing, sources of information other than health professionals, for example, family and friends who live in China, may give an underestimated account of the risks associated with an outbreak. This becomes a particularly important concern for the many participants who rely solely on such information, and as a result undertake inadequate precautionary behaviour.

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International students’ risk perceptions are particularly likely to be influenced by their parents. Many participants from the international student focus groups reported that their parents provided advice regarding whether to be concerned about outbreaks and whether to travel to China during an outbreak, as well as other precautions to take. Some participants did report that their parents gave them useful advice, for example, not to go back to China during an outbreak. However, other participants reported that their friends and family seemed to not be too concerned about outbreaks happening in China (mainly referring to the then-current 2013 H7N9 outbreak), and actively advised them to travel. The importance of this point is further reinforced by the observation of some participants that people in China do not seem to be very concerned about outbreaks in general (discussed further below).

Because advice received from non-professional sources may be inaccurate or counterproductive, education campaigns should reach out to Chinese VFR travellers to adequately warn them about the risks of travel during an outbreak. Such education campaigns should particularly be run when there are actual outbreaks in China. This would be particularly important in the Chinese international student population.

4.5.4 Low concern about outbreaks amongst those living in China

Participants’ risk estimation regarding outbreaks was often dependent on advice from family and friends in China, some whom appeared to have a low level of concern. The lack of concern about outbreaks among those living in mainland China has also been confirmed by other studies, as described in Chapter 1. A survey of 3731 participants conducted across several urban and rural areas in China in 2013 found generally low levels of concern regarding the H7N9 outbreak (170). A generally low level of concern for outbreaks and inadequate uptake of preventive measures was also found in another study conducted in China during the H1N1 2009 pandemic, with 72.4% of respondents not worried about contracting the pandemic virus (169). However, as described in Chapter 1, multiple studies conducted in Hong Kong found that respondents were generally more vigilant about outbreaks and pandemics (161, 162, 164, 166).

This low concern about outbreaks among people living in China clearly presents yet another important barrier to overcome when educating Chinese VFR travellers to take adequate precautions during times of outbreak. Education campaigns should focus on the potential consequences of underestimating risks in the early stages of outbreaks, and hence why it is important to treat every outbreak seriously. Education regarding the potential seriousness of outbreaks and the importance

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of cancelling non-essential travel should also be provided to family and friends in China, to the extent it is feasible to do so. For example, VFR travellers could be encouraged to share internet- based material from education programs with family and friends in China.

4.5.5 Low risk perception, misconceptions and other issues need to be addressed to encourage proper precautions during outbreaks

Low risk perception also means that VFR travellers may not practice an adequate level of preventive behaviour as recommended by health authorities when travelling in China during an outbreak, thus further increasing their risk of infection. Studies conducted in Hong Kong during the SARS pandemic found that travellers to affected destinations, including mainland China, often did not undertake recommended preventive behaviour to adequately protect themselves from the outbreak, for example, by avoiding crowded places, washing hands frequently and wearing masks (321, 322). This is consistent with the findings from focus groups in this study in which participants had mixed attitudes to the adoption of such behaviour. However, some participants stated that during more severe outbreaks they would be more willing to change their behaviour.

Among focus group participants, there were mixed attitudes towards face masks. In contrast, a cross-sectional survey of 1115 participants conducted during the SARS pandemic in Hong Kong found that 75.8% of respondents were willing to wear a mask (167). The focus groups were conducted shortly after the H7N9 outbreak, which usually required contact with birds or poultry for infection (289) and, as stated by some focus group participants, many people in China were not very concerned about the outbreak. The participants’ mixed responses to preventive measures may be a reflection of this lack of concern regarding the current outbreak rather than towards all outbreaks. However, if VFR travellers are selective about applying preventive measures, with some only willing to apply them during severe outbreaks, this is still a major concern, especially in the early phases of outbreaks where severity can be underestimated.

One of the aforementioned studies of travellers from Hong Kong to mainland China during the SARS pandemic also found that the 839 surveyed participants were less likely overall to undertake preventive behaviour while in China (compared with the everyday practices of the general Hong Kong population as reported in other studies during the pandemic), and had a lower risk perception regarding contracting SARS in China (321). The authors of that study hypothesised that those travelling during the outbreak were a self-selected group whose attitudes and behaviours were ‘not conducive to SARS prevention’. Further study may be needed to determine if Chinese VFR

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travellers who travel during an outbreak are also a self-selected group with lower risk perception and vigilance towards outbreaks.

Multiple focus group participants had misconceptions which may also become barriers to adequate preventive behaviour during outbreaks. Some participants believed that ‘keeping healthy’ and taking Chinese medicine could help prevent contracting the outbreak illness, and they may potentially be less vigilant or more willing to undertake non-essential travel because of this. Another important misconception some participants have is regarding masks. Some participants would not wear masks even during an outbreak because they do not believe masks are effective. This is consistent with a Hong Kong study of 13 cross-sectional surveys, which found that, although a majority of participants practiced preventive behaviours during outbreaks, only a minority reported wearing a mask (166). Education on the effectiveness of masks and the way they should be used for maximal effectiveness appears to be needed.

Another concern raised by participants in the focus groups was that they are less willing to wear masks if it is not common in the surrounding general population. This finding is further supported by the aforementioned study of 839 Hong Kong travellers to China during the SARS pandemic, which found that, although 67.3% of participants used masks all or most of the time in Hong Kong, only 51.3% of those participants did so while travelling in mainland China. The authors hypothesised that this may have been due to a lower rate of mask use among the general public in mainland China, and some travellers not wanting to be labelled as ‘different’ while travelling there (321). Education interventions should highlight the benefits of using masks, and the importance of ensuring that adequate self-protection during outbreaks overrides other social concerns.

Education interventions relating to mask use, risk awareness and misconceptions will be further discussed in Chapter 5.

4.5.6 Some Chinese VFR travellers will undertake international travel with influenza symptoms, posing a risk of outbreak transmission to Australia

It is important to note that some focus group participants reported willingness to travel between China and Australia even when they are sick (see Chapters 2 and 3). A random telephone survey of 406 Hong Kong travellers to mainland China also showed that for mild conditions including influenza, 57.2–70.9% of respondents would defer seeking medical treatment until they returned to Hong Kong (93), supporting the idea that travellers commonly believe that upper respiratory

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infections should not pose a barrier to travel. However, a traveller may be developing early symptoms of an outbreak illness while thinking that they have just caught the common cold, for example. This is especially likely during the early stages of an outbreak, when community awareness is low and risk is commonly underestimated, as one participant recalled regarding travel to China during the SARS pandemic. If such travellers then undertake international travel, they will effectively bring the disease to their destination country. A study of 820 travellers returning to Hong Kong via air travel during the SARS pandemic found that 16% of respondents would delay seeking medical care for influenza-like symptoms until their return (322). A French study conducted during the 2009 H1N1 influenza pandemic provided additional evidence that some travellers undertook air travel back home despite having developed symptoms of an outbreak illness while travelling abroad (323). The survey, conducted on 113 returned international travellers who presented in France with symptoms of respiratory illness, found that 54.5% developed such symptoms prior to returning to France, but decided to travel anyway.

In the aforementioned Hong Kong study where a majority of respondents stated they would delay seeking treatment for influenza, reasons given for deferring medical treatment included perceived inferiority of medical services in mainland China, not knowing where to seek medical treatment in mainland China, and the lack of support of family and friends (93). The focus group findings from this study have also found that familiarity and concerns about competency of health professionals may lead to a strong preference of seeking medical treatment in one location over another. While some Chinese VFR travellers preferred to seek treatment in China, others preferred to seek treatment in Australia for various reasons.

There is a very real risk that some Chinese VFR travellers who develop outbreak illnesses while travelling in China will still travel back to Australia before seeking medical attention, effectively importing the outbreak into Australia. The lessons from SARS highlight how even a small number of infected travellers can cause the rapid spread of a global pandemic. Therefore, the importance of seeking medical care promptly during outbreaks and not undertaking further travel until cleared by doctors must be impressed upon every traveller. Because VFR travellers are more likely to undertake non-essential travel during outbreaks, and tend to not seek medical advice before travelling, they may not be aware of this message, and should therefore be particular targets of such an intervention. Chinese language pamphlets distributed at airports during times of outbreaks can be an effective way of reaching this population (324). Advertisements in the local Chinese media could

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also be effective, given the propensity for this population to receive outbreak information from Chinese language media, as previously discussed.

4.5.7 Implications of these findings, in the wider context of China as a source for pandemics

For reasons that were examined in the literature review, southern China is expected to continue to be a source for the emergence of pandemics. The SARS pandemic of 2003 also taught us the important lesson that, in the modern age, air travel can cause pandemics to quickly and effectively spread across the world. VFR travellers are an important potential source in this spread. In the case that the next influenza pandemic originates in China, it is possible that VFR travellers visiting China could introduce the pandemic into Australia.

Although a pandemic caused by a new avian influenza virus has not occurred since 1968, there is now the very real possibility of such a pandemic occurring at any time. If an influenza virus is to become the next pandemic strain, there is a high likelihood it will originate from China where there are already multiple potential candidates. Although HPAI H5N1 is only one of these, it should probably be the one of most concern, due to its high mortality rate and the fact that it has already caused outbreaks among humans in multiple parts of the world. As the virus appears to have originated in southern China and is now endemic in poultry there, and as there have already been a significant number of human infections in various parts of China, China is the most likely source of such a pandemic. H7N9 is another candidate to be concerned about. Although it appears to have a lower mortality rate than H5N1, it also appears to be more transmissible to humans, as the many cases so far have demonstrated.

With the very real risk of a pandemic originating in China and spreading to Australia via VFR travel, Chinese VFR travellers must be made aware of the possibility that outbreaks may happen in China at any time. They should also be informed about how they should act if an outbreak happens while they are travelling there. This research has found that Chinese VFR travellers commonly undertake inadequate preventive behaviour in relation to outbreaks, due to misconceptions and inadequate risk perception. This is consistent with a broader picture of suboptimal travel health behaviour related to low risk awareness more generally, and consistent with the findings of other VFR traveller studies, as described in Chapters 2 and 3. All this further makes the case that efforts to educate Chinese VFR travellers and encourage pre-travel health preparation as well as adequate precautionary behaviour during travel are warranted. These travellers also need to fully understand

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the risks an outbreak may pose to their health, and the importance of delaying non-essential travel to China during outbreaks. Although all this may not prevent the outbreak from eventually reaching Australia, it may help delay its introduction. As demonstrated by the SARS pandemic, this could be crucial in limiting the extent and severity of any local epidemic in Australia.

4.6 Conclusions

China has been the source of multiple important respiratory infection pandemics in the last century. Due to environmental and social conditions, China is likely to continue to be a source of such pandemics in the future. The fact that multiple potential agents for such an outbreak are already present further highlights the likelihood of a future pandemic originating from China. Chinese VFR travellers frequently travel between Australia and China, and have close contact with the local population while in China. Therefore, they are an important group of travellers to target in the effort to prevent importation of pandemics into Australia.

Chinese VFR travellers are generally well informed of the latest outbreaks in China, but some appear to take an overly relaxed attitude to such outbreaks in the early stages, and may even undertake non-essential travel to China. Their attitude of low concern to outbreaks may be influenced by family and friends in China, whom such travellers often rely on for travel health information, and who have been shown to have generally low levels of concern regarding outbreaks. Chinese VFR travellers’ willingness to undertake preventive behaviour if travelling to China during an outbreak was found to be mixed, with some travellers more willing than others to wear face masks and avoid crowded areas, for example. Although generally unlikely to have vaccines before travel to China, they are more willing to receive vaccination specifically for outbreaks.

Overall, there are multiple concerns regarding Chinese VFR travellers and their travel during outbreaks which need to be addressed. The fact that China continues to be a likely source of future pandemics highlights the importance of addressing these issues. Possible education interventions will be further discussed in Chapter 5.

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Chapter 5

Conclusions

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5.1 Introduction

Australian Chinese VFR travellers contribute to a substantial proportion of all travel between Australia and China (84). Ensuring that these travellers are taking appropriate travel health precautions is important for improving their health outcomes. It is also important from the perspective of national disease control, as China continues to be a likely source of future pandemics (2, 3, 11, 302, 313). Towards achieving this objective, this thesis presents novel data which provides an understanding of the baseline knowledge, attitudes and travel health practices among Chinese VFR travellers. The thesis further identifies the reasons for suboptimal travel health preparations and precautionary behaviours among these travellers. This information will be useful to inform the design of tailored, evidence-based and culturally appropriate interventions, including health promotion messages, to improve travel health behaviour and outcomes for Chinese VFR travellers. Furthermore, the international student study has provided important information regarding some unique issues for Chinese international student VFR travellers, such as their reliance on parents to make travel decisions, their extensive use of the internet including social media for health information, and the way university schedules affect their travel patterns.

Numerous studies show that VFR travellers from other ethnic groups are at a higher risk of certain infectious diseases, for a variety of reasons (14, 19), compared to those travelling for other purposes. However, in the absence of studies specifically relating to ethnic Chinese VFR travellers, it was not clear whether findings for VFR travellers of other ethnicities are generalisable to Chinese VFR travellers. The studies included in this thesis are the first substantial studies into the travel health-related knowledge, attitudes and behaviours of Chinese VFR travellers. These studies found that multiple issues previously identified in VFR travellers in general, including low rates of seeking pre-travel health advice, low risk perception of VFR travel and inadequate use of precautions during travel (16, 19, 22, 36, 211), are also applicable to Chinese VFR travellers. However, the studies also identified issues unique to this population, including the influence of family dynamics and Chinese culture, the use of Chinese medicine, the consumption of certain foods, and frequent travel during the Spring festival which coincides with the peak influenza season in China. These issues were explored for the first time using qualitative research methods, allowing issues to be explored in depth in a way that could not be done in quantitative studies, which account for the majority of existing VFR traveller-related studies. The new knowledge gained from these studies is an important contribution to travel medicine. It will be valuable for health professionals providing travel health consultations to Chinese VFR travellers, and for informing strategies to

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improve national disease control, especially in the context of preventing importation of future outbreaks from China.

This concluding chapter summarises the major findings of this thesis and explores the implications of the findings and recommendations for future research.

5.2 Key findings from this research

This thesis explored the knowledge, attitudes and behaviours of Australian Chinese VFR travellers and Chinese international university students, and included an outbreak risk analysis. The major outcomes of the research are summarised in the following sections.

5.2.1 Community focus groups

A series of focus groups were held in two locations in Sydney, Australia, involving ethnic Chinese Australians who had undertaken travel to China for the purpose of visiting friends and relatives in the previous 18 months. The aims of these focus groups were to understand the travel health-related behaviours of Australian Chinese VFR travellers, and to explore barriers to the uptake of travel health-related measures. Participants’ knowledge regarding travel health, travel health-related behaviours and attitudes, including pre-travel preparations and precautionary behaviour during travel, and the use of professional travel health services were explored.

The focus groups revealed that important travel health issues found in other VFR travellers, including low pre-travel health-seeking behaviour, low awareness of the health risks regarding VFR travel and inadequate precautionary behaviour during travel, apply to Australian Chinese VFR travellers, and identified several important reasons for this. Participants usually did not seek pre- travel health advice from health professionals, and often relied on the internet and family and friends in China, similar to the findings of other studies on VFR travellers. However, the influence of family and friends on Chinese VFR travellers was also found to be strong in various areas beyond providing travel advice, including attitudes towards travel health preparation, risk perception, and activities undertaken and food consumed during travel. Participants generally had a low risk perception regarding VFR travel to China, both due to perceived familiarity with China, and several knowledge deficits and misconceptions regarding the infectious risks present in China, including a misconception of residual immunity for respiratory and enteric pathogens. Important barriers to accessing health care in Australia were described, including the prohibitive cost of consultations and vaccinations, and language and cultural barriers, similar to what has been

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described in multiple other migrant health studies. Unfamiliarity with the Australian healthcare system by many participants resulted in low access and the use of health providers in China during travel for nontravel-related health issues such as dental care. Participants were generally sceptical of the need for vaccination for the purpose of travel to China, and important misconceptions relating to vaccination were identified. Most importantly, the belief that vaccines are only required for certain at-risk groups and the belief that vaccines can be harmful for the immune system were common. Participants also reported strong concerns regarding the safety of vaccines, which may be related to such concerns being repeatedly aired in Chinese media in recent years. Also unique to Chinese VFR travellers was the extensive use of Chinese medicine, with which many focus group participants often self-medicated to both prevent and treat illnesses, including in the course of their VFR travel. In fact, some participants reported using Chinese medicine more while in China, due to higher availability.

In summary

Chinese VFR travellers share with other VFR travellers many issues, including a low risk perception of VFR travel, inadequate pre-travel health preparations, relying on advice from non- professional sources including family and friends, and multiple barriers to seeking health care in Australia.

Chinese VFR travellers were found to be extensively influenced by family and friends in terms of the activities they undertake and the food they consume during VFR travel.

Chinese VFR travellers have strong concerns regarding the safety of vaccines. This may be related to the fact that vaccine safety concerns have received substantial publicity in Chinese media in recent years.

Chinese VFR travellers commonly use Chinese medicine, including as self-medication, to treat and prevent illnesses during VFR travel.

5.2.2 International student focus groups

China is a major source of international students for Australia (244), and return travel to their country of origin during their enrolment is common for international students (71). Chinese international students in Australia represent an important group of VFR travellers to China. This population has a different social context to the general ethnic Chinese migrant community in Australia. They very often have no relatives at all in Australia. They also have particular social

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circumstances relating to their temporary residency on student visas, and they often face important issues that are not shared by other Chinese VFR travellers.

Despite the unique issues faced by international students, many of the issues found among other Chinese VFR travellers also arose with the international student groups. For example, there was a reluctance to seek professional health advice for return travel to China, with many not conceiving any risk associated with such travel. Subsequently, inadequate pre-travel health preparations and inadequate use of precautionary behaviours during travel were described. The perception of familiarity with China was a strong influence on poor uptake of professional health advice and assessment of the need for vaccination for the purpose of travel. Although perceived familiarity and associated low risk perception were common among all VFR travellers, a strong view that China is their ‘home’ was uniquely found in the student groups.

Students were generally not aware of the potential health risks related to VFR travel to China. The influence of family and friends was found to be especially strong in this population, and this influence may be either positive or negative in relation to the encouragement of adequate pre-travel health preparations. International students did not view their return trips to China as VFR travel, hence they did not think that preparations or precautions were necessary for this kind of travel. Participants also felt they were more familiar with health risks in China than Australian doctors and therefore did not consider health advice from Australian health professionals as helpful.

Unique to this group was frequent travel during the peak influenza season in China, which coincides with Australian university holidays. Moreover, international students usually did not undertake any vaccination before travel, including influenza vaccination, as they believed they were just ‘going home’. Compared with other VFR travellers, cost was described as a more significant barrier to accessing health care, including vaccinations. While some consultation fees and the cost of some pharmaceuticals and routine vaccines are covered under Medicare and PBS for Australian residents, the equivalent rebate is not always available through the private insurance required for those on international student visas (262). Chinese international students were avid users of the internet and social media to search for and access travel health and other health-related information. They received both professional information (e.g. from health authorities) and non-professional information (e.g. social media discussions among friends) through this channel.

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In summary

Chinese international students as VFR travellers shared many issues with other Chinese VFR travellers, as reported in the previous section.

International students particularly see China as their ‘home’, and view VFR travel as simply returning home. This can further justify their lack of pre-travel health preparations.

International students often travel to China during the peak influenza season, due to the university’s yearly schedule.

International students often use the internet, including social media, for extensive research in pursuit of health information. They receive both professional and non-professional advice through this channel.

5.2.3 Outbreak risks and behaviour modification

As China has been a major source of outbreaks in the past (2, 3, 11, 302, 313), and as VFR travellers have been an important source in the transmission of previous outbreaks like SARS (12), understanding and improving Chinese VFR travellers’ health behaviour from the perspective of potential outbreak transmission is an important part of mitigating the risk of future pandemic importation into Australia. The aim of this chapter was to assess the likelihood of future pandemics arising from China, and also to identify behaviours in Chinese VFR travellers that could potentially facilitate the spread of future outbreaks from China into Australia.

A review of the literature describing previous outbreaks originating in China and ongoing outbreak risks in China provided several important findings regarding the risk of future pandemics. Most importantly, based on both historical precedence and observation of cultural practices, it is expected that China is likely to continue to be a source of future outbreaks of novel influenza viruses and other respiratory pathogens (11, 98, 99). With several possible agents currently circulating in China, such an outbreak may occur at any time (100). H5N1 and other avian influenza viruses have been identified over the past two decades in both humans and animals in China (99, 100) and have pandemic potential. Travellers, particularly VFR travellers, are likely to play an important role in the international spread of such an outbreak. SARS was first introduced to Canada by a VFR traveller (12, 97). The volume of VFR travel was also found to decline less during times of outbreaks than travel for other reasons. Using data collected by the Australian Bureau of Statistics regarding outbound travellers’ reasons for travel during the 2003 SARS outbreak and comparing it

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to data for the same period in 2002 (286), it was found that the magnitude of the decline in travel for VFR purposes was lower than the magnitude of the decline in travel for other purposes (12.5% vs 15.6%), and the difference was statistically significant. Focus group participants described past experiences of travel to China during the SARS pandemic and outbreaks of novel influenza and reported practicing inadequate precautions, for example, by not cancelling travel during the outbreak. Focus group participants also described future intended behaviours during hypothetical outbreaks of respiratory diseases. The intention to practise risky behaviours was common, including an unwillingness to use face masks if this is not common among the local population, and boarding flights when unwell. Some participants also had the misconception that they could prevent contracting outbreak illnesses by ‘keeping healthy’ (e.g. exercising and eating well), or that taking certain Chinese medicines would make them immune. These are important concerns that should inform future outbreak preparedness including future health education for Chinese VFR travellers. These results also highlight the potential risk of infectious diseases from outbreaks in China being introduced to Australia via VFR travellers.

In summary

China is likely to continue to be an important source of major outbreaks and pandemics of respiratory viruses.

There are already potential candidates for such an outbreak or pandemic circulating in wildlife in China, as well as causing occasional human infections. This highlights the importance of being prepared against any potential pandemic originating from China.

Chinese VFR travellers are potential sources for the introduction of any such pandemic into Australia. Focus group findings showed that Chinese VFR travellers do not always cancel non- essential travel during outbreaks, that they often practice inadequate precautionary behaviour when travelling during outbreaks, and that they sometimes still undertake international travel when unwell, all further increasing this risk.

Evidence from the SARS outbreak in 2003 showed that VFR travel is less sensitive to pandemics, compared to travel for other purposes. This is consistent with focus group participants reporting a failure to cancel non-essential travel during past outbreaks.

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5.3 Implications and future recommendations

Multiple barriers to optimal travel health behaviour in Australian Chinese VFR travellers have been identified in this thesis. This information could be used to inform the development of future interventions, such as education programs and awareness campaigns, to address these barriers. This research could also be used to inform the design of quantitative studies to determine the prevalence of identified issues among the wider Australian Chinese community. Although this research has highlighted many important issues, further studies are required to determine the extent of identified risk behaviours among Australian Chinese VFR travellers and the influence of pre-travel health advice and travel health information in changing health behaviours.

The following sections will explore what future interventions should address, and how they can be delivered.

5.3.1 Future interventions will need to first target risk perceptions

A common reason for VFR travellers perceiving travel to China as low risk was the familiarity derived from long periods of residence in China prior to migration to Australia and strong ties to their family and friends currently residing in China. In the absence of personal and close family experiences with severe infectious diseases, travel to China was not perceived as a risk for acquiring these diseases. Familiarity with China and low perceived infectious disease risks were especially strong among international students, who saw travel to China not as a risk activity but as simply ‘returning home’. Higher risk perception is associated with increased willingness to undertake preventive health activities, as shown across various risk reduction activities in public health, including smoking cessation and the cessation of other addictive substances (216, 253, 325, 326), cardiac risk reduction (219), cancer screening (217), diabetes screening (218) and uptake of annual influenza vaccination (215). Indeed, the Health Belief Model recognises perceived susceptibility and perceived severity, which can be further combined into the concept of ‘perceived threat’ (213), among the determinants of health service use (146-149). Risk perception is a key factor in deciding whether to adopt risk reduction activities. The tendency of VFR travellers to be unaware of health risks in their former homeland is not unique to the Chinese. Studies of VFR travellers of other ethnic groups have also shown low risk perception as a major factor influencing uptake of pre-travel health advice, vaccination and compliance with malaria chemoprophylaxis (19, 24, 36, 54, 62). Despite perceived familiarity with China, many focus group participants demonstrated low awareness and poor knowledge of important infectious disease risks in China, including vector-

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borne diseases, the particular risks of visiting rural areas and the diseases preventable by vaccination. It is therefore not surprising that VFR travellers do not adequately seek pre-travel health advice from a health professional or otherwise seek information regarding infectious disease risks in China. This, in turn, limits their ability to be informed or to protect their health during travel. Detailed health information for travel to China is already available, via reputable sources such as the CDC, WHO and Australian Government websites among others, and is easily locatable via Google and other search engines. However, focus group participants did not seek this information during their pre-travel preparations and, in most instances, were not aware of its existence. Instead, participants relied on news and portal websites in China, which provide up-to- date information on outbreaks but generally do not provide advice relating to other aspects of travel health, and believed this to be adequate information for their VFR travel. As such, comprehensive, reputable travel health information can only effectively reach Chinese VFR travellers as a population if it is actively delivered to them without their need to search for it. Only once they have become well informed about the infectious disease risks present in China, and the risks involved in VFR travel to China, will Chinese VFR travellers appreciate the benefit in actively seeking professional pre-travel health advice and undertaking adequate pre-travel health preparations.

Future education interventions must therefore be designed to actively address this pattern, by delivering advice and information to this population without their need to intentionally look for it. Health promotion campaigns delivering messages proactively can utilise channels such as television, radio, newspapers, the internet, the distribution of pamphlets, and event sponsorship, and such campaigns have proven effective in raising awareness for a variety of health issues (327-334). It should be emphasized that any health promotion campaigns targeting VFR travellers should not simply dismiss their strongly held feelings of familiarity with China, as such emotional invalidation can be counterproductive for the acceptance of the health message. Health promotion campaigns should also avoid painting travellers of Chinese decent as a source of contagion for Australia, as this can be misinterpreted as being rooted in xenophobic attitudes and impede these targeted health messages.

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5.3.2 Education to address identified issues should be delivered via multiple channels

As described above, issues identified among Chinese VFR travellers in this study include low risk perception and low awareness of major infectious risks in China, a low rate of obtaining professional travel health advice, inadequate travel health preparations, and unfamiliarity with the Australian healthcare system and the role of preventive medicine. Many of these relate to knowledge deficits and a lack of awareness about certain health topics. Education interventions have been successfully used to improve knowledge, awareness, and associated behaviour in a wide variety of health topics (327, 329, 332, 335-340), and therefore should be useful for the multiple aforementioned issues in Chinese VFR travellers. As there are many issues to address, multiple education interventions, each targeting one or several related issues, will be required. Possible education interventions to address issues identified by this study are presented in Table 5.1.

Table 5.1: Possible education interventions to address important issues for Chinese VFR travellers

• Information to correct the general misconception of VFR travel being low risk • Information to highlight important infectious risks in China • Information to highlight activities during VFR travel that may be high-risk, e.g. visiting wet markets and rural areas, eating street food • Education regarding optimal behavioural precautions for outbreaks of respiratory infections, including handwashing and avoiding crowded areas • Recommendations to delay travel to China during times of major outbreaks • Education regarding the importance of travellers in the spread of disease during the early phase of an outbreak • Education regarding the benefits of vaccination for travel, using discussion of costs vs benefits • Education regarding the importance and benefits of obtaining professional pre-travel health advice, and the particular benefits of using professional travel health services • Education regarding how the Australian healthcare system operates and how patients can best take advantage of the system, e.g. the benefits of scheduling appointments in advance

Delivering travel health advice and education via a combination of channels is also likely to be helpful. Firstly, such advice would be able to reach more travellers; for example, travellers who did not consult a health professional may still be able to receive useful information from other channels.

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Moreover, even travellers who consult their GP or a professional travel health clinic would benefit from education delivered via additional channels. Travellers do not always correctly remember all the advice they receive (341-343), and because travel health interventions are multifaceted, the breadth of advice that needs to be given often makes complete recall from one session unrealistic (30). Therefore, further supplementary education would be of benefit, even for those who have attended travel health clinics. Furthermore, travellers do not always adhere to advice given by travel health clinics (344). Further reinforcement of such advice from other channels, especially from other health professionals and/or health authorities, can serve as an additional reminder, and may improve both motivation to receive travel health information and intention to adhere to advice. This idea is supported by studies of campaigns to encourage the uptake of vaccination that have shown education interventions delivered via multiple channels are more effective (242, 243). It is further supported by a study showing counselling for health behaviour change is more effective in the long term when supported by prolonged mass media exposure to messages that reinforce the counselling (335).

Potential channels through which health advice could be received by Chinese VFR travellers include GPs and travel health clinics, pharmacists, family and friends, mass media (e.g. Chinese language newspapers and radio), websites (both professional and non-professional sources), social media, and information provided at the airport (see figure 5.1). Advising GPs to deliver opportunistic health advice, i.e. delivering the advice to patients consulting for other reasons, has been effectively employed in other areas of health promotion, such as smoking cessation (345), alcohol and drug abuse interventions (346), and skin cancer prevention (347). Therefore, GPs, especially Chinese-speaking GPs who treat many Australian Chinese patients, should be encouraged to deliver opportunistic advice to their Chinese patients regarding VFR travel health. There has also been a recommendation in the literature for GPs to routinely ask their patients if they intend to travel overseas (26). This would be another way to effectively reach Chinese VFR travellers who would otherwise not seek pre-travel consultations. Pharmacists are a potential source of professional health information besides GPs and travel health clinics (348, 349), and should be encouraged to participate in the delivery of travel health advice. However, similar to GPs, pharmacists, as a group, have been found to have substantial knowledge deficits regarding travel medicine (348, 349). Therefore, both GPs and pharmacists should be encouraged to improve their knowledge on important travel health issues, including undertaking professional courses.

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It has been previously found that ethnic Chinese living in Western countries commonly seek information regarding outbreaks from Chinese language mass media (172), and articles and advertisements in Chinese newspapers and Chinese radio can reach many ethnic Chinese living in Australia. Although websites provided by multiple authorities (e.g. WHO, CDC, Australian government) are in and of themselves not sufficient for educating Chinese VFR travellers as a population since many travellers do not access them, their role in reinforcing travel health advice would still be helpful for those who do access them. It is important that this advice is available in Chinese, to prevent language barriers impeding access. Social media, which will be further discussed below, is a promising channel to deliver travel health information (271, 272), particularly to younger Chinese VFR travellers. It has the benefit of reaching those who would not otherwise access the aforementioned authorities’ websites. Education campaigns should also encourage the discussion of travel health issues with family and friends as a way to further propagate the messages delivered, as the focus groups have found that family and friends are not only an important source of advice for Chinese VFR travellers, but also a strong influence on their activity patterns while in China.

Finally, providing information at the airport, for example, in a Chinese language pamphlet to be distributed at check-in counters, could be useful as a final reminder for travellers before they depart. Although this would be too late to optimise pre-travel preparations, behaviour during travel can still be affected, plus there would also be educational value for future VFR travel. Airport information is especially useful for targeting those departing on short notice, who have likely not sought professional pre-travel advice before reaching the airport (324).

Figure 5.1: Potential channels through which health advice could be received by Chinese VFR travellers

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5.3.3 Factors contributing to low uptake of pre-travel health advice should be addressed individually

If efforts to change travel health-seeking behaviours are to be effective, we need to understand the underlying factors that influence health-seeking. Although familiarity with China and low perceptions of the risks of VFR travel were major themes arising in this thesis, barriers to accessing health care were also important. This is supported by quantitative studies of travellers from other ethnicities (24, 25, 32, 47). It is also again consistent with the Health Belief Model, which states that besides a low perceived threat of disease, perceived barriers to access is another reason people may not access health care. In addition to health promotion as discussed above, addressing barriers to health care access is an important dimension for improving VFR traveller health-seeking behaviours. Several major barriers to accessing health services for pre-travel health advice were identified by this thesis and are addressed below.

For both recent immigrants and international students, unfamiliarity with the Australian healthcare system was an important barrier to seeking health care in Australia in general and to attending pre- travel health consultations for VFR travel to China. Residents who are unfamiliar with the Australian health system found navigating the system cumbersome, which discouraged their use of health care generally. For example, some focus group participants raised dissatisfaction regarding the appointment booking system used in Australian GP clinics, in which patients generally need to

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book an appointment in advance before they can see their GP, in contrast with the situation in China, where patients can usually just walk in. Issues like this can discourage visits to the GP that are deemed ‘non-essential’, which for many focus group participants would include travel health- related visits. Unfamiliarity with the health system and associated difficulties and dissatisfaction with its usage have also been reported in other migrant groups in Australia and other countries (221- 223, 350, 351), and migrant groups are also often reported to have lower rates of accessing preventive care (352, 353). A widespread lack of awareness of professional travel health clinics was also identified. There is therefore value in educating Chinese VFR travellers, and more generally the Australian Chinese community, about how the Australian healthcare system works and the value such a system provides to patients, as well as raising awareness about professional travel health services and the benefits of using such services. This could be facilitated by, for example, pamphlets distributed at Chinese-speaking GP offices, or through articles in Chinese newspapers describing the Australian system and its benefits.

Language barriers, which impede effective conversation between healthcare providers and patients, are one of the most important barriers to accessing health care for migrants (225, 226, 350-354). Language barriers were an important concern for many of the participants in this study, particularly those unable to fluently converse in English and older participants. However, even those fluent in English and comfortable with communicating in English can sometimes find receiving health advice in English to be unfamiliar, which negatively impacts on the quality of health advice received. The fact that some participants in the focus groups were able to generally communicate in English but had difficulty referring to medical terms highlighted this. Cultural barriers, including a feeling that mainstream Australian GPs do not respect or understand beliefs regarding traditional medicine, ethnic-specific dietary practices, or culture-specific expressions of health and illness (350, 351, 354) , further compound this. Although there are numerous Chinese-speaking GPs available in the major cities of Australia, this is likely not the case for travel health-specific services. GPs are an important source of travel health advice, especially where cost and access are major barriers to using professional travel health services, but they are not a complete substitute for such services. For example, for travellers to certain rural or other higher risk destinations, Australian GPs may be less familiar with the more complex advice and less common vaccinations and prophylaxis needed for those situations. GPs have been shown to more frequently give incorrect advice than travel health clinics (24), and a recent survey of Sydney GPs also found that the majority failed to recognise VFR travellers as a particularly high-risk group compared to holiday travellers (58). The inability to use professional travel health services due to language and cultural

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barriers is a major disadvantage that needs to be rectified for Chinese VFR travellers, for example, by encouraging the employment of more ethnic and culturally diverse staff in such services. Chinese GPs can also then be encouraged to refer their patients to travel clinics that have employed Chinese doctors. In the meantime, the free interpreter service available in Australia can be of some help to reduce the language barrier for accessing travel health services. However, this service has been shown to be currently underused (227). Therefore, health professionals in Australia, including travel health professionals, should be made aware of the availability of this service and the benefits of its use.

Another important barrier to address is cost. Although previous quantitative studies of VFR travellers of other ethnicities have found that cost was not among the most common reasons for taking inadequate preparation measures (24, 33, 52), such studies typically only allow respondents’ answers to be classified into several limited options. This qualitative study has found that while cost was not the major reason for suboptimal preparations, it was nevertheless an important barrier. This was especially applicable to international students, whose private health insurance may not cover the entire range of services covered by Medicare and PBS for Australian residents and citizens (262). For example, there is a limit on coverage for pharmaceuticals in the standard package. Cost was also an important barrier described by community focus group participants, particularly regarding access to travel health clinics and some travel vaccinations, which are not covered by Medicare or the PBS. Although specialist travel health clinics are an ideal source of advice especially for more complex cases, there is an out-of-pocket cost barrier. Therefore, most travellers will continue to rely on GPs for travel health advice, even if they are aware of the benefits of professional clinics, and even if the language and cultural barriers for professional clinics are removed. Therefore, it is also important that GPs who serve the Chinese community be trained in the provision of appropriate travel health advice for Chinese VFR travellers, especially in light of the knowledge deficits found in GPs in previous studies, as mentioned above.

Although some of the travel health advice that focus group participants received from friends and relatives in China was useful, the reliance on non-professional advice can sometimes mean misguided risk assessment and inaccurate or inadequate travel health preparations, with an adverse effect on travel health outcomes (69). For example, some focus group participants were misinformed that taking certain Chinese medicines can prevent influenza or food poisoning, or were encouraged to travel to China during a major outbreak. Furthermore, focus group participants who relied on health advice from non-professional sources generally believed this was adequate, and did

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not appreciate the benefit of seeing a health professional for travel advice. Therefore, education programs to increase the awareness of the need for travel health preparations also need to stress the importance of obtaining reliable advice from healthcare professionals. This study also found that some Chinese VFR travellers concurrently seek information from both reliable and unreliable sources as part of their ‘research’. For example, they can access both information from government health departments and hearsay found on the internet, such as discussions not involving health professionals on internet forums and social media. It is important that education programs address the need to trust only reliable sources of information. On the other hand, as Chinese VFR travellers strongly trust advice given by family and friends, such advice should not simply be dismissed by health professionals if there is to be effective discussion of travel health issues. Instead, health professionals should encourage VFR travellers to discuss all advice they have received, and correct any misconceptions from there. It may also be useful to distribute Chinese language pamphlets for VFR travellers to give to family and friends in China, so they can be educated too. This would be especially helpful due to advice from family and friends being especially persuasive in Chinese VFR travellers.

Finally, the attitude of stigmatization of migrants being unhygienic and a source of contagion, often unconsciously held, must also be acknowledged as an important barrier for VFR travellers seeking professional pre-travel health advice. This is especially important, as the perception of discriminatory attitudes among health professionals towards migrants can further alienate migrants from seeking health care, including pre-travel consultations. Whilst this study has presented findings regarding the risk of VFR travel to public health in Australia and highlighted the need for appropriate interventions, it should be emphasized that xenophobic, stigmatizing attitudes towards migrants and VFR travellers should be discouraged.

5.3.4 Issues specific to international students require tailored travel health messages

Since Chinese international student VFR travellers have been found to share a lot of common issues with other Chinese VFR travellers, education campaigns targeting Chinese VFR travellers (as well as VFR travellers more generally) would also be useful in this population. Similar to other Chinese VFR travellers, there is a need to promote the use of travel health services and pre-travel health preparation among international students. Education campaigns targeting food safety, preventive health behaviours during outbreaks and misconceptions associated with vaccinations are also needed among this population. High use of the internet and social media for information gathering

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by international students means that these channels would be viable methods for education delivery to students, more so than for other Chinese VFR travellers. This will be further discussed below.

Chinese international students would also benefit from targeted education campaigns to address issues particularly relevant to this population. Obtaining travel health advice from a doctor and receipt of relevant vaccination may be particularly costly for international students. Education campaigns for this population should emphasise the benefits of such preparation, and clearly explain how the benefits of being adequately vaccinated for travel outweigh the costs. Promotion of annual influenza vaccination for this group is particularly warranted considering their high rates of travel to China during the peak influenza season. Despite the unavailability of the northern hemisphere formulation of the influenza vaccine in Australia (269), the southern hemisphere formulation of the influenza vaccine would still be beneficial as it would protect against at least some circulating strains (270). Interest in the availability of the opposing hemisphere formulation for the purpose of traveller vaccination has been reported in the literature (355-357) and would be beneficial to international student travellers.

Chinese international students often view VFR travel as simply returning home, and therefore of no health risk. Education for these travellers should specifically address this view, by pointing out issues such as changed immunity, and their new responsibility, as international students who can potentially facilitate the spread of diseases across international borders, to protect themselves from infection. Chinese international students also strongly depend on their parents for travel health advice, and in some cases, even making the decision whether to receive a vaccine or whether to travel to China during an outbreak. Pamphlets could be provided in Chinese for students to take home to China, to discuss with their parents, so that both parties can be educated, similarly to what has been implemented in various school vaccination programs (358-360). Issues to be discussed can include the safety, efficacy and necessity of vaccines, and the risk of underestimating the danger of travel in the early stages of outbreaks.

5.3.5 Web-based information and social media may be effective channels for targeting younger VFR travellers, including international students

A proclivity among younger Chinese VFR travellers towards web-based health information and the use of social media to discuss travel with their networks presents an opportunity to deliver targeted messages to this population using these platforms. From the focus group discussions, Chinese VFR travellers who rely on the internet for health information are mostly getting advice from non-

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professional sources, including via social media discussion. As previously discussed, this can lead to suboptimal pre-travel preparations (69). In fact, concerns regarding the lack of reliability of health information on social media, and the potential for harmful health consequences from misleading information, have been reported in the literature (272). The adequate delivery of professional web-based travel health information (e.g. from government health departments, the CDC or WHO), including the dissemination of travel health messages through social media, can help in adding to the amount of professional and reliable information available through the internet (271). Dissemination through social media is also an active delivery method with a potentially greater reach than static web pages.

There has recently been some interest in the use of social media for travel health promotion (271, 272). Use of web-based health information resources and social media for health promotion purposes remains a relatively new development, but evidence of their effectiveness from several studies is encouraging. A systematic review of programs that use the online environment to disseminate health behavioural change interventions found “very modest evidence that interventions incorporating online social networks may be effective”, based on the results of ten studies (361). Nine out of the ten studies reported significant improvement in certain measured aspects or outcomes, but, in general, the effect sizes of behaviour change were small in magnitude. A study of a weight loss program for college students delivered using Facebook and text messages found significant weight loss success in the intervention arm, compared to those on the waiting list (362). In addition to the delivery of health interventions through websites and social media networks, smartphone applications (apps) may also be a useful mode of delivering travel health education to young adult travellers. A focus group study in the UK found that young adults showed some interest in using smartphone apps to support health behaviour changes (363). Other studies also suggest that university-educated people are more likely to use digital technologies to obtain health information, for example, to search for online health information sources (364) and download health-related smartphone apps (365), compared to those with lower educational attainment. These studies and the data derived from the student focus groups provide evidence that digitally based interventions, including delivery via websites, social media networks and smartphone apps, may be a particularly effective and viable method for delivering health messages to international university students.

Whilst the CDC already has travel health specific pages on both Twitter and Facebook (272), and the Australian Government also provides updates of travel advisories on Twitter (108), such information is not likely to reach the bulk of Chinese VFR travellers, as the majority of these

147 Chapter 5: Conclusions

travellers do not actively seek out travel health information. The fact that these resources are provided in English only and do not have a specific focus on China further diminish their potential interest to Chinese VFR travellers. For the purpose of health promotion for Chinese VFR travellers including international students, social media pages specifically dedicated to issues surrounding VFR travel to China (e.g. on Facebook, Twitter and the Chinese Weibo) can be set up by organisations concerned about this population, including universities, the Australian Government Department of Health, international health agencies like the WHO, and other professional groups. These should be ideally provided in Chinese. These can be used to connect with Chinese VFR travellers, and information can then be disseminated via these connections. Sharing information is a common use of social media (271, 366-368). Therefore, such information may then be further shared and disseminated, via social media, to even more potential Chinese VFR travellers. As social media is also interactive (366, 368), online discussions, moderated by health professionals, can be used in specific campaigns to educate travellers regarding particular health issues or to correct particular misconceptions (271). Many social media platforms also provide opportunities for paid advertising which can be used to specifically target defined demographics (369, 370), for example, young adults living in Australia who already receive information that is targeted to ethnic Chinese (and who therefore are likely to be Chinese). Such targeted advertising is worth considering to address the fact that, due to their low risk perception, many VFR travellers will not actively seek out travel health information.

5.3.6 Addressing Chinese VFR travel health issues is important for public health in Australia

As discussed in Chapter 4, several possible agents for future outbreaks are already circulating in wildlife in China as well as causing occasional human cases (302-304, 316). It is possible that mutations may occur that facilitate efficient spread of these agents, or other newly emerged pathogens, between humans and potentially cause a pandemic (11, 100). The 2013–2014 influenza A/H7N9 outbreak in China is a contemporary reminder of this reality (313). Of the currently circulating pathogens with pandemic potential, H5N1 is most concerning due to its high mortality rate in humans (300). As the 2003 SARS pandemic showed, a pandemic can be established within a short time frame, facilitated by the movements of travellers (2, 3). In countries such as Australia, with a large ethnic Chinese population, Chinese VFR travellers can potentially be a crucial source for the introduction of pathogens originating in China. This was highlighted by the example of the SARS epidemic in Canada, where the index case was a returned Chinese VFR traveller (12, 97).

148 Chapter 5: Conclusions

The implementation of border screening measures at airports during outbreaks of international concern is especially important for a country like Australia, with no land borders with any other country, but with frequent connections to many other parts of the world via air travel. However, border screening measures, which aim to detect symptoms of the outbreak illness in travellers entering the country (e.g. at international airports), are limited in effectiveness for several reasons (371), including the inability to detect asymptomatic cases such as those still in the incubation period or partially treated patients (372, 373). Therefore, they realistically cannot prevent pandemics from entering Australia for extended periods of time (283). However, they may delay the introduction of the pandemic by one or more weeks to allow Australia to be better prepared. This has been demonstrated via mathematical modelling (278), as well as in modest evidence obtained from the 2009 H1N1 pandemic (282). This small delay may be crucial to the outcome of any pandemic in a given country, as demonstrated by the SARS pandemic. Countries like Vietnam, Singapore and Canada, where SARS was introduced very early in the course of the global pandemic, recorded the highest number of cases outside China (284, 374).

As border measures cannot effectively prevent pandemics from entering Australia for long periods of time, reducing opportunities for pandemics to enter Australia in other ways is just as important. Chinese VFR travellers are potential sources in the introduction of pathogens with pandemic potential from China to Australia. Encouraging travellers, particularly VFR travellers, to adopt appropriate travel health behaviours is therefore a key factor in reducing the importation of infectious diseases into Australia and is important for national disease control. Appropriate travel health behaviours include the practice of precautionary behaviours during travel, especially during outbreaks, for example, not consuming street food or uncooked food, avoiding live poultry markets, washing hands frequently and using face masks (164, 167, 285), as well as cancellation or delay of non-essential travel during outbreaks. Concerningly, the focus groups found that the aforementioned practices have often not been previously adopted. This further highlights the importance of education interventions to encourage such behaviour in Chinese VFR travellers.

5.3.7 Future research questions

This research was able to identify many barriers to the uptake of optimal travel health preparations, including the seeking of professional travel health advice and vaccination, for Chinese VFR travellers. It also uncovered many important knowledge deficits and misconceptions regarding the risks associated with travel to China and recommendations to reduce those risks. However, a qualitative study, by design, is not able to determine how common specific knowledge, attitudes

149 Chapter 5: Conclusions

and practices are in the Chinese VFR population, nor the frequency with which Chinese people in Australia encounter barriers to health service use. Quantifying the barriers to uptake of pre-travel health advice is the next step in understanding the travel health needs of this population, and will be useful for prioritising future interventions. Furthermore, many of the findings of this study regarding the beliefs and practices of Chinese VFR travellers potentially merit further qualitative study, such as an in-depth study regarding the culturally-based attitudes behind the health beliefs identified. Such information, if available, would further inform effective educational interventions. Travel health behaviours identified in this study, particularly surrounding the decision to obtain professional travel health advice or not, and how travellers view VFR travel differently from tourist travel in this regard, should also be studied in further detail such as in a dedicated qualitative study.

International students have been found in the focus groups to have some unique issues compared to other Chinese VFR travellers. Therefore, they will also merit dedicated study in future quantitative research. In such future studies, both general VFR travel-related issues and issues specific to international students should be explored. In particular, there should be exploration of the use of social media and obtaining advice from parents in China.

The role of Australian Chinese VFR travellers in the importation of infectious diseases from China

The outbreak risk analysis contained in this thesis highlights the important role that Chinese VFR travellers may play in the importation of future emerging infectious diseases into Australia, and sheds light on the aspects of VFR traveller health behaviours that may influence their risk of infection and the subsequent importation of diseases with outbreak potential. The logical next step would be a quantitative study focused specifically on Chinese VFR travellers’ health behaviour in relation to outbreaks in China, to quantify which issues are most prevalent and should therefore be addressed as priorities. This would be especially useful since, although there have been many published studies regarding VFR travellers in general, none have focused on travel behaviour during outbreaks.

5.4 Strengths and limitations of this research

Although there are already many published studies regarding VFR travellers specifically or providing substantial findings regarding VFR travellers, this is the first study into Chinese VFR travellers living in Western countries. Although this study found that Chinese VFR travellers share

150 Chapter 5: Conclusions

many issues with other VFR travellers, there are certain aspects of their travel health behaviour that are specifically related to Chinese culture, such as the use of Chinese medicine. This study was thus the first to explore these themes in the context of VFR travel.

Although a number of quantitative studies of VFR travellers have reported important deficits in health knowledge, and major concerns about the attitudes and practices of these travellers, this qualitative study has been able to explore these issues thoroughly, including the underlying reasoning behind some important beliefs and behaviour. Through the use of qualitative research methods, many potential enablers and barriers influencing appropriate travel health preparation were identified and misconceptions and knowledge deficits were more thoroughly explored. This rich and in-depth information can inform future education interventions, to a much greater extent than quantitative data alone. As such, this research illustrates how qualitative research can uniquely benefit public health knowledge and practice. However, due to the qualitative nature of the study, the proportion of participants with particular views, behaviours and level of understanding of travel health risks was not able to be determined.

A relatively high number of community members and students participated in this qualitative study. Use of both community recruitment and the recruitment of international students allowed the exploration of issues surrounding Chinese VFR travel among both older and younger demographics. Even though the international student participants were staying in Australia on a time-limited visa rather than as permanent migrants, there was still an opportunity to explore issues that are likely to be relevant to all young Chinese VFR travellers, for example, advice from parents and the use of internet websites and social media for information gathering. Importantly though, second generation Australian Chinese were not represented. Given that second generation immigrants grew up in Australia, they are likely to be culturally quite different to both first generation immigrants and Chinese international students and less likely to have the same perceived familiarity with China. Previous research on second generation migrants has found that, although in some respects their health behaviour and health risks are more similar to the host country’s mainstream population than to first generation migrants (375, 376), they still have certain health risks specific to their ethnic status (377-379). Furthermore, they can have a higher level of undesirable outcomes in certain aspects of health and disease compared to either the host country’s mainstream population or first generation migrants. This has been found to be the case in studies on general mortality risk, poor dietary practices, diabetes and obesity, for example (380-382). Comparison of the results presented in this thesis with additional studies among second generation

151 Chapter 5: Conclusions

Australian Chinese VFR travellers would further our understanding of the risk and health perceptions of all Chinese VFR travellers.

The international student study focused exclusively on return travel to China by Chinese international students studying in Australia. This study is the first to explore Australian Chinese international students as VFR travellers. As international students are known to undertake a high volume of VFR travel (71), and Chinese international students have a sizeable presence in Australia (67, 244), addressing international student-specific issues will be an important component of any comprehensive strategy to address Australian Chinese VFR travel health. All participants from the international student focus groups were recruited from one single university, UNSW Australia. Chinese international students studying at other Australian universities, particularly regional universities, may face different issues as a result of studying in a different environment. However, UNSW Australia is a major university in Australia, with a substantial population of Chinese international students. Therefore, the study population was still considered to be reasonably representative of Chinese international students in Australia in general.

The focus on travel health behaviours of VFR travellers and their association with outbreaks is a unique and novel study; this issue is not currently explored in detail in the literature. A limitation of the focus group component of the outbreak study is that it was conducted as part of a wider focus group study on VFR travel to China generally, rather than as a focus group study entirely on outbreaks. As a result, there was less time available to focus on outbreak related topics.

Finally, both literature reviews (Chapters 1 and 4) included only articles published in English language journals, as the researcher was not familiar enough with Chinese medical terminology to adequately review Chinese language journals. However, the focus of the literature reviews was on the behaviour of international travellers and infectious risks pertinent to international travellers, and articles relating to such topics are most likely to be published in English, as opposed to Chinese. Whilst some articles on Chinese health beliefs and practices may have been published in Chinese, the English language articles reviewed already provided quite a comprehensive picture regarding issues potentially pertinent to VFR travel health, such as vaccination and Chinese medicine use. Grey literature was also not reviewed, however, the bulk of grey literature in this area consists of quantitative surveillance data, which was not the focus of these literature reviews.

152 Chapter 5: Conclusions

5.5 Conclusions

The aim of this thesis was to explore in depth the important travel health issues relating to Australian Chinese VFR travellers, particularly in relation to preventing acquisition of infectious diseases and preventing the importation into Australia of infections with outbreak or pandemic potential. This research fills a major gap in knowledge internationally in a very high-risk group of travellers. The study identified and explored suboptimal travel health behaviour in this population, including low risk perception and awareness, poor knowledge of potential travel health risks, inadequate travel health preparations, and risk behaviour during travel generally and during outbreaks. The international student focus groups also identified issues specifically important to international students, as well as unique interventional methods that can be used to reach this population. The findings contained in this thesis can be used to inform future education interventions. The outbreak risks analysis highlighted the importance of addressing Australian Chinese VFR travel health issues as a high priority, especially in relation to outbreaks. As the first study of Chinese VFR travellers internationally, this thesis has highlighted many important and unique issues regarding this population, and their importance to public health outcomes in Australia and globally means that further studies in this population are warranted. As emerging infectious diseases continue to threaten the world, more targeted prevention in high-risk groups will be important for disease control efforts.

153 Appendices

Appendix 1 Literature review search strategy

The search strategy used for the literature review contained in Chapter 1 of the thesis included searching the MEDLINE database for articles using a list of keywords and their associated MeSH headings, as well as the identification of additional publications using the reference lists of relevant articles found using MEDLINE as described. Only papers written in English were included. Relevant sources of information from the grey literature, including information from the WHO, CDC and Australian government relating to travel to China, as well as news reports of outbreaks in China during the period of candidature, were also reviewed, and included where relevant.

Articles relating to general VFR travel health issues were identified by searching using the keywords “VFR” or “visiting friends and relatives” AND (i.e. combined with) the keyword “travel”. Both the keywords themselves and their associated MeSH headings were used in the search. A similar strategy was used to identify articles relating to ethnic Chinese and their travel health issues, by using the keywords “travel” AND “Chinese”, “China” or “Hong Kong”. Articles relating to outbreaks of influenza and SARS were searched for using the keywords “China” or “Hong Kong” AND “SARS”, “H5N1”, “H7N9”, “avian influenza” or “influenza” AND “1957” or “1968”. Articles relating to other important diseases were searched for using the keywords “China” or “Hong Kong” AND the name of the disease. Diseases were identified from information from the CDC, WHO and the Australian government, and diseases considered highly relevant for travellers to multiple parts of China were included. These diseases included hand, foot and mouth disease, hepatitis, tuberculosis, Streptococcus suis, dengue fever, chikungunya, Japanese encephalitis, plague and some parasitic infections. Articles relating to health beliefs were searched for using the keywords “China” or “Hong Kong” AND “attitude$”, “behaviour$”, “vaccine$”, “HIV”, “sexually transmitted diseases”, “Chinese medicine” or “self medication”.

154 Appendices

Appendix 2 Focus group guide, demographic survey form, and participant information and consent form

Theme 1: Preparing for travel.– general travel health attitudes and behaviour

Firstly, I would like to start a discussion about how you prepare for your overseas travel and how you stay healthy while you are away.

Possible prompts to be used by facilitator:

• Question about what they usually do • Before you travel, do you get travel health advice? o (to Hong Kong / mainland China?) o (to other destinations?) o Why is that the case? o Why not? • Who do you get your travel health advice from? Why? • What health precautions do you take when travelling overseas? By precautions, I mean things you do to prevent exposing yourself to risks, for example, having vaccinations. o (to Hong Kong / mainland China?) o (to other destinations?) • Have you ever used professional travel health services, such as a travel health clinic? o Why is that the case? o Why haven’t you?

Theme 2: Vaccinations

Would you get vaccinated before travelling to China?

Possible prompts:

• Did you recently discuss with your GP regarding vaccinations, for example, during a recent check-up? Did you have any problems with that? Did your GP have any problems? • Do you know if you have had all the 'basic vaccinations' done? • Have you ever been vaccinated as part of preparing for travel? • Have you ever been vaccinated as part of preparing for VFR travel? • Would you get vaccinated before travelling to Hong Kong / mainland China if advised to? Why or why not? • What are some pros and cons of vaccination that you know about?

155 Appendices

Theme 3: Health-related attitudes and behaviour towards travelling to mainland China and Hong Kong

What health risks do you perceive in travelling to mainland China / Hong Kong, and what precautions will you take?

Possible prompts:

• What travel health issues are you aware of in relation to travelling to mainland China / Hong Kong? • What are some diseases that you know of that people travelling to mainland China / Hong Kong are at risk of acquiring during their journey? • Are you concerned about acquiring infectious diseases during your travel to mainland China / Hong Kong? Why or why not? • Have any of you travelled outside the major cities whilst in China? If so, are you aware of any particular health risks of such travel, and have you taken any appropriate precautions? • How do you feel about health care in mainland China / Hong Kong? • If you fell ill during VFR travel, would you seek treatment in China? Why or why not? • Would you prefer receiving medical treatment in mainland China / Hong Kong rather than Australia?

Theme 4: Destinations and activities during VFR travel

Where do you stay when in China, and what do you do on a typical trip?

Possible prompts:

• Which part(s) of China do you usually travel to during your VFR visits? • What activities do you get involved in during VFR travel? • Where do you stay during VFR travel? • Do you come into contact with animals during VFR travel? • Tell me about your eating habits during VFR travel. Is there any food that you would not eat in Australia that you would eat during VFR travel?

Theme 5: Awareness of major travel health issues in destinations

What are some major health issues that you are aware of pertaining to China?

Possible prompts:

• Are you aware of the major outbreaks of influenza and SARS that have affected China over the past 15 years? Tell me what you know.

156 Appendices

• Did recent outbreaks in China affect how you plan your travels? • Are you aware of the risks associated with travel during outbreaks, and the appropriate precautions to take?

Theme 6: Attitudes towards and use of traditional Chinese medicine

What are your thoughts on the use of traditional Chinese medicine?

Possible prompts:

• Do you use traditional Chinese medicine? Why or why not? • If you use traditional Chinese medicine, do you self-medicate or do you see a professional Chinese medicine practitioner? • When would you use traditional Chinese medicine? • How effective do you think traditional Chinese medicine is? • Are you more likely to use traditional Chinese medicine when in Hong Kong / mainland China?

Theme 7: Self-medication

When you experience minor illnesses in Australia, for example, fever, diarrhoea or respiratory infection, what do you do?

Would you do any differently in China?

What are your thoughts on buying medication over the counter and treating yourself without seeing a doctor?

Possible prompts:

• Would you say that self medication is more available in mainland China / Hong Kong compared with Australia? • Would you self-medicate if you fell ill whilst you are in mainland China / Hong Kong? If so, how would you self-medicate (for example, taking a friend's tablets)? • What are your thoughts on self-medication? • Would you stock up on prescription medication whilst in China / Hong Kong?

157

Approval No 2012-7-40

PARTICIPANT INFORMATION STATEMENT AND CONSENT FORM

Australian Chinese travellers visiting friends and relatives: New approaches to understanding and reducing infectious disease risks

What is the study? Travel is a major way in which infectious diseases can spread globally. Australian Chinese are one of the largest ethnic groups in Australia and many migrants and their children travel back to China to visit friends and relatives. Australia has very low rates of infectious disease, and illness in travellers returning to Australia is common. Researchers from the University of New South Wales are conducting a new study to travel health issues amongst Chinese Australians.

You are invited to participate in a travel health study. In this study we will explore travel health issues, particularly in relation to visiting friends and relatives in China and Hong Kong. You were selected as a participant in this study because you responded to an advertisement seeking Australian Chinese who have travelled to mainland China or Hong Kong in the past 18 months to visit friends or relatives.

What will I have to do? If you decide to participate, we will ask you to take part in a focus group of approximately two hours duration. It will involve a group of a maximum of 10 people, plus a facilitator. The facilitator will ask some questions regarding the topics we wish to explore, and the group will discuss these topics.

We do not expect that you will receive any harm or risk as a result of this study. You may not receive any direct benefit from this study. Participation in this study is voluntary.

Confidentiality and privacy Focus group conversations will be recorded, and will be then transcribed manually. This data will be used for our research and may be published in the future. In any publication, information will be provided in such a way that you cannot be identified. Any information obtained in this study that can be traced back to you will remain confidential and will not be disclosed, unless with your permission, or when required by the law.

Remuneration If you participate in the study, you will receive a $30 gift card.

Further Information If you have any questions, please feel free to ask us. If you have any additional questions later, principle investigator Chun Ma (Phone 0422707170) will be happy to answer them. Complaints may be directed to the Ethics Secretariat, The University of New South Wales, SYDNEY 2052 AUSTRALIA (phone 9385 4234, fax 9385 6648, email [email protected]). Any complaint you make will be investigated promptly and you will be informed out the outcome.

Your consent Your decision whether or not to participate will not prejudice your future relations with the University of New South Wales. If you decide to participate, you are free to withdraw your consent and to discontinue participation at any time without prejudice.

You will be given a copy of this form to keep.

PICF version 2: 12th October 2012 Page 1 of 3

THE UNIVERSITY OF NEW SOUTH WALES

Australian Chinese travellers visiting friends and relatives: New approaches to understanding and reducing infectious disease risks

CONSENT

You are making a decision whether or not to participate. Your signature indicates that, having read the information provided above, you have decided to participate.

…………………………………………………… Signature of Research Participant

…………………………………………………… Please PRINT name

Date: / /2012

.………………………………………………… Signature of Witness

…………………………………………………… Please PRINT name

Date: / /2012

PICF version 2: 12th October 2012 Page 2 of 3

THE UNIVERSITY OF NEW SOUTH WALES

Australian Chinese travellers visiting friends and relatives: New approaches to understanding and reducing infectious disease risks

REVOCATION OF CONSENT

I hereby wish to WITHDRAW my consent to participate in the research proposal described above and understand that such withdrawal WILL NOT jeopardise any treatment or my relationship with The University of New South Wales.

.……………………………………………………. Signature

…………………………………………………… Please PRINT Name

Date: / /2012

The section for Revocation of Consent should be forwarded to Chun Hin Ma, School of Public Health and Community Medicine, Level 2, Samuels Building, the University of New South Wales, Sydney, NSW 2052.

PICF version 2: 12th October 2012 Page 3 of 3 Focus Group Questionnaire Demographic and Other Details Collection

How old are you?  18-24 years  25-34 years  35-44 years  45-54 years  55-64 years  65 years or above

What is your gender?  Female  Male

What is your highest completed educational qualification? (Please tick one box)  None  School certificate  High school certificate  Certificate/diploma  University degree/equivalent

Are you employed? (Please tick one box)  No  Yes Please specify type:  Self employed Full time Casual Part-time

Are you studying? (Please tick one box)  No  Yes Please specify type: Full time Part-time

Who do you live with?  Parents  Spouse or Partner  Children  Friends  I live alone  Other (Please Specify ...... )

How long have you been living in Australia for?  Less than 1 year  1-5 years  5-10 years  More than 10 years  I was born in Australia

1 Since you have lived in Australia, how many times have you been back to China?...... Do you generally seek travel health advice before travelling to China?  Yes, from a professional travel health service  Yes, from a general practitioner  Yes, from family and friends  Yes, from the internet  No

Do you generally seek travel health advice before travelling to other countries (other than China)?  Yes, from a professional travel health service  Yes, from a general practitioner  Yes, from family and friends  Yes, from the internet  No

What is your personal experience regarding professional travel health services?  Very positive  Positive  Mixed  Negative  No personal experience yet

Have you ever got sick during or after travelling to China, when you were living in Australia?  Yes, and it was a major illness requiring seeing a medical professional  Yes, but it was only a minor illness not requiring seeing a medical professional  No  Unsure

How do you rate the health risks of travelling to China for yourself?  Very Safe  Sufficiently safe  Not so safe  Not safe at all  Don’t know

How much would you say you know about travel health?  Nothing at all  A little  A moderate amount  A lot

What additional information would you like most to have on travel health when visiting friends and relatives? ………………………………………………………………………………………………………………………………………………………………… ………………………………………………………………………………………………………………………………………………………………… ………………………………………………………………………………………………………………………………………………………………… …………………………………………………………………………………………………………………………………………………………………

2 Appendices

Appendix 3 Publication arising from this thesis

163 Travel Medicine and Infectious Disease (2015) 13, 285e294

Available online at www.sciencedirect.com ScienceDirect

journal homepage: www.elsevierhealth.com/journals/tmid

FIRST LOOK - STUDENT RESEARCH Chinese travellers visiting friends and relatives e A review of infectious risks Tara Ma a,*, Anita Heywood a, C. Raina MacIntyre a,b a School of Public Health and Community Medicine, UNSW Australia, Kensington, NSW, Australia b National Centre for Immunisation Research and Surveillance (NCIRS), The Children’s Hospital at Westmead, Westmead, Australia

Received 13 May 2014; received in revised form 31 March 2015; accepted 4 May 2015 Available online 14 May 2015

KEYWORDS Summary Background: Travellers are potential vectors in the transmission of infectious dis- Travel medicine; eases across international borders. Travellers visiting friends and relatives (VFR) have a partic- China; ularly high risk of acquiring certain infections during travel. Chinese VFR travellers account for Hong Kong; a substantial proportion of all travel in Western countries with high migrant populations. Infectious diseases; Methods: A literature review was undertaken regarding major infectious disease risks for VFR Emerging infectious travellers visiting China. This included an examination of the previous pandemics arising in diseases China, the likelihood of future outbreaks in China from H5N1 and H7N9 avian inﬂuenza viruses, the potential role of travellers in disease transmission, and the special risks for VFR travellers. Results: China has been the origin of several inﬂuenza pandemics in past few decades, and the origin of several emerging infectious diseases with pandemic potential, including SARS. Travel to and from China has the potential for global spread of emergent infectious diseases, as seen in the SARS outbreak in 2003. For VFR travellers, the risk of other infectious diseases may also be greater in China compared to their countries of migration, including hepatitis A and B, dengue fever, typhoid, and other diseases. Conclusions: VFR travel to China may be associated with increased risk of acquiring a range of infectious diseases, and also poses a potential risk for importation of future pandemics to other countries. Chinese VFR travellers need to be cognisant of these risks and health professionals should consider educational interventions to minimise these risks. ª 2015 Elsevier Ltd. All rights reserved.

* Corresponding author. School of Public Health and Community Medicine, University of New South Wales, Kensington, NSW, Australia. Tel.: þ614 2270 7170. E-mail addresses: [email protected] (T. Ma), [email protected] (A. Heywood), [email protected] (C.R. MacIntyre). http://dx.doi.org/10.1016/j.tmaid.2015.05.004 1477-8939/ª 2015 Elsevier Ltd. All rights reserved. 286 T. Ma et al.

1. Introduction Hong Kong accounts for a significant proportion of all overseas travel. Of resident Australian departures in 2010, In light of the recent outbreak of human H7N9 influenza 4.7% were to mainland China and 3.0% were to Hong Kong cases in China [1], concerns of an influenza pandemic have [24], of those 28.9% were for the purpose of visiting friends again been heightened. Emerging infections, once they and relatives [25]. Chinese VFR travellers contribute sub- arise, can spread rapidly around the world via international stantially to the volume of travel to China from Australia travel, as was the case with Severe Acute Respiratory and other Western countries. Syndrome (SARS) [2e4]. Travellers are an important vector This review describes recently emerged and travel- in the global spread of infectious diseases, especially during associated infectious diseases originating from China and outbreaks. Historically, China has been a major source of the risk to international travellers, particularly those emerging infectious diseases of international concern [5]. visiting friends and relatives. Travellers play a pivotal role The easing of government-imposed travel restrictions has in the spread of infectious diseases across international resulted in a rapid expansion of international travel to and borders, and infectious disease risk awareness, preventa- from China over the last decade. In 2012, outbound Chinese tive practices and behaviour modification are crucial to the were the largest tourist source nation and China ranked comprehensive control of infectious diseases on a global third in the number of inbound tourist arrivals, and is ex- scale. Awareness of emerging infectious disease risks is pected to receive the largest number of international ar- important for travellers to China and for health pro- rivals by 2020 [6]. With this high and increasing volume of fessionals providing pre-travel health advice to Chinese VFR cross-border movements, the global spread of infectious travellers. diseases from China warrants consideration. Travellers are at risk of acquiring and transmitting in- 2. Methods fectious diseases, both in the country to which they travel and upon their return. The risk of infectious disease and A literature review was conducted of infectious disease subsequent importation of disease is greater in travellers risks in China, and with a focus on [1]: recent outbreaks visiting friends and relatives (VFR) travellers [7e9]. VFR including the 2003 SARS outbreak and the H5N1 and H7N9 travellers commonly acquire similar infectious diseases as avian influenza outbreaks and [2] diseases identified as do other travellers [10], but they may be especially at risk highly relevant for Chinese VFR travellers. Only diseases for certain diseases [11]. Whilst there is no standard defi- identified as highly relevant for Chinese VFR travellers, nition of a VFR traveller, the term most commonly refers to either due to a known increased risk for VFR travellers in both first and second generation immigrants who are general [26] or relevance across multiple urban and rural ethnically distinct from the majority population of their regions of China, were explored. The diseases identified country of residence, who return to their country of origin include hepatitis A and B, tuberculosis, malaria and to visit friends and relatives [12,13]. The term generally typhoid. Hepatitis A and B and tuberculosis are prevalent refers to those travelling from high income to lower income across China [27,28], and tuberculosis, malaria and typhoid countries [12] where their risk of infectious diseases are are all known to disproportionately affect VFR travellers greater [7e9]. A range of factors related to higher risk of [7]. exposure and lower uptake of preventative health mea- The Medline database Published literature were sures contribute to the higher risk in VFR travellers [11]. retrieved from the Medline database for each included While there are no data on the travel patterns and travel disease using a combination of keywords and MeSH head- health practices of Chinese VFR travellers, evidence sug- ings, for example, ’SARS’ and ’China’ or ’Hong Kong’. Ar- gests that the proportion of Asian travellers seeking pre- ticles were assessed using their titles and abstracts and travel health information is lower than that of Western selected for possible inclusion based on their relevance. travellers [14e16]. Articles potentially relevant to travel health, articles dis- There is a strong correlation between migration and VFR cussing the spread of the outbreak, and articles discussing travel and an increase in global migration, coupled with the potential future outbreaks in China or Hong Kong were affordability of travel for migrants and their children, is considered for inclusion. All study designs, including review contributing to the increase in the proportion of travel for papers, were considered for inclusion. As H7N9 was a new the purpose of visiting friends and relatives [17]. Globally, outbreak virus that had only caused outbreaks in China, no international travel for the purpose of visiting friends and restriction of the search to articles on China was applied. relatives accounted for a quarter of international tourist Articles published before 31 March 2014 were included. arrivals in 2012 [6], particularly originating from Western Studies were restricted to English language. References of countries [18,19]. In 2011, 46% of outbound international all relevant articles, including reviews, were checked to travel by US residents was to visit friends and relatives [18], identify additional studies. whilst the main purpose of travel for 23% of Australian We also searched the grey literature, including the WHO, resident departures in 2012 was for the purpose of ’visiting CDC and Australian government websites for information on friends and relatives’ [19]. Ethnic Chinese are one of the infectious risks of relevance to Chinese VFR travellers. In largest cultural groups in many Western countries including addition, a general overview of other infectious disease Australia [20], Canada [21] and the USA [22] and was the risks present in China, according to the WHO, CDC and largest source country for migration to Organisation for Australian government websites, was prepared. To provide Economic Co-operation and Development (OECD) countries a geographical reference for readers unfamiliar with the in 2011 [23]. In Australia, travel to mainland China and location of Chinese provinces, maps showing the origins of Chinese travellers visiting friends and relatives 287 the recent SARS and avian influenza outbreaks were pre- H7N9 has a high case-fatality rate, estimated at 34% pared. Maps of selected diseases which have a geographi- based on data up to December 2013 [1]. The majority of cally uneven distribution were also prepared from data known cases and deaths have been in older adults, with a identified in the literature review indicating affected median age of approximately 60 years, with underlying provinces. medical conditions [39,40]. However, there have been reports of cases in children, one asymptomatic child in Beijing 3. Pandemic threats in China tested positive for H7N9 [36], and two mildly symptomatic cases in children aged under 5 years [39]. Therefore, it is not yet known if H7N9 is more severe in certain sub- China has been the source of some of the most important populations, nor the extent of asymptomatic infection in pandemics of recent decades, including Severe Acute Res- the wider population. Also, whilst most cases have had piratory Syndrome (SARS) and numerous influenza pan- known animal contact, human to human transmission could demics [5]. In addition, H5N1 and H7N9 have recently not be ruled out in a small number of cases [1]. To date, emerged in China as potential global threats. there have been no known cases involving VFR travellers. As with all other new zoonotic origin influenza infections 3.1. Lessons from SARS associated with a high mortality rate, travellers to China are advised to be particularly vigilant about their personal Human cases of SARS originated in Guangdong province, hygiene, and avoid direct contact with animals in live southern China in November 2002. Able to efficiently markets [41]. In October 2013, the Chinese National Influ- spread between humans, the SARS virus resulted in a enza Center announced the development of a vaccine for pandemic with significant morbidity and mortality [2]. The the new virus [42]. However the vaccine is not currently SARS coronavirus was of zoonotic origin [29] and Chinese available for travellers. wet markets were likely to have played an important role in the emergence of SARS. A similar virus was isolated in civet 3.3. Other avian influenza A subtypes cats and racoon dogs in wet markets in Guangdong province during the pandemic [30]. After the initial spread from The recent emergence of the H5N1, H7N2, H7N3, H7N7, mainland China to Hong Kong, air travel was central to the H7N9, H10N7, H10N8, H6N1 and H9N2 subtypes of avian- global spread of the SARS virus. As with other outbreaks of origin influenza viruses as human pathogens are of inter- newly emerged pathogens, infection control measures early national concern [30,43]. Importantly, two of the four in the pandemic were hampered by the lack of knowledge influenza pandemics of the past century originated in of the virus [31]. As a result, those countries with impor- China, and three of the four newly emerged subtypes also tations via international travel early in the pandemic, originated in China. before the virus could be properly identified and proper Of the avian influenza viruses that have recently infec- control measures were in place, observed the highest ted humans, the highly pathogenic avian influenza virus number of cases outside China, including Canada, H5N1 subtype (HPAI H5N1) has caused the most concern, Singapore and Vietnam [32,33]. VFR travel also played an due to multiple outbreaks in humans around the world, and important role in the SARS pandemic. The index case of a high mortality rate. In 2003e2013, globally there have SARS in Canada was a VFR traveller [34]. SARS demon- been 648 cases, including 45 from China, and 384 deaths, strated the importance of travellers in national disease including 30 from China [44]. HPAI H5N1 has caused out- control efforts aiming to prevent or delay the introduction breaks in multiple provinces of China [45,46]. However, of an emerging infectious disease and future pandemic there have been no known cases involving Chinese VFR planning. Part of that effort needs to be directed at VFR travellers. The crude mortality rate is around 60%, with the travellers and their role in spreading emerging infectious highest mortality rate, of greater than 70% in cases aged diseases across international borders. 10e39 years [47]. The HPAI H5N1 virus appears to have originated from Southern China (Fig. 1) [45]. Since 1999, 3.2. Avian influenza A (H7N9) HPAI H5N1 has been consistently isolated from animals in southern China, and is now considered endemic in poultry The recent human outbreak of avian influenza A subtype [48]. This virus is not capable of human-to-human spread H7N9 began in Eastern China in February 2013 (Fig. 1) and presently except in limited cases [30]. Concerns remain as of 27 January 2014, 239 cases including 53 deaths have that further genetic reassortment with human viruses, for been reported in multiple provinces throughout China [35]. example occurring in a pig, could lead to direct human to In January 2014, there was a spike in cases (at least 95 human transmission capabilities and global spread with cases in this month compared to 144 cases in the whole of significant global morbidity and mortality, as well as sub- 2013) but associated with a lower death rate [35]. The stantial economic impact [30,49]. reason for this is currently unclear. Sustained human-to- There are a few important differences between H5N1 human transmission of H7N9 has not been documented and H7N9 epidemiology. Whilst H7N9 has caused a much [35], but efficient human-to-human transmission through higher incidence of infections compared with H5N1 using further mutations or reassortment is a possibility [36], with the same timeframe, H7N9 cases tend to be in geographi- H7 viruses having tendencies towards genetic promiscuity cally contiguous areas, whilst H5N1 cases have spread [37]. In addition, H7N9 appears more transmissible to globally in a way consistent with wild bird migration and humans than H5N1 [38]. poultry trade patterns [50]. Whilst H5N1 is more often 288 T. Ma et al.

Fig. 1 Likely origins of the H5N1, SARS and H7N9 viruses [2,35,45]. acquired via close and high-risk contact with birds, H7N9 new, pandemic causing viruses [5,55,56]. There are various appears to be often acquired via only incidental contact reasons for this, including farming practices, close prox- [50]. For unknown reasons, whilst H7N9 avian influenza has imity of humans and livestock, and food preferences in mainly affected older individuals, especially those over 60 Chinese culture [5]. Practices potentially encouraging the years of age [39,40,43], H5N1 avian influenza has more development and spread of new strains of influenza and often affected younger individuals [43,51], especially those other viruses include duck farming on flooded rice fields under 18 years of age [52]. Therefore, VFR travellers at the close to human housing, live poultry markets and wet extremes of age should be especially cautious in the event markets, and the sale and consumption of exotic meats of avian influenza outbreaks. including snakes and civet cats, all potential sources of a There have also been reported cases of human infection range of zoonotic pathogens [5]. These are all long-held with avian influenza type H9N2 in Hong Kong, and H9-like cultural practices, deeply embedded in Chinese history illness in Guangdong province, but none have been fatal and culture [5]. Various provincial and local governments in [53]. In addition, there have been reports of H10N8 in- China have attempted to make changes to these practices, fections in China recently [54]. Since so many different such as requiring enhanced disinfection and regular closure avian influenza subtypes have been able to infect humans of wet markets to mitigate risks [57,58]. Whilst these directly, it must now be assumed that all subtypes of measures may be somewhat effective [57], they may not influenza viruses, including H1-15 and N1-9, have the po- significantly reduce the risks. For example, the Hong Kong tential to become the new pandemic strain [49]. This new government has ordered that certain animals including view of pandemic influenza means that there is now a much ducks, quail and geese be excluded from wet markets, and larger pool of precursor influenza viruses that may trigger a that all markets be simultaneously emptied and cleaned pandemic and the threat of avian influenza outbreaks in twice a month. However, even this has not been effective humans is ever-present. Awareness of the risk of highly in keeping H5N1 out of wet markets [58]. Radical changes pathogenic influenza should be raised amongst VFR travel- like permanently closing all wet markets are not generally lers to China and agencies and professionals dealing with considered a practical option. Banning the sale of live such travellers. Health professionals who may treat poultry, as practiced in Beijing, may not be effective, as returned Chinese VFR travellers should also be well illegal live poultry trade has continued [59]. As these informed regarding the latest outbreaks, so that prompt measures have been implemented regionally rather than diagnosis may be made in returning travellers. nationally, their effectiveness may also be further limited. With the continued potential source of zoonotic pathogens 3.4. Why is China the origin of so many pandemics? remaining, Southern China will continue to be a source for the emergence of epidemics in humans. Outbreak aware- The SARS, H5N1 and H7N9 pandemics have all originated in ness, and awareness of respiratory infection control pro- South-eastern China (see Fig. 1). It has been hypothesized cedures in the event of a new outbreak arising during that Southern China is an epicentre for the emergence of Chinese travellers visiting friends and relatives 289 travel, should therefore be important components of pre- pre-travel preparation program (including vaccinations) travel advice and education for Chinese VFR travellers. designed specifically with their destination in mind.

3.5. Wet markets - a special risk for VFR travellers 4.1. Viral hepatitis

Chinese wet markets have received particular attention Both hepatitis A and B are considered highly endemic in regarding their potential role in the emergence of infec- China [28]. In China, 9.8% of the population are carriers of tious diseases of pandemic potential [49]. Wet markets, the hepatitis B virus, and 3.2% of the population are carriers where live poultry and other animals are slaughtered and of the hepatitis C virus [63]. This high prevalence has sold to the public, are visited daily by large numbers of particular implications for travellers who may seek people and are common across China. Wet markets provide healthcare in China, either due to medical emergencies or an ideal environment for the emergence of new pathogens. planned medical tourism, including dentistry. There is a Numerous species of live and slaughtered animals are kept higher risk of exposure to unsafe blood and blood products in close proximity to each other and to humans, promoting in regional areas, which may pose a risk of hepatitis B, C genetic reassortment and recombination between patho- and E as well as other blood-borne viruses [64]. As hepatitis gens originating from different species and are easily A is transmitted via the faecal-oral route, VFR travellers transmitted to humans, who are also present in great who are more likely than tourist travellers to consume the numbers at the markets [60]. Frequenting live poultry local food are at increased risk of hepatitis A, as seen with markets is not likely a common activity for travellers to VFR travellers originating from other intermediate and high China for the purpose of holiday or business. However, VFR risk countries [65]. The incidence of hepatitis E is highest in travellers are more likely to have close contact with the East and South East Asia, with the estimated seropreva- local population, use local facilities and eat local food [17], lence of 23% in China [66]. A hepatitis E vaccine is manu- compared to other travellers. It can be expected that many factured in China but not currently available outside China Chinese VFR travellers will visit wet markets during their [67]. return visit. Live poultry markets were the likely source of the 1997 4.2. Tuberculosis Hong Kong H5N1 outbreak [49]. More recently, H5N1 viruses were isolated from live poultry markets associated with China is considered a moderate incidence country for cases of human infection in Beijing and in the provinces of tuberculosis, with a high burden of multidrug resistant Guizhou, Hunan, and Xinjiang, suggesting a continuing link cases [27]. Whilst the risk to tourist and business travellers between live poultry markets and cases of human infection is generally low [27], the risk of acquiring tuberculosis has [61]. Also, during the SARS epidemic, the SARS coronavirus been shown to be greater for VFR travellers in general [7]. was isolated from caged animals in wet markets in Guang- Tuberculosis requires prolonged contact for transmission dong province, southern China [60]. Chinese wet markets [68], it is especially relevant to VFR travellers, who often are important not only for the transmission of newly have prolonged contact with the local population and emerged pathogens, many other important infectious dis- longer lengths of stay than tourist travellers [69]. Whilst eases, including bacterial and parasitic infections, can be VFR travellers may acquire tuberculosis during their acquired either when visiting the market, or during food travels, if such travellers present with tuberculosis it may preparation or consumption [60]. Whilst there have been no also be due to disease already acquired at the time of reported cases of infection via wet markets associated with immigration, and reactivated after immigration [10,69]. VFR travel, the visiting of wet markets should be considered a potential risk factor for various infections in Chinese VFR 4.3. Malaria travellers. Malaria is considered endemic in the rural parts of Hainan, 4. Other important infectious risks in China Henan, Yunnan, Fujian, Guangdong, Guangxi, Guizhou, Sichuan, Tibet (Zanbo Valley), Anhui, Hubei, Hunan, China is a middle income country with many infectious Jiangsu and Jiangxi provinces (see Fig. 2), but is not present disease risks that are uncommon in high income countries. in urban areas of China [70]. A 2012 study in five provinces While the risk to travellers of acquiring vaccine preventable affected by malaria in central China found that the inci- diseases in China’s major cities is relatively low [28], the dence rate for each province was 0.05 per 100,000 or less incidence of common vaccine preventable diseases, for [71]. The malaria species found in China is primarily Plas- example measles [62], are substantially higher than in most modium vivax, with P. falciparum common in select loca- high income countries. Therefore ensuring routine vacci- tions [72] with evidence of resistance to chloroquine and nations are up to date is an important consideration for mefloquine [72]. There are no known reports of malaria in travellers to China. Importantly, VFR travellers may have VFR travellers returning from China, and GeoSentinel Sur- different travel patterns to other tourists, placing them at veillance data between 1998 to November 2007 report no higher risk of acquiring certain infectious diseases than cases of malaria amongst travellers to China [73]. Despite those travelling for other purposes [11,17]. China is a vast this, the risk remains and chemoprophylaxis should be used country, with a diversity of infectious diseases risks across by travellers to malarious areas in Hainan, Yunnan, Anhui, different regions [28]. VFR travellers are more likely to Guizhou, Henan, and Hubei provinces, with recommended travel to rural or remote regions [11], and may require a regimens reflecting known drug resistance. Mosquito 290 T. Ma et al.

Fig. 2 Provinces where malaria has been reported [70]. Note that only certain rural areas are affected in each province. avoidance measures alone are recommended for travellers [74]. As the vector is also present in other provinces, there to all other malarious areas [72]. is the potential for further spread [75]. In the past three decades, there have been more than 650,000 reported 4.4. Dengue fever cases nationwide, with at least 610 deaths [74]. Dengue outbreaks now occur frequently in southern China, often as Dengue fever is found in Guangdong, Hainan, Guangxi, a result of the virus being introduced by travellers returning Fujian, Zhejiang, and Yunnan provinces in China (see Fig. 3) from Southeast Asia where dengue is endemic [75]. As there

Fig. 3 The provinces where dengue fever has been reported [74]. Chinese travellers visiting friends and relatives 291

Fig. 4 The four provinces where most typhoid cases occur [76]. is no vaccine, prevention is by mosquito avoidance and the north-eastern forests of China. Schistosomiasis is found vector management [75]. in focal areas especially in the Yangtze River basin, and Leptospirosis is found mainly in tropical areas. Chikungu- 4.5. Enteric fever (typhoid and paratyphoid) nya, leishmaniasis, filariasis and plague are found in certain regions of China [70]. While these regions are not common Enteric fever is endemic in China, but improvement in destinations for tourist travellers, VFR travellers are more sanitation has been associated with a sharp decline in likely than other travellers to visit rural and remote areas incidence [76]. In 2004, there were 3.9 cases of enteric where disease risk is higher. Strongyloidiasis, an intestinal fever (typhoid and paratyphoid) per 100,000 people nationally, with more than half of total reported cases in Guangxi, Guizhou, Yunnan and Zhejiang provinces (See Table 1 Potential infectious disease risks for travellers to Fig. 4) [76]. China is considered a medium incidence China [28,64,70]. country for typhoid [77,78]. Typhoid fever is a risk in areas Relevant for all travellers where hygiene is poor in China [28] and the typhoid vaccination is recommended for most travellers to China, and is Influenza (including Avian influenza) especially recommended for VFR travellers [27]. Measles Hepatitis A and B 4.6. Other infections Tuberculosis Relevant for travellers visiting certain regions only Several other infectious diseases may also pose an Japanese encephalitis increased risk to certain VFR travellers. Japanese Enceph- Hand, foot and mouth disease alitis is a risk for those travelling to certain rural areas [28]. Typhoid Rabies is a risk for those involved in outdoor activities in Rabies rural areas [28]. Rabies most commonly occurs in southern Malaria China, with an increase in the incidence of rabies in China Tick-borne encephalitis in recent years [79]. Hand, foot and mouth disease is Schistosomiasis common in parts of China and sporadic outbreaks occur Leptospirosis [64]. Poliomyelitis is considered eradicated in most of China Dengue Fever [28]. However, an outbreak in Xinjiang province in 2011 [64] Chikungunya highlights the remaining risk of re-introduction to remote Leishmaniasis and rural parts of China. Filariasis In addition, some diseases are found only in certain re- Plague gions of China (Table 1). Tick-borne encephalitis is found in 292 T. Ma et al. parasitic infection spread mainly by larvae penetrating the [2] Christian MD, Poutanen SM, Loutfy MR, Muller MP, Low DE. skin and mucous membranes, is also an emerging problem Severe acute respiratory syndrome. Clin Infect Dis 2004; in China, with rising incidence rates [80]. Immunocompro- 38(10):1420e7. mised patients are most often affected [81]. Infection can [3] Van Herck K, Van Damme P, Castelli F, Zuckerman J, be prevented by not walking barefoot and washing fruit and Nothdurft H, Dahlgren AL, et al. Knowledge, attitudes and practices in travel-related infectious diseases: the European vegetables thoroughly [80]. airport survey. J Travel Med 2004;11(1):3e8. [4] Breiman RF, Evans MR, Preiser W, Maguire J, Schnur A, Li A, 4.7. Vaccination recommendations et al. Role of China in the quest to define and control severe acute respiratory syndrome. Emerg Infect Dis 2003;9(9): In addition to the routine vaccines recommended in 1037e41. developed countries, including MMR and DTP, travellers to [5] Shortridge KF. Severe acute respiratory syndrome and influ- China should also consider hepatitis A vaccination, as it is enza: virus incursions from southern China. Am J Respir Crit Care Med 2003;168(12):1416e20. highly endemic in China. In addition, typhoid vaccination [6] United Nations World Travel Organization. UNWTO world should be considered for those travelling outside major tourism highlights. 2013. Edition 2013 [cited 2014 Jan 23]. cities, inactivated poliovirus vaccine is recommended for Available from: http://dtxtq4w60xqpw.cloudfront.net/ those who will visit Xinjiang province, and Japanese en- sites/all/files/pdf/unwto_highlights13_en_lr_0.pdf. cephalitis vaccination should be considered for those [7] Leder K, Tong S, Weld L, Kain KC, Wilder-Smith A, von staying in rural areas for extended periods during June to Sonnenburg F, et al. Illness in travelers visiting friends and September [28]. The CDC also recommends hepatitis B relatives: a review of the GeoSentinel surveillance network. vaccination for all travellers, and rabies vaccination for Clin Infect Dis 2006;43(9):1185e93. those who are planning outdoor activities especially in rural [8] Boggild AK, Castelli F, Gautret P, Torresi J, von Sonnenburg F, areas [70] and for those who will have contact with bats in Barnett ED, et al. Vaccine preventable diseases in returned international travelers: results from the GeoSentinel sur- Hong Kong [82]. veillance network. Vaccine 2010;28(46):7389e95. [9] Leder K, Black J, O’Brien D, Greenwood Z, Kain KC, 5. Conclusion Schwartz E, et al. Malaria in travelers: a review of the Geo- Sentinel surveillance network. Clin Infect Dis 2004;39(8): e Travel to and from China including VFR travel amongst 1104 12. [10] Monge-Maillo B, Norman FF, Perez-Molina JA, Navarro M, migrant ethnic Chinese populations in countries outside of Diaz-Menendez M, Lopez-Velez R. 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The visiting friends or relatives traveler in inform the control of travel-associated infectious diseases. the 21st century: time for a new definition. J Travel Med 2010;17(3):163e70. Travellers play a significant role in the spread of infectious [13] Center for Disease Control and Prevention. Chapter 8: diseases across international borders and responsible travel Advising travelers with specific needs. In: CDC Health Infor- through preventative practices and behaviour modification mation for International Travel 2014 [Internet]. USA: CDC; is crucial to the comprehensive control of infectious dis- 2014. Available from: http://wwwnc.cdc.gov/travel/ eases on a global scale. Research can inform preventive yellowbook/2014/chapter-8-advising-travelers-with-spe- strategies to effectively target Chinese VFR travellers to cific-needs/immigrants-returning-home-to-visit-friends-and- address their infectious disease risks, reduce the risk of relatives-vfrs. pandemics and the spread of diseases, and improve their [14] Wilder-Smith A, Khairullah NS, Song J-H, Chen C-Y, Torresi J. travel health outcomes. Travel health knowledge, attitudes and practices among Australasian travelers. J Travel Med 2004;11(1):9e15. [15] Lee VJ, Wilder-Smith A. Travel characteristics and health Conflicts of interest practices among travellers at the travellers’ health and vaccination clinic in Singapore. Ann Acad Med Singap 2006; 35(10):667e73. TEM has no conflict of interest to declare. AEH has received [16] Heywood AE, Watkins RE, Iamsirithaworn S, Nilvarangkul K, funding to conduct investigator-driven research from GSK MacIntyre CR. 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