Malaria risk among travelers tends to decrease, but it remains a life-threatening risk at many destinations.1 Also in China, the incidence rate of malaria decreased from 126.41/100,000 to 1.94/100,000 between 1950 and 2000, but morbidity has increased since the early 2000s mainly in two provinces, Yunnan and Hainan.2 Recently, malaria infections have been imported by Chinese international travelers from areas such as sub-Saharan Africa to provinces where malaria had been uncommon for many years.3–5 To evaluate the reasons for the increasing number of imported malaria cases among returning Chinese travelers, we conducted an airport-based questionnaire survey in different geographic areas of the People's Republic of China.
Background. To address the lack of understanding in malaria prevention among Chinese international travelers, we have conducted knowledge, attitudes, and practices (KAP) study in five different Chinese geographic areas. This survey represents one part of the background information needed to analyze imported malaria.
Methods. Standardized questionnaires were distributed to Chinese international travelers in departure lounges at international airports in Guangzhou, Beijing, Shanghai, Qingdao, and Nanjing. The data were entered into the Epidata 3.1 (Jens M. Lauritsen, Odense, Denmark) and analyzed by the SPSS 12.0 statistical package (SPSS Inc., Chicago, IL, USA).
Results. Overall 2,495 completed questionnaires were collected from departing Chinese passengers; 1,573 were contributed by travelers who were going to malaria risk countries. More than half of all travelers spent less than 7 days to organize their trip abroad. Pre-travel medical advice was sought by 998 travelers (40.0%), 65.1% of them did so for 1–7 days before departure. Only 4.0% travelers received their knowledge from travel health providers. Among 389 travelers who were going to high malaria risk countries, only 18.0% realized that there is a high malaria risk in sub-Saharan Africa. Most travelers going to risk areas knew about personal protection measures against mosquito bites, but only 21.4% and 12.1% carried mosquito repellents or insecticides, respectively. Only 18.7% of the 1,573 potentially exposed travelers carried malaria tablets, all of them for self-treatment, none for prophylaxis.
Conclusion. KAP about malaria among exposed Chinese travelers is far from satisfactory. To reduce the rate of imported malaria, specific educational tools should be developed for those at high risk to make them understand and become compliant with chemoprophylaxis.
Similarly to other knowledge, attitudes, and practices (KAP) studies relating to malaria and travel health,6–8 our study was conducted from December 2009 to April 2010 in the departure lounges of five airports: the Guangzhou Baiyun International Airport, Guangdong province; the Capital International Airport, Beijing; the Pudong International Airport, Shanghai; the Qingdao International Airport, Shandong province; and the Nanjing International Airport, Jiangsu province. Health quarantine staff at these airports distributed questionnaires to Chinese international travelers over 16 years of age with destinations in malaria endemic and nonmalarious countries. These questionnaires were derived from the ones used in previous studies,9,10 and were translated into Chinese, tested for ease of comprehension with a limited number of travelers. Further adjustments were made to the questionnaire to accommodate for the different educational backgrounds of our travelers. As travelers may visit destinations anywhere in the countries visited, only countries were evaluated in this survey; the exact location within the country was not investigated in the questionnaire.
We divided the total population into two groups, those with destinations in malaria risk countries and those in malaria-free countries (control group). Malaria risk destinations were defined according to the latest Centers for Disease Control and Prevention (CDC) “Yellow Book” also taking into account malaria-free areas within the destination countries.11 The high-risk endemic areas refer to all the countries that are listed “all areas with malaria” in the section “malaria risk information and prophylaxis, by country”; however, we labeled countries as low-risk endemic areas in which only parts are endemic for malaria. Nonmalarious areas refer to the countries that are marked with “none” in that list.11
The questionnaires were collected from the travelers before they boarded the plane. Data were entered into the Epidata 3.1 (Jens M. Lauritsen, Odense, Denmark) and analyzed with the SPSS 12.0 statistical package (SPSS Inc., Chicago, IL, USA). The data were analyzed with descriptive statistics and chi-square test.
Overall, 2,560 questionnaires were collected, 65 were incomplete and not included in our study. So, 2,495 (97.5%) questionnaires were included; the five international airports each contributed between 391 and 629 questionnaires. The travelers had destinations in 80 countries, including 39 malaria endemic countries. All respondents were Chinese nationals with a male/female ratio of 1.55:1, of whom 2,274 (91.1%) could access the Internet without difficulty (Table 1).
|≥ 60 y||44||1.8|
Among 2,495 respondents, 1,036 (41.5%) were on their first trip and 1,459 (58.5%) had previously been abroad. The purposes of travel were tourism/holiday for 48.7%, business/work abroad for 24.9%, visit to family/friends for 10.6%, research/education for 9.8%, missionary/religious/volunteer accounted for 1.3%, and other for 4.7%. Most travelers were accompanied by a partner, their spouse, friends, colleagues, children, or other team members, while 26.7% traveled alone. While 2,069 (82.9%) travelers declared that they would stay in cities, 121 travelers (4.8%) would travel in rural areas. Among the 527 (21.1%) who intended to backpack, 285 (54.1%) were on their first trip. High and low malaria risk destinations were visited by 1,573 (63.0%) travelers, risk-free countries by 922 (37.0%) travelers. Table 2 describes duration of stay in various risk areas.
|Destinations||Duration of travel (days)|
|High malaria risk countries||164 (42.1%)||77 (19.8%)||17 (4.4%)||131 (33.7%)||389 (15.5%)|
|Low malaria risk countries||708 (59.8%)||215 (18.2%)||49 (4.1%)||212 (17.9%)||1,184 (47.5%)|
|Malaria-free countries||362 (39.3%)||130 (14.1%)||42 (4.6%)||388 (42.0%)||922 (37.0%)|
|Total||1,234 (49.5%)||422 (16.9%)||108 (4.3%)||731 (29.3%)||2,495 (100%)|
Malaria Knowledge, Attitudes and Practices of the Travelers
In the malaria risk group, 833 (53.0%) travelers spent less than 1 week to prepare their trip, 395 (25.1%) spent 1–2 weeks, 196 (12.5%) spent between 2 weeks to 1 month, 65 (4.1%) spent between 1–2 months, and 84 (5.3%) spent longer than 2 months; in the control group the numbers and proportions were 415 (45.0%), 189 (20.5%), 163 (17.7%), 58 (6.3%), and 97 (10.5%), respectively. Thus, travelers going to malaria-free destinations spent significantly more time in planning their travel (χ2 = 50.619, p < 0.001). However, among the 527 backpackers, the preparation period was 64 and 169 days, for the risk-free and at risk countries, respectively.
Among all 2,495 respondents, 1,951 (78.2%) tried to get travel health information before departure. The most common resources were the Internet (32.5%), travel agencies (27.6%), and families/friends (25.6%). Overall, 998 (40.0%) sought a travel health consultation, 65.1% and 21.0% of them did so for 1–7 days and 8–14 days before departure, respectively. The reasons why other travelers did not consult travel health professionals are listed in Table 3. There was no significant difference between the malaria risk and risk-free groups.
|Risk group||Malaria exposure||No malaria risk||Total number|
|Too busy||198 (22.3%)||129 (21.2%)||327 (21.8%)|
|I know what to do||325 (36.6%)||206 (33.8%)||531 (35.5%)|
|No visit to dangerous place||296 (33.3%)||216 (35.5%)||512 (34.2%)|
|Others||69 (7.8%)||58 (9.5%)||127 (8.5%)|
|Total||888 (100%)||609 (100%)||1,497 (100%)|
Travelers to malaria endemic areas learned details about the infection from different sources, the main ones being family and friends (114; 7.2%) and the Internet (105; 6.7%). Only 63 (4.0%) travelers received their knowledge from travel health providers, and 181 (11.5%) received information from other medical providers. However, 905 (57.5%) of the 1,573 exposed travelers declared that they had received no information about malaria. The travelers' risk perception for their destination is shown in Table 4.
|High-risk countries||Low-risk countries||Risk-free countries|
|Do not know||206||53.0||745||62.9||543||59.0||1,494|
Personal protection measures against mosquito bites chosen by travelers to malarious areas are listed in Table 5. A significant difference between the two groups was only noted with respect to indoor measures.
|Measure||Control group N = 922||%||Risk group N = 1,573||%||Total number N = 2,495||%||χ2||p|
|Outdoor||Cover arms and legs||736||79.8||1,213||77.1||1,949||78.1||2.502||0.120|
|Use mosquito repellent||583||63.2||976||62.0||1,559||62.5||0.348||0.578|
|Sleep under mosquito net||342||37.1||654||41.6||996||39.9||4.872||0.028|
|Turn on air conditioning||412||44.7||801||50.9||1,213||48.6||9.050||0.003|
Among 1,573 travelers whose destinations were malaria endemic countries, 336 (21.4%) carried a mosquito repellent, 191 (12.1%) an insecticide, and 134 (8.5%) a mosquito net. Also, 291 (18.5%) carried malaria medication; these were 209 (17.7%) in the low-risk group and 82 (21.1%) in the high-risk group (χ2 = 2.282, p = 0.131). Mostly, these were chloroquine, doxycycline, and artemisinin; some of the travelers carried more than one brand of tablets. Table 6 lists the reasons for not carrying malaria tablets. Acceptance of malaria treatment in case of illness overseas was high: 1,278 (81.2%) would seek medical care abroad.
|Do not know||Do not like to take||Mosquitoes do not bite me’||Allergic to tablets||Disease is not dangerous||Cost||Tablets not effective||May get side-effects||Other|
|Number of travelers||706||322||35||29||26||23||21||9||108|
All respondents were asked to identify the symptoms of malaria. Most of the travelers in the risk group (1,129; 71.8%) and the control group (635; 68.9%) knew that fever is one of the malaria symptoms (not significant).
All respondents of this survey were Chinese international travelers. However, we cannot generalize for all of China due to sample and geographic limitations, and some potential bias exists with respect to different interpretation of the questions among travelers of various educational backgrounds. The information indicates that the current Chinese style of travel focuses on short-term city touring. The travel habits of Chinese are similar to those of other Asian travelers, as illustrated in the surveys on Japanese and Australasians.7,10 Although most people preferred cities, there were still more than 20% who intended to go backpacking.
In this survey, the proportion of travelers to different malaria risk countries were different with travel duration (Table 2), and most travelers visited destinations with low or no malaria risk.
Overall, the preparation period was short and surprisingly, the control group spent more time to prepare the trip, though backpackers in the risk group had a longer preparation time. These short preparation times are considered to be associated with short urban itineraries, a preference for group tours and resort accommodations arranged by travel agencies, and also business trips arranged by companies at very short notice. The reasons that persons traveling to non-malaria areas spent more time getting pre-travel advice compared to those traveling to malaria areas, are not clear. Lack of knowledge about the danger and risk of infection resulting due to lack of seeking pre-travel medical advice may be one of the reasons.
Imported malaria cases have been increasing in 22 provinces since 1980; the cases accounted for even more than half of all reported cases among some lower endemic provinces in 2008.12 However, there has been little information about KAP on malaria among Chinese international travelers. Although the rate of malaria awareness among the travelers of this survey is higher than the rate among local Chinese citizens,13–18 it is still lower than the national goal,17–21 and lower than the rates in Japanese, Australasian, and western international travelers7,8,10 as well.
Our data revealed that most travelers (78.2%) tried to get travel health information before departure. Because of convenient access to the Internet, online search was a more common method for getting travel health information as compared to visiting a medical provider. Travel medicine providers in China served only a very small proportion of travelers with malaria risk exposure (4.0%), a much lower proportion than among other Asians (26.0%).7 The results of this survey showed a high level of ignorance among travelers for the need of seeking pre-travel medical advice and travel health preparedness. But the details about type and quality of the websites consulted by the travelers were not subjected to this survey. Lower proportion with travel health consultation should be related to lower perception for need to seek pre-travel advice. Lower perception for the need to seek pre-travel advice should be related to lower percentage of travel medical consultation.
There were no significant differences between the groups with regards to outdoor personal protection measures against mosquito bites. Knowledge appeared to be rather good in both groups, probably based on common sense for mosquito prevention. In contrast there were significant differences with respect to some indoor measures, such as sleeping under a mosquito net, using air conditioning and products, coils, or insecticides. Only few among those at risk of malaria seemed unaware that perfumes and deodorants could attract mosquitoes and thus would not abstain from their use. Nevertheless, the vast majority of the travelers did not carry anything against mosquito bites. The relationship between a mosquito bite and malaria apparently was not considered by a majority of travelers. It reflects a Chinese proverb, which says theory does not always translate into practice.
The proportion of those carrying antimalarial medication was low, but the highest rate was among the high-risk group. It appears that these travelers paid more attention to malaria prevention, even though, overall, the target population had a poor recognition of malaria endemic areas. Owing to limitations of supply in the Chinese medication market, our survey focused only on chloroquine, doxycycline, and artemisinin. While Japanese travelers were often concerned about side-effects,10 that was rarely an issue for Chinese travelers.
Some of the respondents declared that the antimalaria tablets were to be used for malaria prevention and/or standby treatment, but none of them were taking preventive medication correctly before departure. This result was consistent with the results of surveys among Chinese laborers.7 In comparison, the rates among US, Asian/Australian, and Japanese travelers using chemoprophylaxis were 46.2%,6 41.7%,7 and 20.0%, respectively.10 Further investigation detected some confusion about the concepts of prevention and treatment. Some of the travelers seemed to be misled, as they were told that if any one in a group had a “presumed” case of malaria, the standby treatment doses had to be taken by the entire group for prevention of an outbreak. This reflects that the general practitioners may lack training and knowledge of travel medicine.
Some travelers thought that in case of illness visiting a physician would be better than self-treatment. This belief matched the high acceptance of malaria treatment in case of infection during the trip.
In conclusion, over the last 10 years, Chinese outbound travel and export of labor services have grown dramatically. Our data indicate a profound lack of KAP with respect to prevention of malaria in at-risk travelers. There is an urgent need for public education in malaria prevention for this population; also it must become a common knowledge that pre-travel health consultations are essential. Additionally, professional training of medical providers in travel medicine must be intensified. Moreover, more research is needed to develop effective measures to improve malaria prevention among Chinese international travelers.
We thank Ms Assunta Marcolongo of IAMAT for her encouragement during the survey. We appreciate and thank all CIQ staff members at the international airports for their contributions. Data entry was performed by a working group at Guangdong International Travel Healthcare Center (GD ITHC).
Declaration of Interests
The authors state they have no conflicts of interest to declare.