Awareness and Practice of Pre-travel Vaccination Among International Travelers Departing from Addis Ababa Bole International Airport

Air transportation continues to increase over time,1 and international arrivals are forecasted to reach 1.8 billion by 2030.2 International tourist arrivals at Africa and Europe grew at a higher than average rate in 2017, with Africa having a 9% increment compared to 2016.3 International travel exposes individuals to new cultural, psychological, physiological, and microbiological experiences4; travelers are thus exposed to a variety of health risks in unfamiliar environments.5 Although the medical profession and the travel industry can provide extensive help and sound advice, it continues to be the traveler’s responsibility to seek information, understand the risks involved, and take the necessary precautions to protect their health while traveling.5 Travelers intending to visit a destination in any country should consult a travel medicine clinic or medical practitioner before their journey. This consultation should take place at least four to 8 weeks before the journey and preferably earlier if long-term travel or overseas work is envisaged.5 The traveler should be provided with a personal record of the vaccinations given using the international certificate for vaccination or prophylaxis (vaccination card).5 Travelers who are not aware of travel health services (such as pre-travel vaccination service) carry the risk of contracting or spreading infectious diseases. Travel-related infections have been documented in some countries. For example, on the 4th of November 2015, a 56-yearold German businessman was admitted to a hospital with acute renal failure following a cholera infection contracted during a http://ijtmgh.com Int J Travel Med Glob Health. 2020 June;8(2):58-65 doi 10.34172/ijtmgh.2020.10 TMGH IInternational Journal of Travel Medicine and Global Health J

three-day business trip to Manila, Philippines. 6 In 2017, the Chinese Centers for Disease Control and Prevention (CDC) documented a total of eleven imported yellow fever (YF) cases among male Chinese workers who returned to Beijing from Luanda, Angola. 7 Findings showed that none of the Chinese workers received a yellow fever vaccination prior to traveling to Angola. 7 In another study, vaccinations against rabies, typhoid fever, Japanese encephalitis, and meningococcus were highly inadequate for adolescents traveling from Greece to endemic areas. 8 Forty-seven countries in Africa and Central and South America are either endemic or have regions that are endemic for yellow fever. 9 Ethiopia is one of the African countries with risk of yellow fever transmission. 10 It also requires yellow fever vaccination for travelers arriving from countries with risk of yellow fever. 10 The United States Centers for Disease Control and Prevention (CDC) and the World Health Organization (WHO) recommend the following vaccinations for travelers visiting Ethiopia: hepatitis A, hepatitis B, typhoid, cholera, yellow fever, rabies, meningitis, polio, MMR (measles, mumps and rubella), DPT (diphtheria, pertussis, and tetanus), chickenpox, pneumonia, and influenza. 11 From this list, 3 vaccines (yellow fever, DPT, and influenza) are recommended for all travelers visiting Ethiopia. 11,12 Studies on pre-travel healthcare seeking practices and pretravel vaccinations have been conducted in many developed countries [13][14][15] and a few developing countries 16 ; however, such studies in Ethiopia are generally lacking. There is also a paucity of recent studies globally that compare the pre-travel vaccination status of travelers from developed countries with travelers from developing ones, leaving a gap that informed the internal comparison engaged in this study. Primary data was collected for this study in contrast to the secondary data (from travel clinics) used in previous studies. 13 -15 This study assessed the factors associated with the practice of pre-travel vaccination among travelers departing through Addis Ababa Bole International Airport after their stay in Ethiopia. The rate of vaccination card check at the points of entry of Addis Ababa Bole International Airport were also generated.

Study Design and Study Area
This cross-sectional study was conducted at Addis Ababa Bole International Airport. The airport is located in the Bole area, 6 km southeast of the city center and 65 km north of Debre Ziyet. Terminal II of the airport is dedicated to services for international travelers.

Study Population
The study population comprised international travelers departing from Ethiopia through the Addis Ababa Bole International Airport after their stay in Ethiopia.

Inclusion Criteria
International travelers 18 years and above were included in this study. The age limit was chosen because of the ethical need to acquire consent to participation from the parents/ guardians of minors who might not be traveling with them.

Exclusion Criteria
All passengers on transfer (Transfer passengers are those who change from one flight to another without leaving the airport during the process, while transit passengers are those who change from one flight to another or from one airline to another having had an overnight stay in the country) and those who could not read or write in either English or French (the two languages used for the data collection) were excluded. Ethiopian nationals were also excluded, because the vaccines 11 are recommended for foreigners visiting Ethiopia.

Sample Size Determination
The minimum sample size was determined using the Leslie Fischer's formula with the following assumptions: 95% confidence interval, 4% acceptable margin of error, and proportion (p) of awareness about pre-travel vaccination was taken as 46%. 17 The calculated sample size (596) was increased by 10% to compensate for non-response or improperly completed questionnaires. The value obtained (662) was then rounded up to 670 international travelers.

Sampling Technique
The lists of the international flights and their daily flight schedule for the month of January 2019, the month preceding the study period, were obtained from the commercial travel section of the Operation Unit of Addis Ababa Bole International Airport. The total number of travelers per WHO region for the month of January was computed by the researchers based on the flight schedule and used to project the expected volume of travelers' for the month of  19,20 A multistage sampling technique (involving stratified and simple random sampling) was used to select study participants. First, stratified random sampling and the proportion to population size approach were used to allocate the total sample size per WHO region to ensure the representativeness of travel destinations. The African region was further stratified into the West African, East African, Central African, and Southern African regions. Following stratification, daily data collection targets were set for the total sample size for each WHO region and the African sub-regions. Simple random sampling (using electronically generated random numbers) was then used to recruit subjects for the study according to the daily data collection targets and departure flight schedule.

Instrument for Data Collection and Data Collection Procedure
A questionnaire adapted from related previous studies 13,15,17 was used to collect relevant information. The questionnaire was prepared in the English language, translated to French, and then back translated to English to ensure consistency. The questionnaire was pre-tested prior to the commencement of the actual study, and items which were difficult to understand were reconstructed. Face validity was done by four experts who reviewed the questionnaire separately and answered on "how well the questionnaire measures the awareness and practice of pre-travel vaccination. " The reliability was evaluated using Cronbach's alpha statistics. The value of Cronbach's alpha was 0.821 (0.817, 0.913) for all items in the questionnaire.
The questionnaires were distributed at the departure lounges (near the respective departure gates) before boarding. Twelve staff members (2 per WHO region) of the airport were recruited for data collection and trained for three days. Travelers' vaccination cards were checked to confirm vaccination status whenever respondents (travelers) gave consent. The data collection process took 4 weeks to complete.

Data Management
The data obtained was entered into a computer using EpiData version 3.1 and exported to Statistical Package for the Social Sciences (SPSS), version 25, for statistical analysis. All questionnaires noticed with errors or missing variables were rejected during data entry. Vaccination status was classified as "vaccinated" or "not vaccinated" (vaccinated travelers were those who took at least one of the three vaccines recommended for all travelers visiting Ethiopia, 11,12 while those who did not receive any of the three vaccines were classified as not vaccinated). Bivariate analysis was done (using binary logistic regression) to assess the relationship between pre-travel vaccination status (dependent variable) and the independent variables. Before this step, variables too few to model were re-categorized to have an adequate sample size in each cell. Examples of such re-categorization were marital status, where the married were merged with divorced/separated/ widowed; and occupation, where casual workers were merged with part-time/full-time employment. The regions of Ethiopia were re-categorized as follows: Agrarian (Amhara, Tigray, and Oromia); Pastoralist (Somali, Afar, and Southern nations); Emerging (Gambela and Benishangul-Gumuz); and Cities (Addis, Harari and Dire Dawa). Only variables that were statistically significant during the bivariate analysis were included in the multivariable analysis. The level of statistical significance was set at P < 0.05. The odds ratios (crude and adjusted) were presented with a 95% confidence interval.

Results
A total of 639 valid questionnaires, with a response rate of 95.4%, were analyzed. The median age for all participants was 34 years with an interquartile range (IQR) of 28 to 41. Four hundred and twenty-seven respondents (66.8%) were males; 404 (63.2%) were married; 221 (34.6%) travelers had a postgraduate (masters, PhD or fellowship) level of Of the total respondents, 468 (73.2%) travelers stayed in Addis Ababa. Lengths of stay varied from less than 24 hours (58.5%) to more than 4 weeks (11.9%). The reasons why travelers came into Ethiopia included for work (15.6%), tourism (10.5%), and transit (52.9%) among others ( Table 2).
Of the total respondents, 580 (90.8%) were aware of pretravel vaccinations and 531 (83.1%) received pre-travel vaccinations before coming to Ethiopia. Two hundred and sixty-two (41.0%) took pre-travel vaccinations because it was the right thing to do and 74 (11.6%) because their employer recommended it. Some travelers did not take pre-travel vaccinations, because they did not find it to be important (5.2%) or because they were not aware of it (4.7%). Three hundred and three travelers (47.4%) reported that their vaccination cards were checked at other international airports during previous trips; however, only 185 (29.0%) had their vaccination cards checked upon arrival in Ethiopia. Though 426 (66.7%) of the total respondents accepted to show interviewers their international card of vaccination, only 413 (64.6%) eventually made their cards available for inspection ( Table 3).
Based on recommendations for all travelers visiting Ethiopia, 149 (23.3%) of the total respondents were categorized as not vaccinated, while 490 (76.7%) were vaccinated.
Multivariable analysis found that age, marital status, religion, and having vaccination cards checked in previous trips were all independently associated with vaccination status. Travelers aged 50 years and above were 5.372 times more likely to be vaccinated compared to those between 18 and 29 years at a P value of 0.047. Travelers in the married/ divorced/separated/widowed category were 2.346 times more likely to be vaccinated compared with travelers who were single at a P value of 0.035. Travelers with religions such as Judaism, Buddhism, Atheism, Hinduism, or no religion were 33.556 times more likely than Christians to be vaccinated at a P value <0.001. Travelers whose vaccination cards were not checked in previous trips were 68.4% times less likely to be vaccinated than travelers whose vaccination cards had been previously checked at a P value of 0.002 (Table 5).

Discussion
The rates of pre-travel vaccination in this study were similar to the rates obtained in previous similar travel surveys. The most commonly reported pre-travel vaccinations were hepatitis A, hepatitis B, tetanus, and typhoid. 21,22 Influenza vaccination was reported by 10.8% of travelers compared to <3% of travelers in a previous study. 23 The relatively satisfactory level of documented yellow fever vaccination (72.5%), the highest among the 14 vaccines studied, may indicate that travelers are more inclined to have the mandatory vaccinations. When compared to the study of Toovey et al, in which 60% of respondents were carrying vaccination certificates and a further 21% of respondents admitted to having no vaccination certificate with them, 17 the current study found that 64.6% of respondents were carrying vaccination cards, 1.9% reported that their vaccination cards were not with them, and 9.4% admitted to having no vaccination card. Every 8 out of 10 (83.1%) participants took pre-travel vaccinations. This finding was better than those of previous studies. For example, Maltezou et al assessed the preparedness of adolescents departing from Athens International Airport and found that only 15/68 (22%) adolescents received pretravel vaccinations. 8 This could be due to the fact that their study was conducted on a smaller sample (68 participants) compared with this index study which used 639 respondents. Also, the previous study was conducted among adolescents only, whereas the current study was conducted among adults aged 18 years and above. The finding from this study, however, is in keeping with the fact that bivariate analysis earlier established that travelers from developed countries were less likely to be vaccinated than travelers from developing countries ( Table 5).
The reasons for not receiving pre-travel vaccinations were not different from the reasons reported by Heywood et al. They also found that lack of information was among the main reasons for travelers not getting vaccinated. 24 Age and marital status were found to be associated with pre-travel vaccination status after controlling for the effects of other variables. The higher likelihood of travelers aged 50 years and above to be vaccinated contrasts with results of a study conducted among international travelers in Korea. They found that elderly travelers were less likely to be vaccinated. 25 The reason for non-vaccination among the younger age group in this index study may be explained by their risky health behaviors, phobia for needles, or cost of vaccination.
Travelers following a religion other than Christianity or Islam had a very high vaccination status. This could be explained by the fact that Christians and Muslims might prefer to rely on divine protection when they travel rather than vaccinations. Other studies reviewed, however, did not find any association between vaccination status and religion.
Despite the association of previous vaccination card check with vaccination status, only 29.0% of travelers reported that their vaccination cards were checked upon arrival in Ethiopia. This finding was not different from what was obtained in some other developing countries. For example, vaccination card checks upon arrival in Tanzania were non-systematic. 16 However, non-checking of vaccination cards at points of entry may lead to non-compliance of international travelers with international health regulations and the consequent risk of cross-border spread of diseases.

Limitations
Travelers who could not read or write in English or French were excluded, subjecting this study to selection bias. Selfreported information was used to assess pre-travel vaccination status, because the vaccination cards of some travelers were not available for verification, subjecting this study to recall bias.

Conclusion
This study revealed that the practice of pre-travel vaccination among international travelers is considerably low. Similarly, the uptake level of recommended vaccinations for all travelers, especially DPT and influenza vaccines, was low. Age, religion, marital status, and vaccination cards checked during a previous trip were all associated with pre-travel vaccination status.
The association of religion with vaccination status underscores the need for pre-travel vaccination counseling in churches and mosques as part of health education programs. It is also pertinent that the government of Ethiopia, through the Ministry of Health (Border Health), gear up vaccination card checks at the points of entry to the country. The Ministry of Foreign Affairs, through various Ethiopian embassies across the world, may need to make regulations to encourage travelers to get vaccinated with at least the three vaccines (yellow fever, DPT, and influenza) recommended for all travelers at the point of visa application. Researchers should  consider studies to model the risk of cross-border disease transmission among international travelers categorized as not-vaccinated.

Authors' Contributions
OSJ conceived of the study, organized airport access, and supervised data collection. All authors analyzed and interpreted the data. All authors were major contributors in writing the manuscript. All authors read and approved the final manuscript.

Conflicts of Interest Disclosures
The authors declare that they have no conflicts of interest.

Ethical Approval
Ethical clearance for this study was obtained from the Ethical Review Committee of the Addis Ababa University, Ethiopia.
The permission to carry out the study was obtained from the Airport Security Department through the Operation Manager of Addis Ababa Bole International Airport and also from the Head of the Ethiopian Food, Medicine, and Health Care Administration and Control Authority (EFMHACA). This study did not involve any physical/clinical examinations or investigations, and thus, the study did not pose any risk whatsoever to the participants (respondents). Written consent was obtained from each study participant before collecting information from them, and the respondents had the right to decline or withdraw from the study at any time. The participants were identified using serial numbers only to ensure confidentiality.

Funding/Support
This study was funded by the Postgraduate Academic Mobility for African Physician-Scientists (PAMAPS). The funding body had no role in the design of the study, the collection, analysis, and interpretation of data, or in the writing of the manuscript.