Vaccinations of International Travellers From Greece to Sub-Saharan Africa

During that past few decades, international travel has dramatically increased worldwide. The number of international tourists is expected to reach a total of 1.6 billion by the year 2020. Travel to Africa recorded a growth of 2%.1 International travels to tropical and subtropical countries may increase the risk of exposure to infectious diseases and may facilitate their global spread.2,3 Sub-Saharan Africa is one of the most common destinations (26.7%) where illnesses are acquired by travellers.4 A large proportion of imported infectious diseases to developed countries, including Greece, are related to Vaccine-Preventable Diseases (VPDs).5,6 VPDs account for 3% of febrile episodes. According to GeoSentinel data; typhoid fever, hepatitis A, and influenza A were the most common VPDs.6,7 Therefore, vaccine prophylaxis is an important measure of pre-travel advice. Risk assessment is based on travel variants such as destination, purpose, duration, area and place of travel and travellers’ variants including age, medical and vaccination history. Recommendation of vaccinations prior to travel is based on risk assessment and includes routine vaccines (vaccines recommended by the national immunization program), required vaccines, according to the International Health Regulation (IHR), and recommended vaccines.8 The current study aimed at assessing pre-travel preparation and provision of vaccinations to international travellers from Greece visiting http://ijtmgh.com Int J Travel Med Glob Health. 2017 June;5(2):46-52 doi 10.15171/ijtmgh.2017.10


Dear Editor
International air travel has increased during the recent century, and the number of pregnant women who travel internationally by air is on the rise.Most pregnant women are able to fly safely, but general considerations must be taken into account.Prior to traveling, pregnant women should be assessed for gestational age, fetus and placenta status, blood group and Rh status by laboratory evaluation or with diagnostic ultrasound imaging.The Center for Disease Control and Prevention (CDC) recommends that pregnant women travelers carry a copy of their medical records with them on their trip. 1 The latest recommendation of the ACOG indicates that occasional travel by air during pregnancy is safe.Specifically, occasional air travel by women with a singleton pregnancy can be done until 36 weeks gestation.Women with an uncomplicated multiple pregnancy are allowed to fly up to the end of the 32nd week.As emergencies usually happen in the first and third trimesters, the safest time to travel is probably the middle of the pregnancy, between 14-18 weeks. 2,3lmost all women with a normal pregnancy can travel without limitation up to 28 weeks, but there are few contraindications for air travel, including obstetric complications, severe anemia (Hb<7.5 g/dL), recent hemorrhage, sickle cell anemia, acute otitis media and sinusitis, uncontrolled cardiac or respiratory disease, and a post-operative condition as with recent gastrointestinal surgery. 3lthough air travel is safe, there are specific risks during pregnancy.The incidences of miscarriage and preterm birth are greater among flight attendants than the general population.Exposure to cosmic radiation is not hazardous to the fetus for the occasional pregnant air traveler.One other concern is venous thromboembolism for which flight duration is a key factor.Air travel of more than 4 hours at a time may increase the risk of venous thromboembolism, but this is a weak risk factor.Immobility during long flights can lead to such a condition. 4,5here are some general suggestions for the pregnant traveler to minimize the risk of an adverse outcome related to air travel during pregnancy.Before planning to travel, women should check the airline's policy about air travel during pregnancy.The traveler's seat belt should be closed during a flight, and unnecessary traffic should be avoided.Because of the necessity of take occasional walks, pregnant women should have an aisle seat to facilitate movement.Women should drink plenty of fluids to avoid dehydration.][3] sub-Saharan Africa.

Methods
In Greece, pre-travel vaccination prophylaxis is provided according to the national guidelines issued by the World Health Organization, the Hellenic Centre for Disease Control and Prevention, and the US Centers for Disease Control and Prevention guidelines. 9-11Routine vaccinations are administered according to the National Vaccination Program of Greece. 12These vaccinations include tetanus-diphtheria pertussis, hepatitis A, hepatitis B, measles-mumps-rubella (MMR), Haemophilus influenza type B, poliomyelitis, meningococcus serotype C, pneumococcus, human papilloma virus, tuberculosis (Bacillus Calmette-Guérin vaccine), influenza (for high-risk groups only), and rotavirus vaccines.Travel medicine services are provided by 57 public health departments which are the only designated yellow fever vaccination centres in the country.Rabies, typhoid, and cholera vaccines are exclusively delivered to these centres.Pre-travel services and vaccinations are not free of charge.
The inclusion criteria for participation in this questionnairebased study 13,14 included all adult (>18 years old) international travellers who attended to the public health departments travelling to sub-Saharan Africa from January 1, 2011 to December 31, 2014.The exclusion criteria included travelers who were 18 years of age or less and all those travelling to other destinations other than sub-Saharan Africa.The questionnaire included data in relation to travellers' demographics and medical history and travel variants such as age, gender, nationality, medical and immunization history, date of departure, destination, duration and purpose of travel, place (hotel, camping, local people's home), area of stay (urban or rural), and information about travel medicine services (vaccination, malaria prophylaxis and general preventive measures).The definition of urban accommodation was based on the population of the town.A town with population more than >5000 people was defined urban, whereas rural accommodation was defined as villages with populations less than 5000 or those areas residing in the countryside.A trip less than 1 month duration was considered as short-term travel, while a trip of over 1 month was defined as a long-term travel.
Documentation about proof of vaccination was provided by travellers.A written consent was requested from all participants.

Results
During the study period, 1768 international travellers visited sub-Saharan Africa.The participation rate among international travellers ranged from 75% to 80% per each public health department.The group not participating in the study was similar in terms of age and gender to the participating group.The overwhelming majority (1686 travellers; 95.4%) were Greek citizens with a mean age of 39.2 years (range: 0-82 years; SD: 12.8).International travellers sought pre-travel advice at a mean of 20.9 days (range: 0-336 days; SD: 24.2) before their departure.Their travel characteristics are shown in Table 1.Most travelers (1024 travellers; 57.9%) travelled for short periods of time.Work was the prevalent purpose of travel (1034 travellers; 58.5%).Most travellers stayed at a hotel (876 travellers; 49.5%) and in urban areas (1003 travellers; 56.7%).Nigeria was the most common destination followed by Kenya, Somalia, Tanzania, and Ghana, (15.7%, 10.9%, 8.9%, 8.2%, and 6.7%, respectively) (Table 2).Travellers VFRs accounted for 5.2% of all travellers.
Table 3 shows pre-travel vaccination rates.The yellow  to Appendix 2, no vaccination against hepatitis A was less frequent among recreation travellers compared to VFRs; OR = 0.304).The recommendation of tetanus, hepatitis A & B, poliomyelitis, rabies and meningococcal vaccines was statistically significantly associated with the purpose of travel (Table 5).These vaccines were more commonly recommended for recreational travellers.Lastly, tetanus, hepatitis A, and poliomyelitis vaccines were more frequently recommended to short-term travellers, whereas typhoid vaccine was recommended to long-term travellers.

Discussion
Travelling to tropical and subtropical destinations may increase the risk of exposure to infectious diseases including VPDs. 3,4,6,10Therefore, vaccination prophylaxis is an important part of pre-travel advice and may contribute to the reduction of the risk of VPDs.However, less than one third of those international travellers who are diagnosed with VPDs during travel, seek pre-travel consultation as shown by the GeoSentinel network data. 5uring 2011-2014, 1768 international travellers were studied who attended the public health departments.Although the current study represents only those travellers attending these departments and not the Greek travellers, overall during the same period, the number of travellers attending the few travel clinics available in Greece is very limited.The level of travel health counseling performance between the public health departments showed no difference.Those who travel to destinations where yellow fever vaccine is recommended or required, have to attend these departments since they are the only designated yellow fever vaccination centers in Greece.This fact is also true in regards to vaccination against rabies, typhoid, and cholera since these vaccines are also exclusively available at these departments.7][18][19] Therefore, as shown by the National Statistics Service data, the number of travellers seeking pre-travel advice is very few.
In the current study, the yellow fever vaccine was the most frequently administered vaccine, which is partially explained by the fact that the public health departments are the only yellow fever vaccination centers in Greece.Yellow fever vaccination is recommended to travellers with no history of previous immunization, either for destinations where yellow fever is endemic or where there is a current epidemic (e.g.recent epidemic in sub-Saharan Africa and current epidemic in Brazil) or for destinations which require a proof of vaccination.1]20 The typhoid vaccine was recommended to 30.9% of the travellers in our study.Typhoid fever was the most common VPD, according to GeoSentinel data which accounts for 47.6% of them. 5,21In Greece, half of the typhoid fever cases notified to the National Surveillance System of Greece (2004-2013), are travel related. 6,22However, no typhoid fever cases were reported in the Greek travellers visiting to the sub-Saharan Africa during the study period. 22Typhoid vaccination is recommended for high risk travelers in terms of exposure to typhoid, like those travelling for long-periods of time and those visiting friends and relatives. 23Although longer duration of stay in typhoid endemic areas increases the risk of acquiring typhoid fever, even during short visits of less than 1 week to hyper-endemic areas, risks may be seen. 24,25n this study, the typhoid fever vaccine was delivered to only 40% of long-term travellers and 24.5% of VFR travellers travelling to typhoid endemic fever areas.This is while destinations did not include hyper-endemic areas such as the Indian subcontinent. 24,25Unfortunately the poor awareness of travellers and the public health professionals about typhoid vaccination recommendations may be related to the low typhoid vaccine uptake, despite national guidelines. 13In the present study, hepatitis A vaccination was recommended to travellers with no history of previous immunization or to those with negative anti-HAV testing.However, hepatitis A vaccine was recommended to only 16.8% of all travellers who travelled to destinations of high endemicity for hepatitis A. This rate is lower compared to that shown in other studies in which hepatitis A constitutes the prevalent vaccine administered to travellers. 26Hepatitis A vaccination should be recommended to all those travelling to countries with high or intermediate risks of hepatitis A. 27,28 Hepatitis A infection constitutes one of the most common VPDs in international travellers. 5,6The relative risk of hepatitis A for travellers Research Highlights remains significant although there is up to 50 fold decrease of hepatitis A incidence in travellers during the last few years.This is due to the higher rates of pre-travel vaccination. 28In the current study the lower vaccination rates may be related to possible prior immunization or decline of vaccination due to last minute travelling.
Hepatitis B is also considered as a common cause of VPDs among international travellers. 5In the current study, hepatitis B vaccine was recommended to only 11.5% of the travellers which was lower compared to the rates of other studies (15%-44%). 29,30These low hepatitis B vaccination rates may be related to previous immunization of hepatitis B or the poor perception of the risk of hepatitis B infection. 12,30eningococcal vaccine was recommended to 14.1% of all travellers.Vaccination is generally recommended to travellers such as long-term travellers, expatriates, and those living in close contact with local people. 31In the current study, 35.5% of the travellers stayed in sub-Saharan Africa for over one month and 22.1% of them stayed with local people.The high costs of vaccinations or travellers' poor awareness about meningitis risk during travel to the meningitis belt in Africa may be the main reasons for poor vaccination rates. 32abies vaccination was administered to only 0.4% of all travellers.This was while 8.6% and 2.9% of all travellers reported engagement in outdoor activities and possible contact with animals, respectively.Pre-exposure rabies vaccination is recommended to people travelling to rural areas and those engaging in outdoor activities such as bicycling, hiking, camping, backpacking and to children. 31Lack of knowledge about the risks of rabies exposure of travellers and travel health consultants may be related to the low vaccination rates against rabies in this study, 33,34 as well as to last minute travelling. 35uring this study, vaccination rates against tetanus/ diphtheria which mainly concerned travellers over 18 years, were lower compared to those of a United States study. 26he risk of the acquisition of measles increases in people with no history of immunity against MMR and importation of the disease to countries where not endemic. 7Previous vaccination through the National Vaccination Program of Greece may be related to these low vaccination rates. 12Since the overwhelming majority of the travellers were from the Greek nationality, they had most probably been vaccinated according to the National Vaccination Program in the past.
In terms of purpose of travel, multiple multinomial logistic regressions showed that there is a statistically significant association between gender, nationality and duration of travel.The recommendation of tetanus, hepatitis A & B, poliomyelitis, rabies and meningococcal vaccines was statistically significantly associated with the purpose of travel and of tetanus, hepatitis A, poliomyelitis and typhoid vaccines with duration of travel.These correlations may have significance for advising future travellers.
The large number of participants studied in this research provided the opportunity to study a great range of travellers' and travel characteristics and to assess travel vaccine recommendations.However, lack of information regarding the travellers' pre-existing immunity against VPDs is considered as a limitation in the current study.A clear strength of this research is the prospective study of a large number of international travellers from 57 Public health departments, which are the designated yellow fever vaccine centers.

Conclusion
This research is a large prospective study of pre-travel vaccination recommendations to travellers from Greece visiting sub-Saharan Africa.The results of this study emphasizes the need for more selective and individualized vaccination recommendations based on careful risk assessment, taking in consideration not only the travel destination but also other travel characteristics such as duration and purpose of travel, area and place of stay, and travellers activities.Recommendations should be based on each individual's characteristics including previous immunization, age, underlying medical conditions, possible pregnancy and medication.Public health authorities should be looking for developing strategies in order to increase the awareness of travellers and health professionals about travelrelated health risks and their prevention in particular travelassociated VPDs.They should also promote safety, both for the traveller as well as for the community.

Table 1 .
Travellers' and Travel Characteristics Among 1768 International Travellers From Greece to Sub-Saharan Africa, 2011-2014

Table 4 ;
Appendix 2).Foreign citizens are less frequent among recreational and work travellers compared to VFRs (0.142 and 0.151, respectively;

Table 4 ;
Appendix  2).Vaccination against hepatitis A was more frequent among recreational travellers compared to VFRs (Table4) (according

Table 2 .
Country Destinations to Sub-Saharan Africa Among 1768 International Travellers From Greece, 2011-2014

Table 3 .
Vaccination Rates Among 1768 International Travellers From Greece to Sub-Saharan Africa, 2011-2014 a In accordance with the National Vaccination Program of Greece.b For second destination which was Southeast Asia.

Table 4 .
Purpose of Travel According to Gender, Nationality and Duration of Travel a

Table 5 .
Vaccination Rates According to Purpose and Duration of Travel